@prefix vivo: . @prefix edm: . @prefix ns0: . @prefix dcterms: . @prefix dc: . @prefix skos: . vivo:departmentOrSchool "Science, Faculty of"@en, "Botany, Department of"@en ; edm:dataProvider "DSpace"@en ; ns0:degreeCampus "UBCV"@en ; dcterms:creator "Kim, Jeong Ha"@en ; dcterms:issued "2009-04-15T21:26:20Z"@en, "1995"@en ; vivo:relatedDegree "Doctor of Philosophy - PhD"@en ; ns0:degreeGrantor "University of British Columbia"@en ; dcterms:description """This study is a comprehensive and experimental approach to understand the dynamics producing structure in an intertidal algal community. Both biological factors (competition and herbivory) and physical factors (disturbance and physical stress) were investigated through field manipulative experiments, non-manipulative monitoring and laboratory experiments for the last 3 years in Barkley Sound, Vancouver Island. The community studied contains three dominant perennial macroalgae, Mazzaella cornucopiae (Rhodophyta), Fucus distichus and Pelvetiopsis limitata (Phaeophyta), and some ephemeral algae as well as coexisting invertebrates such as barnacles, limpets and snails. Biological interactions and their mechanisms for all these organisms turned out to be complicated and non-hierarchical interaction networks which include reversal of dominance and indirect interaction. There was evidence for both negative and positive interactions existing between the same pair of species. Competitive dominance was changed depending on the developmental stages of the competitors and due to differences in morphology, and also the outcomes of interactions were modified by physical stresses (i.e., desiccation and wave action). Snails preferentially grazed the red alga, and limpets reduced the abundance of the ephemeral algae (the early colonizers) which otherwise inhibited the settlement of the later successional species such as the fucoids. Barnacles facilitated the colonization of Fucus and ephemeral algae after disturbance. Responses of the three dominant algae and ephemerals to the different sizes and time of disturbance were species-specific and depended on the alga’s life history and reproductive characteristics. The study shows that both the biological and physical factors influenced the structure of this community, and that the non-hierarchical interactions among the major species and their well-balanced responses to disturbance support a high likelihood of maintaining the current diversity in this algal community."""@en ; edm:aggregatedCHO "https://circle.library.ubc.ca/rest/handle/2429/7148?expand=metadata"@en ; dcterms:extent "3803496 bytes"@en ; dc:format "application/pdf"@en ; skos:note "Intertidal community structure, dynamics and models: mechanisms andthe role of biotic and abiotic interactionsbyJeong Ha KimB.Sc., Sung Kyun Kwan University, 1984M.Sc., Western Illinois University, 1988A THESIS SUBMITTED IN PARTIAL FULFILLMENT OFTHE REQUIREMENTS FOR THE DEGREE OFDOCTOR OF PHILOSOPHYinTHE FACULTY OF GRADUATE STUDIES(Department of Botany)We accept this thesis as conformingto the required standardTHE UNIVERSITY OF BRITISH COLUMBIAJune 1995© Jeong Ha Kim, 1995In presenting this thesis in partial fulfilment of the requirements for an advanceddegree at the University of British Columbia, I agree that the Library shall make itfreely available for reference and study. I further agree that permission for extensivecopying of this thesis for scholarly purposes may be granted by the head of mydepartment or by his or her representatives. It is understood that copying orpublication of this thesis for financial gain shall not be allowed without my writtenpermission.(Signature)____________________________Department of_________________The University of British ColumbiaVancouver, CanadaDateb (9DE-6 (2/88)11ABSTRACTThis study is a comprehensive and experimental approach to understand thedynamics producing structure in an intertidal algal community. Both biological factors(competition and herbivory) and physical factors (disturbance and physical stress) wereinvestigated through field manipulative experiments, non-manipulative monitoring andlaboratory experiments for the last 3 years in Barkley Sound, Vancouver Island. Thecommunity studied contains three dominant perennial macroalgae, Mazzaellacornucopiae (Rhodophyta), Fucus distichus and Pelvetiopsis limitata (Phaeophyta), andsome ephemeral algae as well as coexisting invertebrates such as barnacles, limpets andsnails. Biological interactions and their mechanisms for all these organisms turned out tobe complicated and non-hierarchical interaction networks which include reversal ofdominance and indirect interaction. There was evidence for both negative and positiveinteractions existing between the same pair of species. Competitive dominance waschanged depending on the developmental stages of the competitors and due to differencesin morphology, and also the outcomes of interactions were modified by physical stresses(i.e., desiccation and wave action). Snails preferentially grazed the red alga, and limpetsreduced the abundance of the ephemeral algae (the early colonizers) which otherwiseinhibited the settlement of the later successional species such as the fucoids. Barnaclesfacilitated the colonization of Fucus and ephemeral algae after disturbance. Responses ofthe three dominant algae and ephemerals to the different sizes and time of disturbancewere species-specific and depended on the alga’s life history and reproductivecharacteristics. The study shows that both the biological and physical factors influencedthe structure of this community, and that the non-hierarchical interactions among themajor species and their well-balanced responses to disturbance support a high likelihoodof maintaining the current diversity in this algal community.111TABLE OF CONTENTSPageAbstract.iiTable of Contents iiiList of Tables viiList of Figures viiiAcknowledgments xiCHAPTER 1: Thesis introduction 1General Introduction 1The study site and community 4Organization of the thesis 6REFERENCES 7CHAPTER 2: Patterns of interactions among neighbor species in a high intertidal algalcommunity 101NTRODUCTION 10METHODS 14Experiment 1: The relationship between Mazzaella cover andfucoidrecruitment 14Experiment 2: Effects ofpruning Mazzaella turfonfucoid recruitment15Experiment 3: Effects ofMazzaella turfon post-recruitment survivorshipofflicoids 16Experiment 4: Effects offucoids on Mazzaella comucopiae 17RESULTS 21The relationship between Mazzaella cover andfucoid recruitment 21Effects ofpruning Mazzaella turf on fucoid recruitment 21Effects of Mazzaella turf on post-recruitment survivorship offucoids ... 22ivEffects offucoids on Mazzaella cornucopiae.23DISCUSSION 24The complexity ofalgal interactions among the three dominants 24The mechanism ofpositive interaction and neighbor distance 27Coexistence of the major species: Biological perspectives 30REFERENCES 33CHAPTER 3: Preferential feeding by a littorinid: implications for its role in a highintertidal algal community 50INTRODUCTION 50MATERIALS AND METHODS 52Sampling site and organisms 52Natural densities ofsnails 53Single-diet experiments 54Multiple-diet experiments 56Snail behaviors and tide/light effects 57RESULTS 58Natural densities ofsnails 58Single-diet experiments 58Multiple-diet experiments 59Snail behaviors and tide/light effects 60DISCUSSION 61REFERENCES 65CHAPTER 4: The effect of barnacles and limpets on algal succession 75INTRODUCTION 75METHODS 78Experimental design 78Data analysis 80VRESULTS. 81DISCUSSION.83Models and the herbivore role in algal succession 83Direct and indirect interactions during succession 85REFERENCES 88CHAPTER 5: Effects of size of experimental clearings and season of clearing on algalpatch recovery 100INTRODUCTION 100METHODS 104Experimental design 104Data analysis 105RESULTS 106Unmanipulated plots 106Size effects ofdisturbance 107Seasonal effects of disturbance 108Interactions of the disturbance factors 109Barnacle and limpet densities 110DISCUSSION 110Size effects ofdisturbance 110The effect of timing ofdisturbance 113Responses ofbarnacles and limpets to the size ofdisturbance 114Responses of individual algal species to disturbance 115REFERENCES 117CHAPTER 6: Predictive models for community structure following environmentalchanges 129THE MECHANISMS AND COMPLEXITY OF SPECIES INTERACTIONS129viPREDICTIONS OF THE EFFECTS OF ENVIRONMENTAL IMPACTS ON THECOMMUNITY STRUCTURE 133Case 1: Absence of limpets in the system 134Case 2: Absence ofMazzaella in the system 134Case 3: Absence ofFucus in the system 135Case 4: No Mazzaella when a small/medium (e.g., 25- 100 cm2)gap isformed in summer 136Case 5: No limpets when a large gap (e.g., 400 cm2) is formed in winter137REFERENCES 139APPENDIX A: ANOVA tables for natural densities of snails from Chapter 3 144APPENDIX B: Supplementary data and results from other studies in Chapter 4 145viiLIST OF TABLESPageTable 2.1 Results of ANCOVA on fucoid recruitment in the different Mazzaellapruning plots. The ANCOVA was applied to each sampling date. The covariateis Mazzaeila percent cover in each plot (M-cover). Three treatments are ‘totalpruning’, ‘partial pruning’ and ‘no pruning’ (control), see text for details 38Table 2.2 Comparisons of longevity among the distance groups in each species andbetween F. distichus and P. limitata at each distance group. Means are numberof months 39Table 2.3 Results of multivariate statistics as a preplanned multiple comparison fortesting three hypotheses. A Bonferroni adjusted probability value (p=O.O5 /4=0.0 125) was used to compare each pair of treatments 40Table 3.1 Single-diet experiments. Results of three-way ANOVA, a Snail x Algae xTime (2x3x2), with repeated measures on the Time factor 68Table 3.2 Effects of light and tide on snail behavior. Results of a two-way ANOVAwith repeated measures on both light (2) and tide (2) factors. A separate analysiswas applied on each sampling date (Days 1, 4, 7) during the multiple-dietexperiment 69Table 4.1 The mean density ±SE (in 20x20 cm plot) of barnacles and limpets in eachnon-excluded treatment. Data are the mean of 14 sampling dates (April 1992 -August 1994; December 1993 data are missing), in each sampling date thedensity of barnacles and limpets was averaged from the 4 replicate plots 91Table 4.2 The mean percent cover of the five most abundant ephemeral algae in eachtreatment. Data are the mean of 13 sampling dates (February 1992- February1994), in each sampling date the percent cover value of each species wasaveraged from the 4 replicate plots 92Table 5.1 The effect of size of experimental clearings (5x5 and 1 Ox 10 cm) on total algalcover. A separate repeated measures analysis of variance was applied on datafrom each season. Large plots (20x20 cm) were not included in analysis, asdiscussed in text 120Table 5.2 The effect of size and season of experimental clearings on recolonization ofthe three dominant algae, Fucus, Pelvetiopsis, Mazzaella, and the fugitive algalgroup. Repeated measures ANOVA was applied to 16 months of data. Largeplots (20x20 cm) were not included in analysis as discussed in text. All datawere arcsine transformed prior to analysis 121Table A.1 Summaries of ANOVAs on the natural density of snails at Prasiola Point. A.Densities of snails in monospecific patches of the three dominant algae. B.Densities of snails in general habitats (3 transect lines) 144viiiLIST OF FIGURESPageFigure 1.1 Location of study sites. A = Nudibranch Point. B = Prasiola Point 9Figure 2.1 Correlations of M. cornucopiae percent cover and number of fucoid recruits.41Figure 2.2 The effect of Mazzaelia turf on fucoids after recruitment stage. Curves arethe weighted average of plots 42Figure 2.3 Relationship between the size class of Mazzaella blade and wet weight (g).Mazzaella blade height was divided into six 5 mm size classes (SC). SC1 = 1-5mm, SC2 = 6-10 mm, SC3 = 11-15 mm, SC4 = 16-20 mm, SC5 = 21-25 mm,SC6 >26 mm 43Figure 2.4 The effect of pruning Mazzaella blades on Mazzaella percent cover in thesame experimental plots (lOxlO cm) 44Figure 2.5 The effect of Mazzaella pruning on fucoid recruitment. A. Number offucoid recruits actually occurring in the plots. B. Number of fucoid recruitsadjusted by Mazzaella percent cover (the covariate) in each plot at each samplingdate. These values were used in the ANCOVA. Data are means +SE of 9replicates. PT for Pelvetiopsis in the total pruning plots, PP for Pelvetiopsis inthe partial pruning plots, PC for Pelvetiopsis in the control plots; FT, FP and FCfor Fucus in the respective plots 45Figure 2.6 Changes in Mazaella biomass (g) under each treatment after 2 months.CTL for control, CLE for the clear artificial plant, DRK for the dark artificialplant, FUC for Fucus, and PEL for Pelvetiopsis. Data are means ÷SE (n=5 forCLE, FUC and PEL, n=6 for DRK, n=7 for CTh) 46Figure 2.7 The effect of fucoid shading on Mazzaella size class. Data are means +SE(n=5 for clear and n=6 for dark artificial plant) 47Figure 2.8 Diagram of potential factors affecting fucoid mortality. See DISCUSSIONfor further explanation 48Figure 2.9 Fucus survivorship curves in relation to the changing effects of competitionand physical stress with distance from the edge of a Mazzaella turf. The shadedarea represents the probability of Fucus survival 49Figure 3.1 Natural densities of snails at Prasiola Pt. Data are means +SE of 5monospecific patches of each alga and of 18 randomly selected plots fromtransect lines in the general habitat (3 transects x 6 points). GEN for the generalhabitat, MAZ for M. cornucopiae, FUC for F. distichus, PEL for P. limitata. ... 70Figure 3.2 Single-diet experiments. 3.0±0.02 g of thallus was used per cage. Positivevalues indicate weight gain. Negative values indicate weight loss. Data aremeans +SE of five treatments and three controls. MAZ, M. cornucopiae, FUC,F. distichus, PEL, P. liinitata 71Figure 3.3 Results of the multiple-diet experiment. The comparisons of weight loss (g)between treatments and controls and among algal species. 1±0.02 g of each algalixspecies were placed making —3.0 g (total) of food per cage. Data are means +SEof fourteen treatments and seven controls. MAZ, M. cornucopiae, FIJC, F.distichus, PEL, P. limitata 72Figure 3.4 Behavioral choice (attractiveness) of Littorina sp. towards the three algalspecies. Densities of snails attached to the thalli of each algal species 15 mmafter the multiple-diet experiment started. Data are means +SE of sixteenreplicates. See Fig. 3.2 for caption comments 73Figure 3.5 Tidal and light effects on snail movement towards food during the multiple-diet experiment. The data shown are the number of snails attached to M.cornucopiae for every tidal and light condition. Tide/light combinations arepresented in the same order as simulated in the lab. Data are means +SE ofsixteen replicates 74Figure 4.1 Effects of barnacle and limpet removal on each algal group. Data are means± SE of four replicates. +B+L indicates both barnacle and limpet present, -B+Lbarnacle absent, limpet present, +B-L barnacle present, limpet absent, and -B-Lboth barnacle and limpet absent 93Figure 4.2 Effects of barnacles and limpets on algal species interactions in eachtreatment. EPH for ephemeral algae, MAZ for Mazzaella cornucopiae, FUC forFucus distichus, PEL for Pelvetiopsis li,nitata. Data are means ± SE of fourreplicates 95Figure 4.3 The abundance of barnacles and limpets in the experimental plots (20x20cm). Data are the mean densities ± SE per plot (n=4) 97Figure 4.4 A summary of barnacle and limpet effects on algal succession. Dominantalgae were shown in each experimental condition with their relative abundance. 98Figure 4.5 The summary of direct and indirect interactions shown between barnacles,limpets, fucoids and ephemeral algae in this study 99Figure 5.1 Seasonal changes of algal percent cover and the number of fucoid recruits inunmanipulated plots (20x20 cm) at Prasiola Point for two years. Data are themean ±SE of four replicates. EPH for ephemeral algae, MAZ for Mazzaellacornucopiae, FUC for Fucus distichus, PEL for Pelvetiopsis liinitata 123Figure 5.2 Recolonization of total algae in three different sizes of clearing. Largeclearings = 20x20 cm, medium clearings = lOxlO cm, small clearings = 5x5 cm.Plots cleared in the summer (August 1991) were only compared for the sizeeffect on patch recovery. Data are the mean ±SE of fifteen replicates for smalland medium plots and of four replicates for large plots 124Figure 5.3 Patch recovery of each dominant algae, Mazzaelia, Fucus, Pelvetiopsis, andephemeral algae in three different sizes of clearing. Data shown are from thesummer-cleared (August 1991) plots. Data are the mean ±SE of fifteenreplicates for small and medium plots and of four replicates for large plots 125Figure 5.4 The effect of season of clearing on algal recovery of each species in smallplots (5x5 cm). The time for each seasonal clearing is August 1991 (forsummer), October 1991 (for fall), February 1992 (for winter) and April 1992 (forspring). Data are the mean ±SE of fifteen replicates 126xFigure 5.5 The effect of season of clearing on algal recovery of each species in mediumplots (lOxlO cm). See Fig. 5.4 for captions and the number of replicates 127Figure 5.6 Barnacle and limpet densities in the three sizes of patch at three samplingdates (4, 10, 16 months after clearing). Data are the mean ±SE of fifteenreplicates for small and medium plots and of four replicates for large plots.When results of ANOVA on three sizes were significant, results of Tukey’s HSDtests were labeled (e.g., LM indicates that density in small patch issignificantly greater than that of either large or medium patch). N/S for p>0.05.128Figure 6.1 The summary of interactions among the major component organismsshown in this study. PEL and FUC in the upper diagram indicate Pelvetiopsisand Fucus at the recruitment stage, while those in the lower panels indicate thefucoids after recruitment stage. Small letters are the abbreviations for types ofinteraction: (co) for competition, (fa) for facilitation, (gr) for grazing, (ov) forovergrowth, (pr) for preemption, (pt) for protection, (re) for refuge, (sh) forshading 141Figure 6.2 A predictive model for community structure, in the absence of Mazzaella,when a smalllmedium gap (e.g., 5x5 to lOxlO cm) is created in summer. Thesize of the circles represents the relative abundance of component species 142Figure 6.3 A predictive model for the community structure, in the absence of limpets,when a large gap (e.g., 20x20 cm) is created in winter. The size of the circlesrepresents the relative abundance of component species 143Figure B.1 Farrell?s model for the effect of consumers on the rate of succession (i?’ -consumers increase the rate of succession,0- no effect, , - consumers decreasethe rate of succession) cited from Farrell (1991) 145Figure B.2 Dynamics of ephemeral algae in limpet-excluded plots (-L), with (+B) andwithout (-B) barnacles 146Figure B.3 Direct and indirect interactions shown in other studies 147xiACKNOWLEDGMENTSI very much thank my teacher, friend and supervisor, Dr. Robert E. DeWreede, for hisconstructive suggestions, encouragement and support throughout the past five years. Thisstudy is partially funded by his grant from the Natural Science and Engineering ResearchCouncil of Canada (grant # 5-89872). My thanks go also to my committee members,Drs. Roy Turkington and Paul G. Harrison, for their critical suggestions and editorialcomments on this thesis. I am grateful to Carol Ann Borden for the flexibility that sheshowed when I was juggling teaching assistant responsibilities with the field trip toBamfield in every two months. My field works could not have been finished without thehelp of the following people: Ok Hyun Ahn, Kim Ailcock, Put Ang, Arnold Cheung,Angela Crampton, John Danko, Kristen Drewes, Glenda Eberle, Nick Grabovac, Ann-Marie Huang, Andrea Park, Brent Philips, Ricardo Scrosati, Frank Shaughnessy, LauraWong. I much appreciate their time and effort in the field, particularly in the often rainy,windy and freezing cold weather. I thank my colleague in the Dr. DeWreede’s lab, PutMg, Frank Shaughnessy, Brent Philips, Ricardo Scrosati, Kristen Drewes, RussellMarkel, Tania Thenu and Andrea Sussman, for useful discussion, help and friendship.Staff at the Bamfield Marine Station kindly allowed me to use some of their facilities.For technical help, I am indebted to Drs. Han Ju Eom and Robert Schutz, Department ofHuman Kinetics at UBC, for spending time helping me to analyze my data. My thanksalso go to Drs. Elizabeth Boulding and Thomas Carefoot for their help on identifyingsnails, limpets and barnacles.I am most grateful to my wife, Meeok Kim, who has shown her continuous patience andsupport in many ways and for many years. Her precious and painstaking supportfacilitated this study and exempted me from many house-keeping responsibilities. Iwould like to thank my parents, Hong Ki and Sun Hee Kim, for their understanding,encouragement, patience and support during my study at UBC as well as during the entireperiod of my graduate study in North America. I also appreciate my mother-in-law forher earnest prayer for me and my family during the study. Finally, I thank to my lovelyMm Jee and Dong Hyun for their understanding of this student daddy who could notspend much time to play with them the last several months.1CHAPTER 1THESIS INTRODUCTIONGeneral IntroductionIn 1966, Elton suggested an explicit aim for community ecology: to discover andmeasure the main dynamic relations between all organisms living on an area over someperiod of time. His view on community ecology was supported by other ecologists (e.g.,Dayton 1971, Connell 1972, Paine 1980) as an appropriate protocol guiding communityecologists. Later, Dayton (1971) amplified Elton’s view by adding disturbance as amechanism forming open space which is a common limiting resource in marine benthichabitats. Dayton carried out a pioneer study of the marine rocky intertidal communitywhich incorporated dynamic interactions among the component populations, trophicstructure, and the effects of major community disturbances. After Dayton’s work, manymarine community ecologists have continued to focus their research on factors thatinfluence community structure and dynamics. The effect of major biotic and abioticfactors on community structure and dynamics have been extensively reviewed; theseinclude studies on competition (Connell 1983, Schoener 1983, Denley and Dayton 1985,Olson and Lubchenco 1990, Paine 1990), herbivory or predation (Lubchenco and Gaines1981, Hawkins and Hartnoll 1983, Estes and Steinberg 1988), and disturbance (Connelland Keough 1985, Sousa 1985). These studies have contributed to the establishment anddevelopment of theories and models for community organization. Because the process oforganization and dynamics of any community is not a product of a single mechanism butof a combination of various biotic and abiotic factors which often interact with eachother, the most convincing demonstration of the factors influencing community structurerequires a comprehensive approach, one which examines all major interactions and2mechanisms that occur in the community under investigation. Few such studies havebeen done except for some which focussed on community succession and its mechanisms(Menge 1976, Lubchenco and Menge 1978, Sousa 1979, Turner 1983, Farrell 1991).My research was designed to implement such a comprehensive study. The targetcommunity which I chose to study is a high intertidal algal community on a rocky shore.This provides some unique benefits for direct measurement of various biotic interactions.Firstly, because many of the common species are sessile or slow moving and not hiddenin the substratum, their abundance and other characteristics can be measured readily.Secondly, most populations are amenable to experimental manipulation in the field, sothat replicate treatments and undisturbed controls can be set up at the same time. Thirdly,the upper zones are easily accessible and one can collect data on a very small spatial scalewith high accuracy, which is often impossible in most mid and low intertidal andsubtidal zones.Factors influencing intertidal algal communities can be divided into two groups:biological factors (e.g., competition and herbivory) and physical factors (e.g., disturbanceand physical stress). The importance of biological factors in controlling the abundanceand distribution of algal species is generally accepted to decrease with increasing tidalheight on rocky shores and physical factors are more important in structuring upperintertidal communities (Castenholz 1961, Connell 1972, 1975, Chapman 1973, Menge1978, Underwood 1980). However, this generalization has been questioned (Dayton1975, Underwood and Denley 1984) and needs further investigation with moreexperimental tests especially for its application to upper intertidal zones.Some ecologists have developed models to explain the relative importance offactors producing structure and dynamics by focusing on the interplay between physicalfactors and biological factors (Menge and Sutherland 1976, 1987, Connell and Slatyer1977). Specifically, Menge and Sutherland’s model addresses limits to speciesdistributions correlated with gradients in environmental harshness. Such correlations3may arise because abiotic factors impose direct physiological limits on species, orgradients in environmental stress may indirectly influence the abundance of prey (animalsor plants) by altering the impact of their consumers (carnivores or herbivores). However,such models do not reflect the likelihood that harsh abiotic factors alter the patterns ofspecies interactions and consequently influence species distribution. Palumbi (1985)showed an explicit example of such an interaction in which two species were competitorsin areas of low desiccation, but the interaction was a commensal one under moredesiccating conditions. So in one case the interaction would be called inhibition, while inthe other it would be termed facilitation. Bertness and Callaway (1994) recentlysuggested that a positive interaction, facilitation, may be a predictably important force incertain environments, and proposed that it should be incorporated into future communityparadigms. Therefore, the above models still need more experimental data from variablehabitats to either reject or support them.The main objectives of this thesis are: 1) to investigate interactions and theirmechanisms of action in a target community, 2) to provide empirical evidence from thestudy of a high intertidal habitat so that some current views of the mechanisms andmodels of community structure can be tested, and 3) based on the results, to predictcommunity-level responses to environmental impacts which may lead to reorganizationof the existing community structure.4The study site and communityThe study areas are the rocky upper intertidal communities at Prasiola Point andNudibranch Point located in Barkley Sound on the west coast of Vancouver Island,British Columbia, Canada (48°49’ N, 125°10’ W; Fig. 1.1). The two sites are about 0.4km apart and are both exposed to intermediate waves from the north-west and strongerwaves from the west; both sites have a similar flora and fauna. The experimental plotswere located on rocky substratum with a gentle slope; the zone ranged from 3.4 m to 5.3m above Lowest Normal Tide (LNT: Canadian Chart Datum).The algal community was dominated by three perennial macrophytes, Mazzaellacornucopiae (Post. & Rupr.) Hommersand et al. (Gigartinales, Rhodophyta; previouslyknown as the genus Iridaea), Pelvetiopsis limitata Gard. and Fucus distichus L. (bothFucales, Phaeophyta). These species grow both in well-mixed and mono-specific standsdepending on wave-exposure. Other stands of M. cornucopiae occurred in extremelywave-exposed sites characterized by the alga Lessoniopsis littoralis (Tilden) Reinke andthe invertebrate Pollicipes polymerus Sowerby, whereas fucoid stands were also found inrelatively more wave sheltered sites. However, sites for all experimental plots andsampling were set up in areas where mixed stands of the three macroalgae predominated.Most M. cornucopiae was 2-3.5 cm in length and grew as a dense turf on the rockysubstratum. The two morphologically similar fucoids are erect and usually 4-7 cm inlength at maturity. There are also some ephemeral algae in the community, such asCladophora columbiana Coil., Enteromorpha spp., Mastocarpus papillatus (Agardh)Kutzin, Porphyra spp., Scytosiphon dotyi Wynne, benthic diatoms, Endocladia muricata(Post. & Rupr.) 3. Ag., Analipusjaponicus (Harvey) Wynne, Urospora sp. and crustosealgae (‘Petroceli& phase of Mastocarpus, Hiidenbrandia sp. and Ralfsia sp.).Barnacles are the most abundant invertebrates in the habitat. The dominantspecies was Balanus glandula Darwin, whereas B. cariosus Pallas and Chthamalus dalli5Pilsbury occurred less frequently. The most abundant herbivores were snails (mostlyLittorina sp., see Boulding and VanAlstyne 1993 for further description) which occurredin a seasonal pattern with a peak abundance in summer (Chapter 3). Littorina scutulataGould and L. plena Gould often occurred in my study sites but their frequency was verylow (<3% of total snails). Other common herbivores were limpets, primarily Lottiadigitalis Rathke and a few L. pelta Rathke. There was an occasional occurrence ofmussels, primarily Mytilus trosselis L.Note: In this thesis, I discuss the ecology of a common high intertidal species of algae,Fucus distichus L. A recent treatment has revised the name to F. gardneri Silva, butmany questions remain on the appropriate nomenclature. I have chosen to retain the firstname as this is one by which it is commonly discussed in the ecological literature.6Organization of the thesisNon-manipulative field monitoring, manipulative field experiments andlaboratory experiments were conducted to address the stated objectives. This thesisconsists of six chapters, an introductory chapter, four research chapters, and theconcluding chapter.In Chapter 2, I deal with patterns of interactions among the dominant macroalgaeand discuss mechanisms of both algal competition (between morphologically distinctgroups) and positive interactions between them under harsh physical conditions.Coexistence of the three dominant algae is discussed in the light of these algalinteractions.Chapter 3 examines the effect of herbivorous snails on the three dominant algae.The abundance and distribution of the snails were monitored in the field, and theirfeeding preference on the three algal species was tested in the laboratory.Chapter 4 addresses the role of barnacles and limpets in this algal community.Results of three years of monitoring evaluate their role in algal recolonization andsuccession.Chapter 5 assesses the response of algae to physical disturbance. Two aspects ofdisturbance (i.e., size and season) are tested for their effects on the algal patch recoverypatterns.Chapter 6 synthesizes events in this intertidal system using information from theprevious chapters. Some predictions on the effect of altering presence or density ofcommunity biota are discussed, incorporating the insights gained from this research.7REFERENCESBertness, M. D., Callaway, R. (1994). Positive interactions in communities. Tree 9: 191-193.Boulding, E. G., Van Aistyne, K. L. (1993). Mechanisms of differential survival andgrowth of two species of Littorina on wave-exposed and on protected shores. J.Exp. Mar. Biol. Ecol. 169: 139-166.Castenholz, R. W. (1961). The effect of grazing on marine littoral diatom populations.Ecology 42: 783-794.Chapman, A. R. 0. (1973). A critique of prevailing attitudes on the control of seaweedzonation on the sea shore. Bot. Mar. 16: 80-82.Connell, J. H. (1972). Community interactions on marine rocky intertidal shores. Ann.Rev. Ecol. Syst. 3: 169-192.Connell, J. H. (1975). Some mechanisms producing structure in natural communities: amodel and evidence from field experiments. In: Cody, M. L., Daimond, J. M.(eds.) Ecology and evolution of communities. Belknap, Cambridge. pp. 460-490.Connell, J. H. (1983). On the prevalence and relative importance of interspecificcompetition: evidence from field experiments. Am. Nat. 122: 661-696.Connell, J. H., Slatyer, R. 0. (1977). Mechanisms of succession in natural communitiesand their role in community stability and organization. Am. Nat. 111: 1119-1144.Connell, J. H., Keough, M. J. (1985). Disturbance and patch dynamics of subtidal marineanimals on hard substrata. In: Pickett, S. T. A., White, P. S. (eds.) The ecology ofnatural disturbance and patch dynamics. Academic Press. New York. pp. 125-15 1.Dayton, P. K. (1971). Competition, disturbance and community organization: theprovision and subsequent utilization of space in a rocky intertidal community.Ecol. Monogr. 41: 35 1-389.Dayton, P. K. (1975). Experimental evaluation of ecological dominance in a rockyintertidal algal community. Ecol. Monogr. 45: 137-159.Denley, E. J., Dayton, P. K. (1985). Competition among macroalgae. In: Littler, M. M.,Littler, D. S. (eds.) Ecological field methods: macroalgae. Handbook ofphycological methods. Cambridge University Press. New York. pp. 511-530.Elton, C. S. (1966). The pattern of animal communities. Wiley, New York. pp. 432.Estes, J. A., Steinberg, P. D. (1988). Predation, herbivory, and kelp evolution.Paleobiology 14: 19-36.Farrell, T. M. (1991). Models and mechanisms of succession: an example from a rockyintertidal community. Ecol. Monogr. 61: 95-113.Hawkins, S. J., Hartnoll, R. 0. (1983). Grazing of intertidal algae by marineinvertebrates. Oceanogr. Mar. Biol. Ann. Rev. 21: 195-282.8Lubchenco, J., Menge, B. A. (1978). Community development and persistence in a lowrocky intertidal zone. Ecol. Monogr. 48: 67-94.Lubchenco, J., Gaines, S. D. (1981). A unified approach to marine plant-herbivoreinteractions. I. Populations and communities. Ann. Rev. Ecol. Syst. 12: 405-437.Menge, B. A. (1976). Organization of the New England rocky intertidal community: roleof predation, competition, and environmental heterogeniety. Ecol. Monogr. 46:355-393.Menge, B. (1978). Predation intensity in a rocky intertidal community. Oecologia 34: 1-16.Menge, B. A., Sutherland, J. P. (1976). Species diversity gradients: synthesis of the roleof predation, competition, and temporal heterogeneity. Am. Nat. 110: 35 1-369.Menge, B. A., Sutherland, J. P. (1987). Community regulation: variation in disturbance,competition, and predation in relation to environmental stress and recruitment.Am. Nat. 130: 730-757.Olson, A. M., Lubchenco, J. (1990). Competition in seaweeds: linking plant traits tocompetitive outcomes. J. Phycol. 26: 1-6.Paine, R. T. (1980). Food web: linkage, interaction strength and communityinfrastructure. J. Anim. Ecol. 49: 667-685.Paine, R. T. (1990). Benthic macroalgal competition: complications and consequences. J.Phycol. 26: 12-17.Palumbi, S. R. (1985). Spatial variation in an alga-sponge interaction and the evolution ofecological interactions. Am. Nat. 126: 267-274.Schoener, T. W. (1983). Field experiments on interspecific competition. Am. Nat. 122:240-285.Sousa, W. P. (1979). Experimental investigations of disturbance and ecologicalsuccession in a rocky intertidal algal community. Ecol. Monogr. 49: 227-254.Sousa, W. P. (1985). Disturbance and patch dynamics on rocky intertidal shores. In:Pickett, S. T. A., White, P. S. (eds.) The ecology of natural disturbance and patchdynamics. Academic Press. Orlando. pp. 101-124.Turner, T. (1983). Complexity of early and middle successional stages in a rockyintertidal surfgrass community. Oecologia 60: 56-65.Underwood, A. J. (1980). The effect of grazing by gastropods and physical factors on theupper limit of distribution of intertidal macroalgae. Oecologia 46: 201-213.Underwood, A. J,, Denley, E. J. (1984). Paradigms, explanations, and generalizations inmodels for the structure of intertidal communities on rocky shores. In: Strong, D.R., Simberloff, D., Abele, L. G., Thistle, A. B. (eds.) Ecological communities:Conceptual issues and the evidence. Princeton University Press. New Jersey. pp.151-180.9I IAlaskaW7’.?j(4550 -British Columbia- v.I. 500 —WA.A‘tb.) —OR.CA.Pacific Ocean12500’WI.B-1 .:.:BaifieIdBarkleySound 11400I1350I130°I1 25IFig. 1.1 Location of study sites. A = Nudibranch Point. B = Prasiola Point.10CHAPTER 2PATTERNS OF INTERACTIONS AMONG NEIGHBOR SPECIES IN AHIGH INTERTIDAL ALGAL COMMUNITYINTRODUCTIONSpecies interactions are fundamental in understanding community structure anddynamics. Marine ecologists working on the direct and indirect interactions betweenmarine benthic organisms have reported various such interactions. The usefulness ofexperimental tests of hypotheses about the roles of species interactions in determining thedistribution and abundance of marine organisms has been reviewed (Connell 1974, 1983,Paine 1977, 1990, Schoener 1983, Denley and Dayton 1985, Olson and Lubchenco 1990).Despite the criticism of the nature and design of some of the experiments (Dayton andOliver 1980, Underwood and Denley 1984), such experimentation is a powerful approachfor the development of realistic models of the structure and dynamics of naturalcommunities (Connell 1974, 1983, Dayton and Oliver 1980, Denley and Dayton 1985).Typically ecologists have focused on negative interactions (e.g., competition) whilepositive interactions (e.g., facilitation or protection) have received less attention or areignored in some current models of community organization (Connell and Slatyer 1977,Menge and Sutherland 1987, Tilman 1994; but see Bertness and Callaway 1994). Thistrend is not unique to marine benthic algal ecology. Thus, current reviews on competitionof marine benthic macroalgae indicate the necessity of more experimental data on thevariability of mechanisms of competition with changing life-history stages of competitors,variable environmental conditions, and on positive interactions, to improve ourunderstanding of the role of species interactions in structuring algal assemblages (Paine1990, Olson and Lubchenco 1990).11The mechanisms of interaction between competitors have traditionally beenrecognized as consisting of two basic kinds, exploitative competition and interferencecompetition, although these can be further subdivided into as many as six kinds (Schoener1983). Exploitative competition (e.g., consumption, preemption) is an indirect interactionbetween competitors, and the interaction is always mediated by the resource in short supply(Keddy 1989). Three important resources for macroalgae are light, space and nutrients(Denley and Dayton 1985). In contrast, interference competition (e.g., whiplash,overgrowth) occurs when one individual directly affects another. The interaction causesdirect mortality even when the resource might not be in short supply. However, there aresome situations in which both types of competition may occur simultaneously between thesame pair of competitors (reviewed by Denley and Dayton 1985).The outcome of competitive interactions may depend on such plant traits asmorphological type and life history stage, and also on the mechanism of competition (Olsonand Lubchenco 1990). For example, if the interaction is preemption of space, then largersize, spreading habit, and the ability to perennate may afford competitive dominance. Ifinterference is involved, rapid lateral growth, ability to raise the growing edge off thesubstratum and production of toxins are traits that may affect the outcome of an interaction(Olson and Lubchenco 1990). However, the above relationship between traits andcompetitive dominance may not be straightforward, and sometimes the outcome ofcompetition may be strongly affected by other biological interactions (e.g., herbivory) orphysical interactions (Connell 1975, Lubchenco and Gaines 1981, Hawkins and Hartnoll1983, Paine 1990).Many authors (Connell 1975, Underwood and Denley 1984, Denley and Dayton1985, Olson and Lubchenco 1990) have proposed difficulties or cautions in conductingexperiments on algal competition. First is the problem of detecting competition in naturalhabitats. Results of field manipulation experiments on the outcome of competition are oftenmisleading because other biotic or abiotic factors may interfere with or simulate competition12(often called “apparent competition” by Holt 1977 and Connell 1990). The most commonexample of the latter in algal competition is caused by herbivores (Lubchenco and Gaines1981, Hawkins and Hartnoll 1983, Paine 1990). Second, it is often difficult to identify asingle mechanism of competition. For example, exploitative competition (e.g., shading)can be accompanied by inteiference (e.g., allelopathic effect). Third, measuring theoutcome of interspecific competition may not be sufficient for understanding coexistence ofcompeting species where intraspecific competition is strong (Connell 1983). Therefore, theknowledge of, or a simultaneous experiment for, the intensity of intraspecific competitionis recommended (Connell 1983, Denley and Dayton 1985, Paine 1990). Fourth, theoutcome of competition may be changed depending on the developmental stages ofcompeting plants (e.g., germling vs. adult or adult vs. adult) (Olson and Lubchenco 1990).Similarly, the effect of one species on settlement and recruitment of another may not be thesame as the effect on the subsequent survival and growth of the species. Fifthly, whenrank order of competitive superiority is involved, reciprocal tests on both members in a pairare necessary to deal with the problem that asymmetrical competition resulting in theelimination of inferior species is not always the case. Reversals of competitive rank may becommon in natural communities (Connell 1983, Schoener 1983). To obtain such evidencerequires at least two experiments (on each member of a pair), which is rarely done(reviewed by Connell 1983, Denley and Dayton 1985). Ideally, experimenters shouldconsider as many of the problems listed above as possible to produce a clear andunambiguous demonstration of interspecific competition. There is no work in algalcompetition that addresses all the problems listed above; it may in fact be impossible toconduct such a field experiment. It is important, however, that field studies on competitionbe rigorous and comprehensive, combining manipulative experiments of potentiallyimportant factors in communities with a suitable knowledge of the biology of the algaeunder investigation. In this study, among the five problems listed above most of them(except the third) were taken into account for designing a series of field experiments.13Although positive interactions have been investigated less frequently, in marinebenthic organisms, than competition, its possibility and relevance have been discussedtheoretically by many ecologists (Connell and Slatyer 1977, Vandermeer 1980, Connell1983, Dethier and Duggins 1984, Sousa 1984, Bertness and Callaway 1994). Somepositive interactions occurred as a consequence of direct beneficial influences of onespecies to the other (e.g., Dayton 1975, Brawley and Johnson 1993), others as aconsequence of negative interactions acting indirectly through other species, possibly calledindirect commensalism, in a same trophic level (e.g., Duggins 1981, Kastendiek 1982) orin a different trophic level (e.g., Dethier and Duggins 1984, Hay 1986). Particularly in aphysically stressful habitat (e.g., upper intertidal zones), positive interactions (e.g.,neighbor habitat-amelioration; Bertness and Callaway 1994) rather than competition couldbe an important factor which allows coexistence of various species in the community.There is no study examining the variation of positive interactions along withmicrohabitat gradients (e.g., neighbor distance in the case of neighbor habitat-amelioration)in marine intertidal zones. The concept of neighbor distance has been studied particularlyin terrestrial plant communities (Fawcett 1964, Mack and Harper 1977, Turkington andHarper 1979, Lindquist et al. 1994). In marine habitats, the importance of biologicalinteractions in small patches has been invoked in a few studies (Connell 1972, Paine1990). Connell (1983) stated that for organisms that compete for space, and in particularclonal plants and attached colonial animals, competition occurs mainly between neighbors.In this context, neighbor distance was measured as a parameter to test if the outcome ofalgal interactions was affected by the distance between two interacting species.This study investigates how algal interaction patterns change due to thedevelopmental stages of the competitors and on the neighbor distance betweenmorphologically distinct groups. Because of the morphological similarity of the twofucoids, Fucus distichus and Pelvetiopsis limitata, the study focused on interactionsbetween Mazzaella cornucopiae and the two fucoids. Both manipulative and non-14manipulative field experiments were designed to address the following questions andhypotheses. First, does the turf-forming red alga, M. cornucopiae, affect the zygotesettlement or germination of the fucoids? Second, does M. cornucopiae affect the post-recruitment survivorship of the fucoids? Third, do the taller erect fucoids affect the growthof the shorter turf-forming M. cornucopiae by shading, whiplash or scour, or by chemicalcontent (e.g., phenolic compounds) by which the fucoids allelopathically suppress M.cornucopiae? Shading and scouring are commonly reported mechanisms of competition inboth subtidal and intertidal habitats (reviewed by Denley and Dayton 1985, Olson andLubchenco 1990, Paine 1990). A few studies have reported that chemical content ofcertain algae (including some fucoids) affected other algae by allelopathic influences(McLachlan and Craigie 1966, Carison and Carlson 1984).Although Hawkins and Hartnoll (1983) and Paine (1990) suggested the primaryimportance of the consumer’s role in algal interactions, in this chapter I generally avoidmentioning other biological factors (e.g., herbivory), because the next two chapters (3 and4) deal with this topic. I wifi present a synthetic view on the patterns of algal interactionincluding other biological and physical factors in Chapter 6.METHODSExperiment 1 : The relationship between Mazzaella coverand fucoid recruitmentIn August of 1991, sixteen permanent plots (20x20 cm) were randomly establishedon mixed stands of the three dominant algal species at Prasiola Point. Concrete nails werehammered to mark at least 3 corners of each plot. The nails were sometimes supported byplacing cement around them, so that most nails lasted for the experimental period. Thesepermanent plots were monitored at two-month intervals using a 20x20 cm quadrat divided15by monofilament line into 400 squares, each 1 cm2. Percent cover and exact location ofMazzaeiia cornucopiae turf was estimated by mapping the squares that had >50% cover ofblades; in this way, the squares with <50% were dropped so estimation will be balancedfor overestimation. The position of fucoids was also mapped using this technique and thesize class and reproductive condition was also noted. At each sampling date it was possibleto recognize newly recruited individual fucoids and thus the method enabled me to followindividual fucoid thalli from birth to death. The sixteen plots initially, and continuously,received four treatments Mazzae11a-removed, Fucus-removed, Pelvetiopsis-removed, andcontrol). Because there were no significant treatment effects between the control and eitherFucus-removed or Pelvetiopsis-removed plots (J. H. Kim, data not shown in the thesis),Fucus recruits used for analysis were collected from the control and Peivetiopsis-removedplots, and Pelvetiopsis recruits used were from the control and Fucus-removed plots.Monitoring was done until October of 1993.Statistical analyses were done using SYSTAT, version 5.2.1 for Macintosh,(Wilkinson et al. 1992). The Pearson Product Moment Correlation between number ofrecruits (log-transformed) and percent cover of Mazaelia was calculated for both fucoids.The significance of the correlation coefficients was assessed using Fisher and Yates’ tables(1963).Experiment 2 : Effects of pruning Mazzaella turf on fucoid recruitmentCorrelations found in Experiment 1 do not necessarily indicate a cause and effectrelationship, so I conducted a manipulative field experiment to test the hypothesis thatremoving Mazzaella turf enhances recruitment of Fucus and Pelvetiopsis. The experimentalunits consisted of three levels of Mazzaella pruning; 1) “total pruning” - cutting wholeMazzae11a blades leaving only their holdfasts, 2) “partial pruning” - cutting the upper part ofthe blades and leaving 1 cm of the bottom, and 3) “control” - no pruning. The different16levels of Mazaella pruning were done to test if the dense turf physically blocked fucoidpropagule arrival. The different heights of Mazzaeila blades were used to simulate differentlevels of ‘blocking’ recruits and ‘shading’ growing recruits. At Prasiola Point, 8permanent transect lines (about 1 m each) were marked by hammering concrete nails at bothends of each line. Using 10 cm intervals on the transect line, I numbered all potential plotsfor treatments on both sides of the transect line. Treatments were assigned by randomlychoosing three plots (lOx 10 cm) per line. The position of individual fucoid plants wasmapped using a lOx 10 cm quadrat with subdividing lines (comprising 100 lxi cmsubplots); this enabled me to obtain both the number of fucoid recruits and percent cover ofM. cornucopiae in each plot on every sampling date. The experiment was initiated in June,1993. Data were collected in October, 1993, and February and April, 1994.I found a correlation between Mazzaella percent cover and fucoid recruitment (Fig.2.1), so I first examined the relationship between the pruning treatment and Mazzaellacover as independent variables. The first step in this analysis was a test for homogeneity ofslopes, which can be determined by examining the interaction term of a regression, usingthe pruning treatment and percent cover as independent variables and the parameter valuesas dependent variables. In all 6 cases (3 sampling dates and 2 species), the probabilityvalue for the interaction term was not significant (p>.0,05) so I then conducted ANCOVA’swith the pruning treatment as an independent variable and Mazzaella cover as a covariate.Analyses were done using the BMDP2V statistical package.Experiment 3 : Effects of Mazzaella turf on post-recruitment survivorshipof fucoidsWhile Experiment I was designed to test the effect of Mazzaella cornucopiae on therecruitment stage of both fucoids, this experiment tests its effects on post-recruitmentsurvivorship of the fucoids. Non-manipulative field monitoring for the sixteen permanent17plots (the same plots used in Exp. 1) at Prasiola Point were done from August, 1991 toOctober, 1993. Using the quadrat with subdividing lines described previously, theposition of M. cornucopiae turf and individual fucoid plants in each plot were tape-recordedin the field and then mapped on a sheet in the laboratory. The life span of individualfucoids was obtained by following individual thalli from recruitment to disappearance.Individuals recruited or found after August, 1992, were not included in the analysisbecause their complete life span could not be followed. Using the map, the distancebetween each fucoid thallus and the nearest M. cornucopiae was measured. However,because the edge of the Mazzaella turf changed over time due to vegetative growth ordecline, the distance for each fucoid from turf was not always the same in bimonthlysamples. Therefore, I calculated the mean distance for each fucoid for its life span fromdistance values measured bimonthly and used these values for analysis. The life span andthe mean distance for each fucoid were plotted to investigate their relationship.For data analyses, I divided the distance between the Mazzaeila turf and fucoidrecruits into three groups based on the pattern of Fucus life span along with the neighbordistance (Fig. 2.2). Three distance groups include ‘CONTACT’ for those growing withinthe turf (or 0 cm from turf), ‘CLOSE’ for those growing between 0.3 and 0.7 cm fromturf, and ‘FAR’ for those growing >2 cm from turf One-way ANOVA was used to testthe difference among the distance groups for each fucoid species. Tukey’s HSD test wasalso used when ANOVAs were significant. Student’s t-test was used to compare the lifespan (months) of Fucus distichus and Pelvetiopsis limitata in the same distance group.Experiment 4 : Effects of fucoids on Mazzaella corn ucopiaeA manipulative field experiment was initiated at Nudibranch Point in June, 1994.The experimental design included five treatments using both live fucoid thalli and artificialplants which were attached to a mesh strip and set up on Mazzaella turf. The five18treatments and their characteristics are as follows: 1) live Fucus thalli which tests forcanopy (shading), scouring (disturbance) and phenolic (chemical) effects, 2) livePeivetiopsis thalli testing for the same characteristics as live Fucus, 3) ‘clear’ artificialplants which tests only for scouring, but not for canopy nor phenolic effects, 4) ‘dark’artificial plants which test for canopy and scouring, but not for phenolics, and 5) a controlwith neither live nor artificial thalli.Adult thalli (about 7 cm in length) of F. distichus and P. li;nitata were haphazardlycollected (with holdfasts intact) from within the normal vertical range at Nudibranch Point,and were transferred to running seawater tanks at the Bamfield Marine Station. Then, thalliwith similar weight (20.5±1.3 g blotted wet weight) were selected, although sometrimming was sometimes needed to equalize thallus weight for each experimental unit.Holdfasts and lower parts (—1 cm) of each thallus were placed into twists of 9.4 mmpolypropylene rope (5 cm in length) which had both ends melted to prevent untwisting.Vinyl covered wire (1.1 mm in diam.) was tightly wound around the rope to secure thethalli. For the artificial plants, a transparent, flexible plastic sheet (0.55 mm in thickness)was cut to make one type of treatment, ‘clear’, and an opaque plastic sheet (0.65 mm inthickness) was cut to make the other ‘dark’. Artificial plants (13.5 cm long, 5.7 cm widefor ‘blade’ area, 1.0 cm wide for ‘stipe’) were made by attaching two extra layers of sheet(one of 5.0 cm and the other 8.0 cm long) to the lower part of the artificial plants and, toattach these extra layers, the margin of each extra layer was sewed with thin monofilamentline. Therefore, each artificial plant consisted of a three-layered stipe, a two-layered lowerblade and one-layered upper blade. This construction provided sufficient strength underforceful wave action and mimicked the motion of live plants in the back and forth waterflow observed at high tides. Like real fucoid plants, the lower part (about 2.5 cm) of‘stipe’ area of the artificial plant was inserted to the rope and tightened. Vinyl coveredmesh (3.5 mm diam.), cross-linked every 2.5 cm x 5.1 cm, was used to hold the treatmentplants to the substratum. This mesh is strong and yet malleable enough to bend with the19rock substratum (Shaughnessy 1994). Mesh strips were cut so that each was 90 cm x 4 cmallowing five treatments (including a control for an empty spot) thaffi haphazardly placed 20cm apart. The ropes with fucoid thalli and artificial plants inserted were attached to themesh strip with an electrician’s cable tie. Seven mesh strips (7 replicates) were horizontallyattached to the rock substratum at Nudibranch Point where mixed stands of the threespecies occurred. The orientation of existing live fucoids, which was mostly caused byout-going waves and the slope of rock substratum, was used as an indicator for orientingmesh strips, because all the treatment thalli should necessarily be sitting on the Mazzaeliabeds in the same direction at every low tide to achieve the treatment effects, especially forcanopy and phenolic effects. Attachment sites for mesh strips were chosen where therewas an untouched Mazzaella bed (by existing fucoids, other algae or barnacles) underneatheach treatment thallus. The entire mesh strip was kept in contact with the rock substratumby using either concrete nails or bolts secured at each end and at the middle of the strip.Some artifacts due to using artificial plants were considered as noted in Connell(1974) and Underwood (1980). To test for effects on understory Mazzaelia due to theshade caused by fucoids, replicate light readings (mean ± SE, n=5) were taken under thefucoid canopy, ‘clear’ and ‘dark’ artificial plants and natural light intensity (‘control’) usinga Licor (LI- 185A) quantum photometer. Under no canopy, 2600±0.0 iE m2s’ of lightreached the substratum, compared to 12.9±1.8 iE m2s’ under F. distichus, 13.7±4.4 pEm2s1 under P. limitata and 2650±6.0 E m2s1under ‘clear’ artificial plants. To obtainthe ‘dark’ artificial plant that best mimicked the shade cast by fucoid canopies, Ihaphazardly made eight holes (2.5 mm diam.) on each blade using a hole punch so that14.3±4.0 pE m2s1of light reached the substratum. Replicate temperature readings werealso made under each treatment plant. In the sunny mid-day of June 23, 1994,temperatures under F. distichus, P. limitata and ‘dark’ plants were 18.5±0.7 °C, 19.2±0.90C, 20±0.4 °C, respectively. High temperatures under the ‘clear’ plants (due to agreenhouse effect) was lowered by making twelve holes (3.8 mm diam.) on each blade so20that a similar temperature was obtained compared to that of the control (23.5±0.5 °C,23.1±0.3 °C, respectively).Size class (5 mm difference in each class; size class 1 for <5mm, size class 2 for 5-10mm, etc.) densities of M. cornucopiae blades in 2x2 cm quadrats under each treatmentplant were measured in the field, and these were then converted to biomass (g) using theregression coefficient (Fig. 2.3) between size class and wet weight. Data were collected atthe beginning (June, 1994) and the end (August, 1994) of the experiment. Although thesites for quadrat placement were not marked, sampling was done at the center under eachtreatment plant so some portion of the 4 cm2areas for the sampling probably overlapped.Therefore, a 5x2 (Treatment x Time) ANOVA with repeated measures on Time factor and apreplanned multiple comparison with Bonferroni adjusted probability (p=O.OS /4=0.0125) were used for analysis and hypothesis tests. Since it is a repeated measuresdesign, probability values for a multivariate statistic (Wilk’s lambda), rather than forunivariate statistics, were used for the multiple comparisons. Hypothesis I (shading effect)was tested by comparing Mazzaella biomass between ‘clea? and ‘dark’ artificial plants.Hypothesis II (scouring effect) and Hypothesis III (phenolic effect) were tested bycomparing ‘clear’ vs. control, and ‘dark’ vs. Fucus and Peivetiopsis, respectively. If aneffect was significant, a further analysis was done to examine if the effect influenced thesize class structure of M. cornucopiae. For each size class, an independent t-test wasapplied to compare the changes in blade density (density after exp. - before exp.) betweentwo factors. Since there were six size classes, the t-test was performed six times with aBonferroni-adjusted probability value (p=O.05 /6 = 0.0083). The homogeneity of variancewas tested using Bartlett’s test (Wilkinson et al. 1992) and Cochran’s test (Winer 1971).The results of both tests were not significant (p>0.05) indicating an equal variance. Theresiduals were plotted for inspection for normality. A few artificial plants and fucoid thalliwere partly broken or lost during the two-month experimental period, and these were21dropped from the analyses. As a result, a reduction (e.g., to 5) in replicates occurred incertain treatments.RESULTSThe relationship between Mazzaella cover and fucoid recruitmentLower recruitment of Fucus distichus occurred in the piots where greater M.cornucopiae cover existed (Pearson Product-Moment Correlation, r=-O.423) (Fig. 2.1).Pelvetiopsis limitata exhibited the same pattern (r=-O.523) (Fig. 2.1). Both correlationswere significant (Fucus, F(1.132)=28.73, p0.05) changed by the pruning treatments atany sampling date (Table 2.1). Therefore, removing Mazzaella turf (canopy) which wasconsidered ‘blocking’ recruits or ‘shading’ growing recruits from the results of Experiment1 did not increase the fucoid recruitment in this manipulative experiment.Effects of Mazzaella turf on post-recruitment survivorship of fucoidsThe Mazzaella turf influenced the two fucoid species differently in theirsurvivorship after the recruitment stage. The mean life span of Fucus distichus recruitedwithin the turf was relatively short (2.2 months). However, as the mean distance (seeMETHODS) between individual F. distichus and turf became greater, Fucus life spanshowed a sharp increase and reached a peak (5.4 months) at a distance of about 0.5 cmfrom the edge of the turf (Fig. 2.2). The mean life span then decreased gradually to adistance of approximately 2 cm, and at >2 cm the changes in life span were relatively small.Patterns in life span of Pelvetiopsis limitata were different from those of F. distichus. Thelongest mean life span of Pelvetiopsis limitata (5.0 months) was found in the individualswithin Mazzaelki turf. However, the life span along with the neighbor distance changedirregularly (Fig. 2.2).The results of one-way ANOVA and a post hoc test comparing the life span of thethree distance groups indicated that in F. distichus the life span of the ‘close’ group (0.3-0.7 cm) was significantly higher than that of either ‘contact’ (within turf or 0 cm) or ‘far’(>2.0 cm) group (Table 2.2). The life spans in the ‘contact’ and ‘far’ groups was notsignificantly different. However, in P. limitata the life span of all three groups were similar(5.0, 4.6, 4.3 months for ‘contact’, ‘close’, ‘far’, respectively). When comparing the two23fucoid species for their life span with the same distance group, there was no significantdifference between the two species in any distance group (independent t-test at p=O.05).However, the mean life span in the ‘contact’ group was notably different (2.2 months forFucus and 5.0 months for Pelvetiopsis; p=O.004 at df=20 if pooled variances were used),although this difference was not statistically significant (the use of separate variances wassuggested because of the severely unequal sample sizes, n=16 and 6, respectively;Wilkinson et al. 1992).Effects of fucoids on Mazzaella cornucopiaeThe effects of live fucoid thalli and of the two types of artificial fucoid on Mazzaellabiomass showed that there were significant differences in biomass of M. cornucopiaeamong the treatments (p=O.OO1, one-way ANOVA with repeated measures). Biomass(blade wet weight) of M. cornucopiae generally decreased during the experimental period(June to August, 1994). The mean biomass for the control decreased by 0.38g (16.8%)per 2x2 cm plot (Fig. 2.6). The Mazzaella biomass under the ‘clea? artificial plant showedthe least reduction (0. 14g, 9.0%) and that under the ‘dark’ artificial plant had the largestreduction (0.88g. 50.7%) (Fig. 2.6).Of the 3 hypotheses tested, only the canopy effect (shading) was significant.Mazzaella biomass change (after-experiment minus before-experiment) in ‘dark’ wassignificantly greater than in ‘clear’; that is, biomass of Mazzaella was affected by reductionof light (Table 2,3). Reduction of light also caused a color change of Mazzaella thalli, fromlight greenish red to dark red. The scouring effect, tested by comparing the control with‘clear’, showed no significant difference in the biomass change between these two factors,hence the second hypothesis was rejected. The hypothesis of allelopathy (tested bycomparing the ‘dark’ with either ‘Fucus’ or ‘Pelvetiopsis’) was rejected for both fucoids24(p=O. 189 and p=O.374, respectively), indicating that Mazzaelki biomass was not affectedby allelopathy.The significant canopy effect of fucoids on Mazzaella biomass was further analyzedfor its potential effect on the size class of the red alga. Mazzaella blade densities decreasedin all size classes under the canopy of ‘dark’ artificial blades, whereas the blade densitiesunder the ‘clear’ artificial blades had a variable change depending on the size classes (Fig.2.7). Independent t-tests for the blade density changes (‘after’ minus ‘before’) between‘clear’ and ‘dark’ on each size class indicated that only blades in size class 2 weresignificantly different (p=O.008) in density between the two treatments.DISCUSSIONThe complexity of algal interactions among the three dominantsThe results presented here provide an example of bi-directional interactions inwhich competitive dominance is reversed depending on the developmental stages or lifehistory stages of competitors. Space preemption by Mazzaella corlwcopiae lowered thenumber of recruits of both Fucus distichus and Pelvetiopsis limitata within its turf.However, once the fucoids successfully recruited, they formed a canopy and reducedMazzaella biomass by shading.The preemption of suitable space by a turf-forming species and the subsequentreduction of settlement of other morphological forms has been commonly observed bymany authors (Lubchenco 1978, Hruby and Norton 1979, Ambrose and Nelson 1982,Chapman 1984, Kennelly 1987). From this literature, the mechanisms by which theMazzaella turf prevented recruitment of fucoids can be presumed to be as follows, Onepossibility is that the physical occupation of space by turf reduces the area available forsettlement by fucoid propagules. Another is that the turf may outcompete juvenile fucoids25for light or nutrients. However, experimental removal of turf did not significantly increaserecruitment of either Fucus or Peivetiopsis. This was an unexpected result even thoughthere were slightly more fucoid recruits in the “total-pruning” plots than in control plots.This result might imply that there must be another factor(s) involved in survivorship ofjuvenile fucoids in the turf-removed plots. These factors may be the relatively strongerdesiccation and the increased wave impact caused by removing the turf, discussed in thenext section.Morphological differences in adult plants between Mazzaella and the two fucoidsbrought these algae to another arena of competition when fucoids successfully settlednearby or within the red algal turf. Olson and Lubchenco (1990) documented that the arenaof competition changes as the developmental stages of competitors change; as a result, theoutcome of competition may depend on the developmental stages that are competing. Inthis study, as fucoids grew (>3-4 cm), they formed a canopy and reduced the biomass ofMazzaella underneath their thalli because of light interception. A similar case has beenreported by Lubchenco (1983). She found that Enteromorpha outcompeted Fucusgermlings early in succession by its faster growth rate in the absence of grazers. However,Fucus became established and overtopped Enteroinorpha when grazers were effective, andin the long term Fucus excluded Enteromorpha from the rock surface by preempting space.In the upper intertidal communities at Nudibranch Pt. and Prasiola Pt., successful fallrecruitment of both fucoids to the substratum within Mazzaella beds (see Chapter 5) couldbe possible because Littorina sp. prefered to eat Mazzaelia and the intensity of thispreferential feeding could be increased in summer months due to increasing snail densities(see Chapter 3). The summer decline of Mazzaella populations opens up free space forfucoids which have their recruitment peak in October. These series of coincident eventschange the direction of competition and its outcome.Fucoids did not affect adult Mazzaella either by scouring (or whiplash) or by theirchemical contents such as phenolic compounds. However, allelopathic effects of brown26algae were noted to be important many years ago when workers studied the antibacterialand antialgal properties of phenolic compounds in dictyotalean and fucalean algae(McLachlan and Craigie 1966, Fletcher, 1975). Schiel and Foster (1986) have pointed outits importance in determining the dynamics of some communities, and some studies haveshown that allelopathic effects of brown algae (probably due to phenolic compounds)inhibited the abundance of other algae in intertidal (Fletcher 1975) and subtidal habitats(Kennelly 1987). Fucus distichus and Pelvetiopsis limitata were known to containphenolic compounds of 4.35% and 4.93% dry mass, respectively (Steinberg 1985).However, the biomass of Mazzaella underneath real plants was slightly less reduced thanthat underneath ‘dark’ artifitial plants; this indicated that further reduction of Mazzaellabiomass caused by the chemicals did not occur at all. Although there was a possibility thatfucoids whiplashed and affected the settlement of barnacles and some ephemeral algae insmall gaps (5x5 cm) cleared in the proximity of the fucoids (Chapter 5), fucoids did notaffect Mazzaeila growing within their boundary of scouring. The result of careful fieldobservation on Mazzaelia around mature fucoid thalli supported this result. The absence ofa scouring effect by the fucoids is probably because the relative size of the fucoids is notlarge enough (Grant 1977, Farrell 1989) to affect adult Mazzaella turf.The reduction of light (about 0.51% of unshaded condition) by fucoids affected thesize class density of Mazzaella, with a particularly significant decrease in the size class 2(0.5-1 cm in blade length). It is not certain why this particular size class was significantlyreduced. Shading effects on understory species in algal communities have been extensivelystudied in subtidal kelp communities (Dayton et. al. 1984, Reed and Foster 1984,Santeiices and Ojeda 1984, Kennelly 1989, Dean et. al. 1989, Reed 1990) and intertidalalgal communities (Dayton 1971, 1975, Schonbeck and Norton 1980, Ang and DeWreede1992). In intertidal habitats, shading has sometimes been reported as a positive factor,especially where or when desiccation is strong (Dayton 1975, Ang 1991). However, inthis study light may have been important for Mazzaella growth, even when the population27is declining between June and August 1994, such that shading reduced more biomass thanthe amount of natural reduction in the control sites. This result ensures that the deleteriouseffect on Mazzaelia by fucoid shading should also be effective at other times of the year;thus the effect may be more intense when Mazzaella actively grows in February to April (tobe discussed in Chapter 5).In this study, competitive superiority was reversed depending on the developmentalstages of fucoids. Mazzaelia outcompeted fucoids at the recruitment stage of the fucoids bypreempting space. However, after the recruitment of fucoids, both fucoids inhibited thegrowth of Mazzaella by shading. When a reversal of competitive superiority occurscompetitive elimination is less likely (Connell 1983). In his review of field experiments oncompetition, Connell (1983) reported that only a few studies were sufficientlycomprehensive to provide evidence concerning such reversals. There were a few exampleson non-hierarchical competitive networks among marine subtidal animals (reviewed byConnell and Keough 1985). Similarly among macroalgae, the direction of competitiveovergrowth was reversed in the presence of grazers (Paine 1984, Steneck 1985). Unlikethese two studies on macroalgae, the change of the direction of competition betweenMazzaella and the fucoids was more likely due to the difference in morphology and lifehistory stages of these algae rather than to the presence of herbivorous snails. Preferentialfeeding on Mazzaella by snails did facilitate the reversal of the competitive direction but it isalso possible that such reversal could occur as plants grew in the absence of the grazer.This will be discussed more in chapter 3.The mechanism of positive interaction and neighbor distanceThe relatively high survivorship of Fucus growing at the edge of Mazzaella turf isevidence of a direct facilitation by the neighboring species against potentially limitingphysical stresses. A possible explanation for the different longevity patterns of Fucus and28Pelvetiopsis with respect to distance from Mazzaella is based on the hypotheticalrelationships between competitive interactions and physical stresses (Fig. 2.8). Individualplants of Fucus and Pelvetiopsis growing within the Mazzaella turf may encounter lessdesiccation because of the moisture-holding ability of the red algal tuif (Hay 1981, Padilla1984). As the fucoids grow up, they may have limited space for holdfast expansionbecause of Mauaeila’s preemption of space. This increases the susceptibility of fucoids towave impact. This lethal factor is probably more effective on Fucus which has relativelywider thalli than Pelvetiopsis. However, biomechanical differences between the twofucoids with respect to wave force have not been reported. It has been reported that thecompetitive outcomes in macroalgae were sometimes influenced by local (microhabitat)physical conditions (e.g., desiccation, wave action) (Padilla 1984). Thus, the shortlifespan of Fucus within Mazzaella turf may be a result of competition coupled withphysical stress. The microhabitat conditions at the turf edge can be ameliorated byMazzaella’s buffer against wave impact and also by sufficient moisture from turf, inaddition no competition for space apparently occurs. However, at a distance >2 cm, bothdesiccation and wave impact can be lethal for Fucus because it is “too far” to get the bufferand moisture from Mazzaella (its blade length is about 2-3 cm).I suggest a model for Fucus survivorship in relation to the distance from theprimary space-holder, Mazzaella, and with respect to the two limiting factors, competitionand physical stress (Fig. 2.9). Competition is probably effective only if the two species arein contact. The intensity of competition then drops suddenly as the neighbor distanceincreases. At the same time, physical stresses gradually increase as the two species arefurther apart. The highest survivorship of Fucus occurs at the point (or distance) wherethe combined effect of two factors is minimal.The effect of Maz.zaella on post-recruitment survival of Fucus as shown by thisstudy suggests three important factors that structure this algal assemblage. First, directpositive interactions may be common, predictable, and pervasive forces in natural29communities and in physically harsh environments in particular. The mechanism of theinteraction found in this study is an example of neighbor habitat-amelioration (Bertness andCallaway 1994). This can be differentiated from the results of Paine (1980) and Dethier andDuggins (1984) which showed empirical evidence of positive indirect interactions andfeedback mechanisms in food webs. In some harsh intertidal habitats, there is limitedevidence that neighbor species improved deleterious habitat conditions (e.g., severe heatand desiccation pressure) and facilitated recruitment of barnacles (Bertness 1989) andmussels (Bertness and Grosholz 1985). Dayton (1975) reported an example of directpositive interaction between macroalgae and showed that larger overstorey algae (e.g.,Hedophyllum) protected smaller understorey species from desiccation or radiation damage.Second, the concept of neighbor distance, which was first introduced in terrestrialplant interactions (Fawcett 1964, Turkington and Harper 1979), should be adapted tomarine benthic algal interactions with a modified mechanistic concept. Since nobelowground competition exists among benthic algae, the outcome of algal interactions issolely dependent upon the morphological form and size of thalli (Hay 1981, Paine 1984);this is particularly true if the limiting resource is space or the competition is by interference.This study confirms the idea that for organisms that compete for space, and in particularclonal ones such as plants and some sessile animals, competition occurs mainly betweenneighbor species (Connell 1983). In addition, neighbor distance in this upper intertidalhabitat determined which factor(s) are responsible for the fate of an individual plant. Thalliof Fucus distichus encountered different biotic and abiotic factors (competition to protectionto physical stress) as neighbor distance increased. Consequently, the longer survival of aFucus thallus in this high intertidal site which features an intermediate to strong wave actionrequires a certain optimum distance (e.g., 0.5 cm±0.2) from its neighbor. Therefore, themaintenance of a Fucus population is partially dependent on the presence of Mazzaellacornucopiae, particularly when Fucus increases its population size toward the site with30more extreme conditions (e.g., higher tidal height, more wave-exposed) from its ownnatural habitats with milder conditions.Third, the importance of interactions at a small spatial scale in this communityshould be noted. Paine (1990) pointed out that interaction mechanisms on a small (<2 m2)scale are important in understanding the nature of algal assemblages. The range of spatialscales at which one species affected another was surprisingly small (<2 cm). This shouldbe considered in designing field experiments for detecting species interactions of smallorganisms. Brawley and Johnson (1993) reported that microclimate was an importantpredictor of the likelihood and spatial pattern of survival of settled larvae, reproductivepropagules, and other microscopic stages in the life histories of organisms growing inintertidal and other water-stressed (desiccating) environments. It is certain that relevantspatial scale is mainly determined by the size of organisms interacting (this applies only toplants) and the severity of physical stresses.Bertness and Callaway (1994) proposed that positive interactions during successionand recruitment, as well as among established adults, are unusually common in harshphysical environments for the simple reason that primary space-holders frequently bufferneighbors from potentially limiting stresses. In this perspective, the Mazzaella -Fucusinteraction in a stressful environment with strong wave force and desiccation deservesincreased empirical attention and should be incorporated into models of communityorganization in harsh habitats like the upper intertidal zone.Coexistence of the major species Biological perspectivesIs coexistence of the three dominants due to the variation in algal interactions amongthem? This research has shown that patterns of interactions among neighbor species arecomplicated but well-balanced. The balance in competitive direction (or dominance)between Mazzaella and fucoids as well as the balance in the positive and negative31interactions between Mazzaella and Fucus supported the persistence of each member in thecommunity. Looking at their distinctive functional morphology, the shorter turf-formingMazzaella probably has a competitive disadvantage over upright and relatively fast-growingfucoids because the turf-former may have a reduced photosynthetic activity limited to theupper portions of the thallus due to self-shading and also may suffer nutrition depletionwithin the turf matrix (Hay 1981). In contrast, Mazzaella must be the species best adaptedto high desiccation and strong wave action among the three dominants because it has water-holding capacity and self-cushioning thalli in a dense turf (Hay 1981, Padilla 1984). Fucusdistichus is the only species among the three dominants which also appears in the lowerzone (upper-mid intertidal), where it grows up to 3-4 times larger than individuals in mystudy sites. Although this alga has a physiological adaptation (i.e., high photosyntheticrate in air) to tidal emergence (Johnson et al. 1974, Quadir et al. 1979), it still may havesome morphological limitation (e.g., relatively wider thallus than Pelvetiopsis) to survivein the force of breaking waves. Consequently, the advantage from the positive interactionwith Mazzaella, the relatively high recruitment (compared to Peivetiopsis; J. H. Kimunpubl. data) and the facilitation of settlement by barnacles (Chapter 4) are the importantparameters which allow Fucus to maintain its co-dominance in this community. Naturalhabitats for Pelvetiopsis limitata appear to be confined to the upper intertidal, unlike F.distichus (Sousa 1984, Farrell 1989, 1991). According to a recent review on fucoid algaeby Chapman (1995), there was no information available for the physiological andreproductive ecology of P. limitata. However, in this study P. limitata seemed to be arelatively better-adapted species to the upper intertidal zones in Prasiola and NudibranchPoints than F. distichus, because survival and colonization of this alga was not affected bysome biological (i.e., the presence of Mazzaella) and physical (i.e., size of disturbance; tobe discussed in Chapter 5) factors.From a biological perspective, coexistence of these three macroalgae in thiscommunity is likely because of the biological adaptation of each species to physical stressand because the outcomes of their interactions are well-balanced. Thus, competitiveelimination is unlikely because competition among the species is symmetric (Connell1983). However, it still remains an open question whether the biological interactions arerelatively more or less important in structuring a community under harsh physicalconditions such as those experienced in this algal community. The data presented in thischapter provide experimental evidence that detectable biological interactions occur in thiscommunity, and such interactions, together with other factors described in subsequentchapters of this thesis, are important determinants of community dynamics.3233REFERENCESAmbrose, R. F., Nelson, B. V. (1982). Inhibition of giant kelp recruitment by anintroduced brown alga. Bot. Mar. 25: 265-267.Ang, P. 0. (1991). Natural dynamics of a Fucus distichus (Phaeophyceae, Fucales)population: reproduction and recruitment. Mar. Ecol. Prog. Ser. 78: 7 1-85.Ang, P. 0., DeWreede, R. E. (1992). Density-dependence in a population of Fucusdistichus. Mar. Ecol. Prog. Ser. 90: 169-181.Bertness, M. D. (1989). Intraspecific competition and facilitation in a northern acornbarnacle population. Ecology 70: 257-268.Bertness, M. D., Grosholz, T. (1985). Population dynamics of the ribbed mussel,Geukensia demissa: the cost and benefits of an aggregated distribution. Oecologia67: 192-197.Bertness, M. D., Callaway, R. (1994). Positive interactions in communities. Tree 9: 191-193.Brawley, S. H., Johnson, L. E. (1993). Predicting desiccation stress in microscopicorganisms: the use of agarose beads to determine evaporation within and betweenintertidal microhabitats. J. Phycol. 29: 528-535.Carlson, D. J., Carlson, M. L. (1984). Reassessment of exudation by fucoid macroalgae.Limnol. Oceanogr. 29: 1077-1087.Chapman, A. R. 0. (1984). Reproduction, recruitment and mortality in two species ofLaminaria in southwest Nova Scotia. J. Exp. Mar. Biol. Ecol. 78: 99-109.Chapman, A. R. 0. (1995). Functional ecology of fucoid algae: twenty-three years ofprogress. Phycologia 34: 1-32.Connell, J. H. (1972). Community interactions on marine rocky intertidal shores. Ann,Rev. Ecol. Syst. 3: 169-192.Connell, J. H. (1974). Field experiments in marine ecology. In: Mariscal, R. (ed.)Experimental marine biology. Academic Press. New York. pp. 2 1-54.Connell, J. H. (1975). Some mechanisms producing structure in natural communities: amodel and evidence from field experiments. In: Cody, M. L., Diamond, J. M.(eds.) Ecology and evolution of communities. Bellcnap, Cambridge. pp. 460-490.Connell, J. H. (1983). On the prevalence and relative importance of interspecificcompetition: evidence from field experiments. Am. Nat. 122: 661-696.Connell, J. H. (1990). Apparent versus “reaU’ competition in plants. In: Grace, J. B.,Tilman, D. (eds.) Perspectives on plant competition. Academic Press, Inc. NewYork. pp. 9-26.Connell, J. H., Slatyer, R. 0. (1977). Mechanisms of succession in natural communitiesand their role in community stability and organization. Am. Nat. 111: 1119-1144.34Connell, J. H., Keough, M. J. (1985). Disturbance and patch dynamics of subtidal marineanimals on hard substrata. In: Pickett, S. T. A., White, P. S. (eds.) The ecology ofnatural disturbance and patch dynamics. Academic Press. New York. pp. 125-151.Dayton, P. K, (1971). Competition, disturbance and community organization: theprovision and subsequent utilization of space in a rocky intertidal community. Ecol.Monogr. 41: 351-389.Dayton, P. K. (1975). Experimental evaluation of ecological dominance in a rockyintertidal algal community. Ecol. Monogr. 45: 137-159.Dayton, P. K., Oliver, J. S. (1980). An evaluation of experimental analyses of populationand community patterns in benthic marine environments. In: Tenore, K. R., Coull,B. C. (eds.) Marine benthic dynamics. University of South Carolina Press. pp. 93-120.Dayton, P. K., Currie, V., Gerrodette, T., Keller, B. D., Rosenthal, R., Ven Tresca, D.(1984). Patch dynamics and stability of some California kelp communities, Ecol.Monogr. 54: 253-289.Dean, T. A., Thies, K., Lagos, S. L. (1989). Survival of juvenile giant kelp: the effects ofdemographic factors, competitors and grazers. Ecology 70: 483-495.Denley, E. J., Dayton, P. K. (1985). Competition among macro algae. In: Littler, M. M.,Littler, D. S. (eds.) Ecological field methods: macroalgae. Handbook ofphycological methods. Cambridge University Press. New York. pp. p. 511-530.Dethier, M. N., Duggins, D. 0. (1984). An ??indirect commensalism” between marineherbivores and the importance of competitive hierarchies. Am. Nat. 124: 205-2 19.Duggins, D. 0. (1981). Interspecific facilitation in a guild of benthic marine herbivores.Oecologia 48: 157-163.Farrell, T. M. (1989). Succession in a rocky intertidal community: the importance ofdisturbance size and position within a disturbed patch. J. Exp. Mar. Biol. Ecol.128: 57-73.Farrell, T. M. (1991). Models and mechanisms of succession: an example from a rockyintertidal community. Ecol. Monogr. 61: 95-113.Fawcett, R. G. (1964). Effects of certain conditions on yield of crop plants. Nature 204:858-860.Fisher, R. A., Yates, F. (1963). Statistical tables for biological, agricultural and medicalresearch (6th ed.). Oliver & Boyd. Edinburgh. pp. 138.Fletcher, R. L. (1975). Heteroantagonism observed in mixed algal cultures. Nature(London) 253: 534-535.Grant, W. S. (1977). High intertidal community organization on a rocky headland inMaine, U.S.A. Mar. Biol. 44: 15-25.Hawkins, S. J., Hartnoll, R. 0. (1983). Grazing of intertidal algae by marineinvertebrates. Oceanogr. Mar. Biol. Annu. Rev. 21: 195-282.35Hay, M. E. (1981). The functional morphology of turf-forming seaweds: Persistence instressful marine habitats. Ecology 62: 739-750.Hay, M. E. (1986). Associational plant defenses and the maintenance of species diversity:turning competitors into accomplices. Am. Nat. 128: 617-641.Holt, R. D. (1977). Predation, apparent competition, and the structure of preycommunities. Theor. Pop. Biol. 12: 197-229.Hruby, T., Norton, T. A. (1979). Algal colonization on rocky shores in the Firth of Clyde.J. Ecol. 67: 65-77.Johnson, W, S., Gigon, A., Gulman, S. L., Mooney, H. A. (1974). Comparativephotosynthetic capacities of intertidal algae under exposed and submergedconditions. Ecology 55: 450-453.Kastendiek, J. (1982). Competitor-mediated coexistence: interactions among three speciesof benthic macroalgae. J. Exp. Mar. Biol. Ecol. 62: 201-210.Keddy, P. A. (1989). Competition. Chapman and Hall. New York. pp. 202.Kennelly, S. 3. (1987). Inhibition of kelp recruitment by turfing algae and consequencesfor an Australian kelp community. 3. Exp. Mar. Biol. Ecol. 112: 49-60.Kennelly, S. J. (1989). Effects of kelp canopies on understorey species due to shade andscour. Mar. Ecol. Prog. Ser. 50: 2 15-224.Lindquist, J. L., Rhode, D., Puettmann, K. 3., Maxwell, B. D. (1994). The influence ofplant population spatial arrangement on individual plant yield. Ecol. Appi. 4: 518-524.Lubchenco, 3. (1978). Plant species diversity in a marine intertidal community: importanceof herbivore food preference and algal competitive abilities. Am. Nat. 112: 23-39.Lubchenco, J. (1983). Littorina and Fucus: effects of herbivores, substratum heterogeneityand plant escapes during succession. Ecology 64: 1116-1123.Lubchenco, 3., Gaines, S. D. (1981). A unified approach to marine plant-herbivoreinteractions. I. Populations and communities. Ann. Rev. Ecol. Syst. 12: 405-437.Mack, R. N., Harper, I. L. (1977). Interference in dune annuals: spatial pattern andneighborhood effects. J. Ecol. 65: 345-363.McLachlan, 3., Craigie, 3. S. (1966). Antialgal activity of some simple phenols. J. Phycol.2: 133-135.Menge, B. A., Sutherland, J. P. (1987). Community regulation: variation in disturbance,competition, and predation in relation to environmental stress and recruitment. Am.Nat. 130: 730-757.Olson, A. M., Lubchenco, 3. (1990). Competition in seaweeds: linking plant traits tocompetitive outcomes. 3. Phycol. 26: 1-6.36Padilla, D. K. (1984). The importance of form: differences in competitive ability,resistance to consumers and environmental stress in an assemblage of corallinealgae. J. Exp. Mar. Biol. Ecol. 79: 105-127.Paine, R. T. (1977). Controlled manipulations in the marine intertidal zone and theircontributions to ecological theory. Spec. Pubi. Acad. Nat. Sci. 12: 245-270.Paine, R. T. (1980). Food webs: linkage, interaction strength and communityinfrastructurre. J. Anim. Ecol. 49: 667-685.Paine, R. T. (1984). Ecological determinism in the competition for space. Ecology 65:1339-1348.Paine, R. T. (1990). Benthic macroalgal competition: complications and consequences. J.Phycol. 26: 12-17.Quadir, A., Harrison, P. J., DeWreede, R. E. (1979). The effects of emergence andsubmergence on the photosynthesis and respiration of marine macrophytes.Phycologia 18: 83-88.Reed, D. C. (1990). An experimental evaluation of density dependence in a subtidal algalpopulation. Ecology 71: 2286-2296.Reed, D. C., Foster, M. S. (1984). The effects of canopy shading on algal recruitment andgrowth in a giant kelp forest. Ecology 65: 937-948.Santelices, B., Ojeda, F. P. (1984). Effects of canopy removal on the understory algalcommunity structure of coastal forests of Macrocystis pyrifera from southern SouthAmerica. Mar. Ecol. Prog. Ser. 14: 165-173.Schiel, D. R., Foster, M. S. (1986). The structure of subtidal algal stands in temperatewaters. Oceanogr. Mar. Biol. Annu. Rev. 24: 265-307.Schoener, T. W. (1983). Field experiments on interspecific competition. Am. Nat. 122:240-2 85.Schonbeck, M. W., Norton, T. A. (1980). Factors controlling the lower limits of fucoidalgae on the shore. J. Exp. Mar. Biol. Ecol. 43: 13 1-150.Shaughnessy, F. J. (1994). Population differentiation of two sympatric species of redalgae, Mazzaella splendens and Mazzaella linearis, in Baridey Sound, BritishColumbia, Canada. Ph. D. Thesis. University of British Columbia.Sousa, W. P. (1984). The role of disturbance in natural communities. Ann. Rev. Ecol.Syst. 15: 353-391.Sousa, W. P. (1984). Intertidal mosaics: Patch size, propagule availability and spatiallyvariable patterns of succession. Ecology 65: 19 18-1935.Steinberg, P. D. (1985). Feeding preferences of Tegukifuneblaris and chemical defensesof marine brown algae. Ecol. Monogr. 55: 333-349.37Steneck, R. S. (1985). Adaptations of crustose coralline algae to herbivory: patterns inspace and time. In: Toomey, D. F., Nitecki, M. H. (eds.) Paleoalgology:Contemporary Research and Applications. Springer-Verlag, Berlin. pp. 352-366.Tilman, D. (1994). Competition and biodiversity in spatially structured habitats. Ecology75: 2-16.Turkington, R., Harper, J. L. (1979). The growth, distribution and neighbourrelationships of Trifolium repens in a permanent pasture. I. Ordination, pattern andcontact. J. Ecol. 67: 201-218.Underwood, A. J. (1980). The effects of grazing by gastropods and physical factors on theupper limit of distribution of intertidal macroalgae. Oecologia 46: 201-2 13.Underwood, A. J., Denley, E. J. (1984). Paradigms, explanations, and generalizations inmodels for the structure of intertidal communities on rocky shores. In: Strong, D.R., Simberloff, D., Abele, L. G., Thistle, A. B. (eds.) Ecological communities:Conceptual issues and the evidence. Princeton University Press. New Jersey. pp.151-180.Vandermeer, J. (1980). Indirect mutualisms: variations on a theme by Stephen Levine.Am. Nat. 116: 441-448.Wilkinson, L., Hill, M. A., yang, E. (1992). SYSTAT: Statistics, version 5.2.1 edition.SYSTAT. Evanston, IL, USA.Winer, B. J. (1971). Statistical principles in experimental design. McGraw-Hill. NewYork.38Table 2.1 Results of ANCOVA on fucoid recruitment in the different Mazzaella pruningplots. The ANCOVA was applied to each sampling date. The covariate is Mazzaellapercent cover in each plot (M-cover). Three treatments are ‘total pruning’, ‘partialpruning’ and no pruning (control), see text for details.October 1993 February 1994 April 1994Source ofvariation df MS F 12 MS F 12 MS F 12FucusTreaunent 2 3.48 1.51 0.242 1.60 0.90 0.419 0.07 0.03 0.967M-cover 1 23.12 10.02 0.004 34.29 19.2 0.000 20.06 9.41 0.005Error 23 2.31 1.78 2.13PelvetiopsisTreatment 2 2.23 0.84 0.444 0.19 0.12 0.889 0.60 0.51 0.608M-cover 1 11.67 4.42 0.047 14.12 8.78 0.007 21.18 17.87 0.000Error 23 2.64 1.61 1.1939Table 2.2 Comparisons of longevity among the distance groups in each species andbetween F. distichus and P. lirnitata. at each distance group. Means are number ofmonths.CONTACT CLOSE FAR One-way(0 cm) (0.3- 0.7 cm) (>2.0 cm) ANOVAMean Mean Mean SE NFucus 2.19 0.95 16 5.42 0.53 52 3.57 0.51 56 0.004t-test (p) 0.086 * 0.322 0.175Pelvetiopsis 5.00 1.50 6 4.62 0.51 53 4.25 0.56 44 0.831Tukey’s HSD on FucusCONTACT CLOSE FARCONTACT 1.000CLOSE 0.008 1.000FAR 0.405 0.031 1.000* Separate variances are used due to the severely unequal sample sizes (Wilkinson et al.1992).40Table 2.3 Results of multivariate statistics as a preplanned multiple comparison fortesting three hypotheses. A Bonferroni adjusted probability value (p=0.05 / 4 = 0.0 125)was used to compare each pair of treatments.Wilk’slambda 1iCanopy effect(Clear vs. Dark) 0.541 9.320 2, 22 0.001Scouring effect(Control vs. Clear) 0.974 0.293 2, 22 0.749Allelopathic effect(Darkvs.Fucus) 0.859 1.801 2,22 0.189(Dark vs. Pelvetiopsis) 0.9 14 1.029 2, 22 0.37441r=-O.423n=1 343- p26 mm.447060LU50C)I—zLU0LU03020Fig. 2.4 The effect of pruning Mazzaella blade on Mazzaella percent cover in the sameexperimental plots (lOx 10 cm).OCT93 FEB 94 APR 94454Fig. 2.5 The effect of Mazzaella pruning on fucoid recruitment. A. number of fucoidrecruits actually occurring in the plots. B. number of fucoid recruits adjusted by Mazzaellapercent cover (the covariate) in each plot at each sampling date. These values were used inthe ANCOVA. Data are means +SE of 9 replicates. PT for Pelvetiopsis in the totalpruning plots, PP for Pelvetiopsis in the partial pruning plots, PC for Pelvetiopsis in thecontrol plots; PT, FP and FC for Fucus in the respective plots.A543PTPPPCFTAFPFC210B3210OCT93 FEB94 APR9446C”EC)ci)0CoCl)E0coFig. 2.6 Changes in Mazzaella biomass (g) under each treatment after 2 months. Clifor control, CLE for the clear artificial plant, DRK for the dark artificial plant, FUC forFucus, and PEL for Pelvetiopsis. Data are means +SE (n=5 for CLE, FUC and PEL, n=6for DRK, n=7 for CTL).3210CTL CLE DRK FUC PELAfter experiment0 Before experimentTREATM ENTS475.a)Cl)Darkc,)-5.C-)>,-io ØCIear1 2 3 4 5 6Size ClassFig. 2.7 The effect of fucoid shading on Mazzaella size class. Data are means +SE (n=5for clear and n=6 for dark artificial plant).DESICCATIONDESI CCATIONDESICCA11ONLimitedspaceforholdfastexpansion?Biomechanicaldifference?Fig.2.8Diagramofpotential factorsaffectingfucoidmortality.SeeDISCUSSIONforfurtherexplanation.—LETHALFACTOR4—NON-LETHALFACTORWAVEWAVEWAVEWAVE2.52.01.51.00.50cmDistancefromMazzaellaturf0049(I)0Cl)Cl)LUI—U)-J0U)>-I00.5 1.0 1.5 2.0 3.0 4.0C.)z0II—LU0010Distance (cm) from MazzaellaFig. 2.9 Fucus survivorship curves in relation to the changing effects of competition andphysical stress with distance from the edge of a Mazzaella turL The shaded area representsthe probability of Fucus survival.50CHAPTER 3PREFERENTIAL FEEDING BY A LITTORINID: IMPLICATIONS FORITS ROLE IN A HIGH INTERTIDAL ALGAL COMMUNITYINTRODUCTIONThe importance of biological factors in controlling the abundance and distribution ofalgal species is generally thought to decrease with increasing tidal height in rocky shores.Physical factors (e.g., disturbance, desiccation) have been shown to be more important instructuring upper intertidal communities, while algal abundance in the lower intertidal levelsappears governed principally by herbivory and competition (Castenholz 1961, Connell1972, 1975, Chapman 1973, Menge 1978, Underwood 1980). Many of the studiesdealing with herbivory and its influence on algal community structure have been confinedto the low and mid intertidal zones. Few authors have shown experimental evidence of theimpact of herbivory on algal abundance in upper intertidal zones (Dayton 1975, Robles andCubit 1981, Cubit 1984, Farrell 1991). The relative importance of biological and physicalfactors requires more experimental field tests to verify its application to upper intertidalzones.In the uppermost intertidal zones of rocky shores dominated by three perennialmacrophytes, Mazzaella cornucopiae, Pelvetiopsis limitata and Fucus distichus, dramaticincreases of littorinid snails were observed each summer in these habitats. The snails weresmall (<4 mm in shell length) and seemed to be restricted to upper exposed intertidal areas(Boulding and Van Aistyne 1993, personal observation). Since the foraging behavior ofthis species has not been described (Norton et al. 1990, Boulding and Van Aistyne 1993),its potential role in the algal community is not known.51Littorinid snails are primarily herbivorous and are able to feed on a variety ofmacro- and micro-algae in numerous habitats using their versatile radulae (see reviews byNewell 1970, Underwood 1979, Hawkins and Hartnoll 1983, Norton et al. 1990). Somelittorines are highly selective grazers demonstrating strong preferences for some speciesand rejecting others after prolonged periods of starvation (Norton et al. 1990). Authorshave recognized feeding preference by measuring two components of diet, edibility andattractiveness (Nicotri 1980, Watson and Norton 1985). The former, which is the primarymeasure of preference, reflects both the speed with which a given food item satisfies thephysiological needs of a herbivore and the ease with which that item can be handled andingested. Attractiveness is largely dependent on the capacity of the herbivore to detect plantchemicals and the non-nutritive characteristics of the plant as a habitat (Nicotri 1980).These two factors, when tested together, have shown a correlation in some studies (Watsonand Norton 1985, 1987; used Littorina littorea, L. inariae, L obtusata); in others nocorrelation was found (Nicotri 1980; used an isopod, Idotea baltica).Adaptation of intertidal littorines to air exposure in relation to their activity andforaging has been described by many authors (Newell et al. 1971, McMahon and Russell-Hunter 1977, Newell 1979, Underwood 1979, Underwood and Chapman 1985, Voltorinaand Sacchi 1990). Newell et al. (1971) demonstrated that L. littorea feeds mainly whenmoistened by the tide and is quiescent when exposed to air. Similar results have beenreported using L. scutulata and L. sitkana from upper intertidal zones on Vancouver Island,Canada, indicating that limited feeding activity occurs during day time emergence whereasactive feeding occurs in the early morning emergence, especially on moistened surfaces(Voltorina and Sacchi 1990). In contrast, McMahon (1990) indicated that some eulittoralspecies of littorines displayed adaptation shown by active movement and foraging duringday time emergence. Because of contrasting results, it is difficult to generalize aboutfeeding behavior of the upper intertidal littorines. Underwood and Chapman (1985) havethus pointed out that care should be taken when examining intertidal snail behavior because52ambiguous results can be obtained when they occur under different environmentalconditions, including tidal height, topography and substratum.The objective of this chapter is to investigate littorine distributions in the field andfeeding preference of the snails on the 3 dominant algae in the laboratory. The role oflittorine herbivory as a potential biotic factor affecting the structure of the upper intertidalalgal community is discussed. Experiments were designed to address the followingquestions: (1) Are there temporal and spatial variations in the distribution of the littorinids?(2) Which alga is preferentially eaten when presented separately to the littorinids? I use theterm ‘single-diet’ for this experiment hereafter. (3) Which alga is preferentially eaten whenall algae are simultaneously presented to the littorinids? I use the term ‘multiple-diet’ forthis case. Both edibility and attractiveness of the algae were tested. (4) How is feedingbehavior and movement of the littorinids affected by simulated tidal conditions (low orhigh) and light (present or absent)?A field experiment on feeding preference was not attempted because of (1)difficulties in controlling such a small herbivore in the wave-exposed sites, (2) possiblecage effects due to the small size of holes in metal mesh needed to retain the snails (Denleyand Dayton 1985), and (3) the ineffective non-cage method to exclude littorinids, e.g., theuse of copper-based antifouling paints (Cubit 1984).MATERIALS AND METHODSSampling site and organismsThe algae and snails were collected from the upper intertidal zone at NudibranchPoint. Due to limited space and to avoid the impact of manipulated density, naturaldensities of snails were determined at Prasiola Point, 0.4 km south of Nudibranch Point,53where physical and biological conditions (e.g., wave-exposure, slope, algal flora) weresimilar to the collection site.There is an unresolved taxonomic problem for the Littorina species used in thisstudy. Boulding et al.(1993) distinguished the taxon used in this study from other relatedspecies in the northeastern Pacific coast, such as L. sitkana and L. scutulata, based onmorphological and allozyme data, and suggested this taxon was an undescribed species.The littorinid in this study could not be identified as a known species for the followingreasons. First, there were habitat differences between Littorina sp. and L subrotundatawhich occurs commonly in estuaries (Boulding et al. 1993), even though Littorina sp. isthe species most closely related to or conspecific with L. subrotundata (Reid and Golikov1991). Secondly, Littorina sp. used in this study have non-planktonic larvae (i.e., directdevelopment) (Boulding et al. 1993), which is different from the planktonic larvae of L.scutulata , one of the more common species in the northeastern Pacific (Behrens 1971,Buckland-Nicks et al. 1973, Mastro et al. 1982). Thirdly, L sitkana resides in moresheltered and lower habitats, as well as differing in size and foot color from the species(Buckland-Nicks et al. 1973, Boulding and Van Alstyne 1993). Therefore, I havefollowed Boulding’s suggestion and used the name Littorina sp.Juvenile L. scutulata or L. plena may have been mistakenly included in theexperiments although their numbers were low (<3% of the total snails used), and reflectthe in situ species abundance of littorinids at the study site.Natural densities of snailsSnail densities were monitored at Prasiola Pt., at 6-8 week intervals for 16 months.Three transect lines (each 3 m long) were marked along the same tidal height at the studysite. Areas for these transects included variable habitat conditions, such as mixed ormonostands of the three macrophytes, bare rock, and variable barnacle cover. Snails from54a lOxlO cm quadrat placed at each of 6 randomly selected points (different points for eachsampling date) on each transect line were vacuumed for 12 seconds using a rechargeablehand vacuum (Hoover Wet and Dry), counted and returned to the original plot. Another setof collections was made to estimate snail densities in monospecific patches of the threedominant algae. In each of 5 marked (but randomly selected initially) monospecific patchesper species (5 replicates per algal species), a lOxlO cm quadrat was randomly placed ateach sampling date, and snails were counted using the same collecting protocol.Data were analyzed using two-way analysis of variance to examine both temporaland spatial distribution (among monospecific patches). Another two-way ANOVA wasapplied to data from the transect lines (natural densities from the general habitat) to assesstemporal and spatial (among transect lines) distribution. Snail densities from one samplingdate to another were treated independently because they were not obtained from fixedquadrats.Cochran’s test was performed to check homogeneity of variance (Winer 1971).Plots of residuals, where applicable, were examined after each ANOVA to check if errorterms were normally distributed. These procedures were applied to all univariate statisticsin this study. Data were square-root transformed, where necessary, to meet the assumptionof equal variances among treatments. All data analyses were performed using SYSTAT,version 5.2.1 for Macintosh, (Wilkinson et al. 1992).Single-diet experimentsThis experiment was conducted in June 1992. Littorina sp. was collected with thehand vacuum and maintained in running seawater tanks without any added food for 3 daysbefore each alga was added. Cages were made from plastic pot liners (3090 cm3), intoeach of which four windows were cut. Nylon mesh was attached over each window aswell as over the open top of the cages. Healthy, nongrazed, nonreproductive thalli of each55macrophyte were presented individually to snails in separate experimental cages. Icollected short fucoids (3-5 cm in length), so that a similar surface area for each specieswas exposed to herbivores. Thalli (blotted wet weight 3.0±0.03 g per cage) of each algawere placed in each of 5 cages containing snails and in each of 3 control cages withoutsnails. Each thallus was tied to the bottom of the cage with a thin monofilament hook toprevent it from floating when cages were submerged. The 24 cages were randomly placedin three aerated, running sea water tanks (0.134 m3).Tide and light conditions were created to approximate summer air-exposed times foralgae and snails in the upper intertidal zones of British Columbia. High tide was simulatedby attaching 6 pieces of cork to the outside of each cage so that it floated with 3/4 of thecage submerged for 6 hours a day (8:00-11:00 AM and 8:00-11:00 PM). This ensured thatpart of the cage was out of water and allowed snails to choose to be in or out of the water.Low tide conditions were achieved by taking the cages out of the water for 18 hours eachday (11:00 AM-8:00 PM and 11:00 PM-8:00 AM). Light was controlled as follows: 12 hdays and 12 h nights, and consequently combinations of tide and light regime, such asday/high, day/low, night/high and night/low, alternatively were achieved.I placed 75 snails, 3-4 mm in length, in each treatment cage reflecting the averagenatural density during summer months. After 5 days, thalli were removed, blotted,weighed and returned to their original cage. After another 5 days (10 days in total), thalliwere weighed again and the experiment terminated. The grazing effect was determined bycomparing algal weights between treatment (with snails) and control (without snails)groups.Data analysis employed 2x3x2 ANOVA (Snail x Algae x Time) with repeatedmeasures on Time factor. This enabled me to interpret the data in various ways. The Snaileffect, which has 2 levels, present (=treatment) and absent (=control), tested whetherconsumption by snails actually occurred. The Snail x Algae interaction indicates thepresence or absence of feeding preference among algae. The result of Snail x Algae x Time56interaction indicates whether the consumption pattern or preference was consistent over thecourse of the feeding trial. A simple main effect as a post hoc analysis was applied whenthe Snail x Algae interaction was significant (Kiockars and Sax 1990).Multiple-diet experimentsThe treatment consisted of 16 cages, each containing 120 snails and about 3.0 g offood per cage in units of 1.0±0.02 g blotted wet weight of each alga. Seven cages,containing the same amount of food but no snails, were used as the control. I increased thenumber of herbivores to obtain more obvious visual evidence for the part of thallus actuallyeaten than in the single-diet experiment. This density was still within the range of naturaldensities in the field. Thalli of each species were attached (in the same way as the single-diet experiment) alternately around the perimeter of each cage, so that each algal specieswas the same distance away from the snails initially located in the center of each cage. Thetidal regime and light control were the same as in the single-diet experiments. Only 14treatment cages were used for the analysis because of mishandling of some thalli at the endof the experiment. The experiment ran for 10 days in August 1992 with a singlemeasurement at day 10.Edibility was measured by comparing algal weight between the treatments andcontrols. However, since two or more foods were held in the same experimental unit(e.g., container or cage), consumption of one type of food was not independent ofconsumption of other types. Therefore, ANOVA or t-tests were not appropriate ways toanalyze the data because the assumption of independence of response variables forunivariate statistical tests (t-tests, ANOVA) was invalid (Peterson and Renaud 1989). Inorder to avoid problems where ANOVA was incorrectly applied (Vadas 1977, Schiel 1982,Paul et al. 1987), or where no statistic was used (Barker and Chapman 1990) in multiple-diet experiments (see Peterson and Renaud 1989 for review), I used a two-sample57(treatment and control) Hotelling’s T2 test with three dependent variables (algal species), amultivariate analog of the Student’s t-test. Since Hoteffing’s T2 is distributed as F, F isused to determine critical values (Tabachnick and Fidell 1989). When results weresignificant by Hotelling’s T2 test, I applied univariate t (or F) statistics to determine whichvariance(s) contributed most to the significant Hotelling’s T2.Snail behaviors and tide/light effectsDuring the multiple-diet experiment, snails that attached to each algal species within15 minutes after snail introduction were counted to assess the attractiveness of algae. Theresult of the snails’ initial movement towards food (attractiveness) was compared with theactual amount of food eaten (edibility) at the end of the experiment to determine acorrelation between these two quantities. In each of 14 cages, the 3 algae were ranked bythe number of snails attached. The Kruskal-Wallis test was used on the ranked data,followed by the Kolmogorov-Smirnov test if the former test was significant.The multiple-diet experiment was used to assess potential effects of tide and lightregimes on feeding behavior of the littorinid. The number of snails on each algal specieswas subsequently counted four times each day; one for each tide/light combination. Thesecounts proceeded for 9 days. These data were evaluated only for those species wheresignificant consumption(s) occurred. The reason for this is to interpret these data withregard to the snails’ foraging behavior corresponding to the tide/light regimes.For data analysis, I used two-way ANOVA with repeated measures on both tide (2)and light (2) factors. Tests were done for samples of 1, 4, 7 days after the beginning of theexperiment. These sampling dates, although arbitrarily chosen, represent changes of snailbehavior according to tide and light in the course of feeding time.58RESULTSNatural densities of snailsSnail densities in the upper intertidal zones at Prasiola Point varied significantlyover sampling dates (ANOVA, F(s,los)=33.336, p Pelvetiopsis > Fucus (F(1,9)=19.6l,p either Fucus orPelvetiopsis, p=O.8954. for Fucus and Pelvetiopsis; Fig. 3.4). This attractiveness of algaecorrelated with the results of thallus loss (edibility) in the multiple-diet experiment in termsof the same most preferred species. However, the rank order of two fucoids in themultiple-diet experiment for edibility (Pelveliopsis > Fucus) was reversed for attractiveness(Fucus > Pelvetiopsis); however, the degree of difference between the two species wassmall in both cases (Fig. 3.4).Results of the littorine movements according to the tide/light regime are shown inTable 3.2. I used the number of snails attached to M. cornucopiae because significantgrazing only occurred on this alga. More snails averaged over ‘day’ and ‘night’ wereattached to M. cornucopiae at ‘low tide’ than ‘high tide’ for every sampling date (Fig. 3.5;Table 3.2, Tide effects p=O.Ol9, p=O.Ol5, p=O.OO7; dayl, day4, day7, respectively). Onthe other hand, light did not affect snail movement on any of these dates. In particular,snails’ movement towards M. cornucopiae was distinctive when night high tide switched tonight low tide (the order of tide/light regime for each day shown in Fig. 3.5 corresponds tothe actual order in the experiment). The pattern that appeared with the tidal shift from highto low at ‘night’ was not consistent during the ‘day’ time; the same pattern was shown onlyon day 1, not days 4 and 7 (Tide x Light interactions were significant only on days 4 and7).61DISCUSSIONRepeated measures on the amount of food consumed showed a significantinteraction between food preference and time. This indicates that food preference can varywith length of feeding time. In many feeding preference studies, only results from a singlemeasurement have been considered and the variation in grazing pattern in the course of thefeeding trial was typically ignored. However, a short feeding time may allow foruncomplicated estimation of consumption due to less autogenic change in the food materialsused (Peterson and Renaud 1989). In a natural situation, herbivores face a variety of foodsover an extended period of time. Therefore, I suggest that assessment of algalconsumption over time is important to reduce the risk of misinterpretation of grazing orpreference patterns. This is particularly critical when differences in preference among foodchoices are not large.The responses of Littorina sp. to changes in tide and light condition were notconsistent throughout the experiment (Day 1, 4 and 7). Nevertheless, the greatest numberof snails appeared on thalli found in the ‘low tide’ at ‘night’. Particularly there were activemovements to the food when ‘high tide’ shifted to ‘low tide’ at ‘night’. However, thesedata are a measurement of snail behavior or movement, not a measurement for grazing.Thus, there is no direct evidence in the data for a relationship between littorinid movementand foraging. Nonetheless, a correlation between these two quantities can be found in afew other studies (Newell et al. 1971, Underwood and Chapman 1985, Watson andNorton 1987). Since only M. cornucopiae was significantly grazed, the number of snailswhich appeared on this alga could be partly related to the snail’s foraging activity. if snailswere attached to the red alga just for the benefit of moisture during ‘low tide’, more snailswould be expected to move toward the thalli in ‘day time’ (relatively greater desiccation)than in ‘night time’. However, no evidence for this was observed throughout theexperiment although laboratory conditions could not completely mimic desiccation levels in62natural habitats. Results of the present study support McMahons (1990) results that activemovement and foraging of eulittoral snails occur during tidal emergence. In addition, ourresults are in accordance with the feeding behaviors of two other local species, L. scutulataand L. sitkana, in which the greatest consumption of foods occurred during low tide in theearly morning (Voltorina and Sacchi 1990).The results in this study consistently suggest that M. cornucopiae should be themost palatable food for Littorina sp. Results of the attractiveness trials were similar. Iconclude that Littorina sp. had no consistent preference between the two fucoids. In thesingle-diet experiment, F. distichus was consumed slightly more than P. limitata and wasselected over P. limitata for attractiveness in the multiple-diet experiment. In contrast, inthe multiple-diet experiment more P. limitata was consumed than F. distichus.A variety of cues have been suggested as responsible for attracting the littorines to aparticular alga. In the multiple-diet experiment, it is unlikely that the phenomenon of snailsfollowing previously laid tracts (deposited by one snail and followed by others) affects theresults. If the initial foraging were random (Norton et al. 1990), then significantdifferences in choice are highly unlikely to occur due to “tracking. If movement is inresponse to chemical or other cues, tracks laid by early arrivals will be followed by latersnails; presumably this same behaviour occurs on the shore.Why is the red alga chosen over the fucoids in the laboratory as well as in the field?In the present study, the littorines’ choice may have been affected by phenolic compounds,which are known to deter feeding by herbivorous snails on some marine brown algaeincluding fucoids (Hay and Fenical 1988). Steinberg (1985) reported that F. distichus andP. limitata contained similar amounts of tissue phenolics (4.35±0.28% and 4.93±0.39%dry mass, respectively) and demonstrated that these two fucoids were least preferred byTegulafunebralis, the black turban snail, among 13 common Phaeophyta from centralCalifornia. Secondary metabolites of red algae are relatively poorly known as herbivoredeterrents except for a few species (e.g., elatol in Laurencia) (see the review by Hay and63Fenical 1988). No studies appear to have reported on chemical deterrents in the genusMazzaelia (previously Iridaea). The absence of chemical deterrents may explain theimmediate (e.g., 15 mm) attraction of Littorina sp. to M. cornucopiae at the start of themultiple-diet experiment.Thallus toughness may be related to feeding preferences although no attempt wasmade to measure this characteristic. The relatively softer texture and thinner thallus of M.cornucopiae may have been one of the reasons why M. cornucopiae was selected over themore solid, thicker fucoids. This suggestion is supported by visual observations of thalliafter each experiment. Only blade tops (relatively thinner than the bottom part of the blade)of M. cornucopiae were heavily eaten. A few studies on the relationship between thallustoughness and feeding preferences (Steinberg 1985, Pennings and Paul 1992) suggest thatthe specific herbivore determines the relative importance of plant toughness and chemicaldefenses as feeding deterrents. For example, larger species of littorinids, e.g., L. littorea,have been known to feed on fucoid algae (Lubchenco 1983, Barker and Chapman 1990).In addition to being the preferred food, the dense turf of M. cornucopiae mayprovide a better refuge for Littorina sp., especially in wave-exposed sites (Boulding andVan Alstyne 1993). Small snails may be better protected from dislodgment by moving tothe bottom of Mazzaella turf during high tide rather than hiding beneath fucoid thalli whichexhibit a sweeping movement. However, while Mazzaella may be a better refuge, thisstudy indicates that Mazzaella was a preferred food. Furthermore, there were many moresnails in Mazzaella beds than on Fucus and Pelvetiopsis on the shore at low tide (when allthe data were collected) when there is no stress for dislodgment caused by wave action.Therefore, the higher abundance of snails on Mazzaella observed in the field is probablydue to a combination of both preferred food and better habitat.The present study suggests that the summer decline of the M. cornucopiaepopulation (Fig. 5.1) is partially caused by littorinid herbivory. Desiccation may alsoreduce the abundance of this red alga. Olson (1985, 1992) observed that blades of M.64cornucopiae occurring on the upper margin of its habitats in Oregon, U.S.A. were usuallybleached, and a portion of bleached blade disappeared at the end of summer. She arguedthat the upper limit of this population was affected by a combination of desiccation andherbivory by limpets. I observed that bleached blades commonly occurred in the upperzone whereas loss of non-bleached thalli occurred throughout the population. It hasgenerally been assumed that the importance of physical factors is higher in the upperintertidal shore and that of biological factors is greater in the lower shore (Castenholz 1961,Connell 1972, Chapman 1973, Menge 1978, Underwood 1980). The validity of thisparadigm has been questioned (Dayton 1975, Cubit 1984, Underwood and Denley 1984,Farrell 1991). My data strongly suggest that the most abundant herbivore, Littorina sp.,could decrease Mazzaella biomass which may, in turn, affect interactions among the threealgal dominants. For example, the dense turf of Mazzaelkx prevents recruitment of bothFucus and Pelvetiopsis in this habitat (Chapter 2). Summer decline of the Mazzaellapopulation and its slow recovery over the winter may open up space for fucoid recruitment.Active recruitment of both Fucus and Pelvetiopsis during fall (i.e., October; Fig. 5.1) mayassist these two species in maintaining their place in this community.65REFERENCESBarker, K. M., Chapman, A.R.O. (1990). Feeding preferences of periwinkles among fourspecies of Fucus. Mar. Biol. 106: 113-118.Behrens, S. (1971). The distribution and abundance of the intertidal prosobranchs Littorinascutulata (Gould 1849) and L. sitkana (Phillipi 1845). M.Sc. Thesis. Univ. ofBritish Columbia. Vancouver, British Columbia.Boulding, E. G., Van Aistyne, K. L. (1993). Mechanisms of differential survival andgrowth of two species of Littorina on wave-exposed and on protected shores. J.Exp. Mar. Biol. Ecol. 169: 139-166.Boulding, E. G., Buckland-Nicks, J., Van Alstyne, K. L. (1993). Morphological andallozyme variation in Littorina sitkana and related Littorina species from theNortheastern Pacific. Veliger 36: 43-68.Buckland-Nicks, J., Chia F. S., Behrens, S. (1973). Oviposition and development of twointertidal snails, Littorina sitkana and Littorina scutulata. Can. 3. Zool. 51: 359-365.Castenholz, R. W. (1961). The effect of grazing on marine littoral diatom populations.Ecology 42: 783-794.Chapman, A. R. 0. (1973). A critique of prevailing attitudes on the control of seaweedzonation on the sea shore. Bot. Mar. 16: 80-82.Connell, J. H. (1972). Community interactions on marine rocky intidal shores. Ann, Rev.Ecol. Syst. 3: 169-192.Connell, J. H. (1975). Some mechanisms producing structure in natural communities: amodel and evidence from field experiments. In: Cody, M. L., Diamond, 3. (eds.)Ecology and ecolution of communities. Belknap, Cambridge, p. 460-490.Cubit, J. D. (1984). Herbivory and the seasonal abundance of algae on a high intertidalrocky shore. Ecology 65: 1904-1917.Dayton, P. K. (1975). Experimental evaluation of ecological dominance in a rockyintertidal algal community. Ecol. Monogr. 45: 137-159.Denley, E. 3., Dayton, P. K. (1985). Competition among macroalgae. In: Littler, M. M.,Littler, D. S. (eds.) Handbook of phycological methods. Ecological field methods:Macroalgae. Cambridge University Press, Cambridge, p. 511-530.Farrell, T. M. (1991). Models and mechanisms of succession: an example from a rockyintertidal community. Ecol. Monogr. 61: 95-113.Hawkins, S. J., Hartnoll, R. G. (1983). Grazing of interdal algae by marine invertebrates.Oceanogr. Mar. Biol. Ann. Rev. 21: 195-282.Hay, M. E., Fenical, W. (1988). Marine plant-herbivore interactions: The ecology ofchemical defense. Ann. Rev. Ecol. Syst. 19: 111-145.66Klockars, A. J., Sax, G. (1990). Multiple comparisons. Sage Publications, Inc.Newbuny Park, California.Lubchenco, 3. (1983). Littorina and Fucus: Effects of herbivores, substratum heterogeneityand plant escapes during succession. Ecology 64: 1116-1123.McMahon, R. F. (1990). Thermal tolerance, evaporative water loss, air-water oxygenconsumption and zonation of intertidal prosobranchs: a new synthesis.Hydrobiologia 193: 241-260.McMahon, R. F., Russell-Hunter, W. D. (1977). Temperature relations of aerial andaquatic respiration in six littoral snails in relation to their vertical zonation. Biol.Bull. 152: 182-198.Mastro, E., Chow, V., Hedgecock, D. (1982). Littorina scutulata and Littorinaplena:sibling species status of two prosobranch gastropod species confirmed byelectrophoresis. Veliger 24: 239-246.Menge, B. (1978). Predation intensity in a rocky intertidal community. Oecologia 34: 1-16.Newell, R. C. (1970). Biology of intertidal animals. Lagos Press, London.Newell, R. C. (1979). Biology of intertidal animals. Marine Ecological Surveys Ltd.,Faversham, Kent.Newell, R. C., Pye, V. I., Ahsanullah, M. (1971). Factors affecting the feeding rate of thewinkle Littoriiw littorea. Mar. Biol. 9: 138-144.Nicotri, M. E. (1980). Factors involved in herbivore food preference. 3. Exp. Mar. Biol.Ecol. 42: 13-26.Norton, T. A., Hawkins, S. I., Manley, N. L., Williams, G. A., Watson, D. C. (1990).Scraping a living: a review of littorinid grazing. Hydrobiologia 193: 117-138.Olson, A. M. (1985). Early succession in beds of the red alga, Iridaea cornucopiae Post. &Rupr. (Gigartinaceae): Alternate pathways. M.S. Thesis. Oregon State University.Corvallis, Oregon.Olson, A. M. (1992). Evolutionary and ecological interactions affecting seaweeds. Ph.D.Thesis. Oregon State University. Corvallis, Oregon.Paul, V. J., Littler, M. M., Littler, D. S., Fenical, W. (1987). Evidence for chemicaldefense in tropical green algae Caulerpa ashrneadii (Caulerpaceae: Chiorophyta):isolation of new bioactive sesquiterpenoids. 3. Chem. Ecol. 13: 1171-1185.Pennings, S.C., Paul, V. 3. (1992). Effect of plant toughness, calcification, and chemistryon herbivory by Dolabella auricularia. Ecology 73: 1606-16 19.Peterson, C. H., Renaud, P. E. (1989). Analysis of feeding preference experiments.Oecologia 80: 82-86.Reid, D. G., Golikov, A. N. (1991). Littorina naticoides, new species, with notes on othersmooth-shelled Littorina from the Northeastern Pacific. Nautilus 105: 7-15.67Roble, C. D., Cubit, J. (1981). Influence of biotic factors in an upper intertidalcommunity: dipteran larvae grazing on algae. Ecology 62: 1536-1547.Schiel, D. R. (1982). Selective feeding by the echinoid, Evechinus chioroticus, and theremoval of plants from subtidal algal stands in Northern New Zealand. Oecologia54: 379-388.Steinberg, P. D. (1985). Feeding preferences of Tegukifunebralis and chemical defensesof marine brown algae. Ecol. Monogr. 55: 333-349.Tabachnick, B. 0., Fidell, L. S. (1989). Using multivariate statistics. 2nd edition. Harper& Row Publishers, New York.Underwood, A. J. (1979). The ecology of intertidal gastropods. Adv. Mar. Biol. 16: 111-210.Underwood, A. J. (1980). The effect of grazing by gastropods and physical factorson the upper limits of distribution of intertidal macroalgae. Oecologia 46: 201-213.Underwood, A. J., Denley, E. J. (1984). Paradigms, explanation and generalizations inmodels for the structure of intertidal communities on rocky shores. In: Strong, D.R., Simberloff, D., Abele, L. G., Thistle, A. (eds.) Ecological Communities:Conceptual Issues and the Evidence. Princeton University Press, New Jergy, pp.151-180.Underwood, A. J., Chapman, M. G. (1985). Multifactorial analyses of directions ofmovement of animals. J. Exp. Mar. Biol. Ecol. 91: 17-43.Vadas, R. L. (1977). Preferential feeding: an optimization strategy in sea urchins. Ecol.Monogr. 47: 337-371.Voltorina, D., Sacchi, C. F. (1990). Field observatios on the feeding habits of Littorinascutulata Gould and L. sitkana Philippi (Gastropoda, Prosobranchia) of southernVancouver Island (British Columbia, Canada). Hydrobiologia 193: 147-154.Watson, D. C., Norton, T. A. (1985). Dietary preferences of the common periwinkle,Littorina littorea (L). J. Exp. Mar. Biol. Ecol. 88: 193-211.Watson, D. C., Norton, T. A. (1987). The habit of feeding preferences of Littorinaobtusata (L.). and L. inariae Sacchi et Rastelli. J. Exp. Mar. Biol. Ecol. 112: 61-72.Wilkinson, L., Hill, M. A., yang, E. (1992). SYSTAT: Statistics, Version 5,2.1 Edition,Systat, Inc., Evanston.Winer, B. J. (1971). Statistical principles in experimental design. McGraw-Hill BookCompany, New York.68Table 3.1 Single-diet experiments. Results of three-way ANOVA, a Snail x Algae xTime (2x3x2), with repeated measures on the Time factor.Source ifBetween SubjectsSnail .399 1 12.00 .003Algae .247 2 7.41 .005Snail x Algae .207 2 6.22 .009Error .033 18Within SubjectsTime .032 1 14.68 .001TimexSnail .035 1 15.93 .001Time xAlgae .007 2 2.95 .078Time x SnailxAlgae .014 2 6.30 .008Error .002 1869Table 3.2 Effects of light and tide on snail behaviors. Results of two-way ANOVA withrepeated measures on both light (2) and tide (2) factors. A separate analysis was applied oneach sampling date (Days 1, 4, 7) during the multiple-diet experiment.Source EWithin Subjects DAY 1Light 33.063 1 .784 .390Error 42.196 15Tide 297.563 1 6.883 .019Error 43.229 15LightxTide 30.250 1 1.419 .252Error 21.317 15Within Subjects DAY 4Light .562 1 .026 .874Error 21.563 15Tide 72.250 1 7.487 .015Error 9.650 15Lightx Tide 256.000 1 15.547 .001Error 16.467 15Within Subjects DAY 7Light 21.391 1 .865 .367Error 24.724 15Tide 153.141 1 9.567 .007Error 16.007 15Lightx Tide 221.266 1 12.158 .003Error 18.199 1580 70 60050040Cl) W30I C’)20U10 019911992Fig.3.1NaturaldensitiesofsnailsatPrasiolaPt.Dataaremeans+SEof 5monospecificpatchesofeachalgaandof 18randomlyselectedpiots fromtransectlinesinthegeneral habitat (3 transectsx6points). GENforthegeneral habitat,MAZforM. cornucopiae,FUCfor F. distichus,PELfor P. limitata.•GENPELVJFUCMAZAUCCNCFEAPMAJLCCDE07115 DAY5105i— -10 I] CONTROLTREATMENTw-1515 DAYIO10wMAZ PEL FUCFig. 3.2 Single-diet experiments. 3.0±0.02 g of thallus was used per cage. Positivevalues indicate weight gain. Negative values indicate weight loss. Data are means +SE offive treatments and three controls. MAZ, M. cornucopiae, FUC, F distichus, PEL, P.la.720.200.15Cl)U)0-J0.10(!3w0.050.00Fig. 3.3 Results of the multiple-diet experiment. The comparisons of weight loss (g)between treatments and controls and among algal species. 1±0.02 g of each algal specieswere placed making -3.0 g (total) of food per cage. Data are means +SE of fourteentreatments and seven controls. MAZ, M. cornucopiae, FUC, F. distichus, PEL, P.limitata.IZI CONTROLTREATMENTMAZ PEL FIJC7330U) 20wI—U)zw-JzU) I0 _i_ I IMAZ PEL FUCFig. 3.4 Behavioral choice (attractiveness) of Littorina sp. towards the three algalspecies. Densities of snails attached to the thalli of each algal species 15 mm after themultiple-diet experiment started. Data are means +SE of sixteen replicates. See Fig. 3.2for caption comments.7430g 20I—U)zw0-Jz 10Cl)0Fig. 3.5 Tidal and light effects on snail movement towards food during the multiple-dietexperiment. The data shown are the number of snails attached to M. cornucopiae for everytidal and light condition. Tide/light combinations are presented in the same order assimulated in the lab. Data are means +SE of sixteen replicates.Night/LowNight/HighDay/LowDay/HighDAY1 DAY 4 DAY775CHAPTER 4THE EFFECT OF BARNACLES AND LIMPETS ON ALGALSUCCESSIONINTRODUCTIONWhen a disturbance opens up a free space and space-related resources in acommunity, some organisms quickly invade the space and use the liberated resources,while other organisms (species) replace the early colonists and come to predominate later.This process of species introduction and replacement in a community over time is termedsuccession. The mechanisms involved in succession which determine the actual pathwaybetween the early and the later colonists have long been of interest to ecologists. Earlyviews of succession focused on the competitive interactions between species in differentsuccessional stages and the influence of physical environments on colonists (Colinvaux1973, Horn 1974). Later, Connell and Slatyer (1977) proposed three general models ofsuccession by considering the net effect of early colonists on the establishment of the latersuccessional species: 1) the early colonists enhanced the establishment of the later colonists(facilitation); 2) the early colonists do not affect establishment of the later colonists(tolerance); 3) the early colonists slow the settlement or growth of the later colonists(inhibition). These models have provided valuable guides for researchers although manycomplexities have been revealed in natural systems; these include seasonality ofdemographic characteristics of component species (Turner 1983), indirect interactions(Dethier and Duggins 1984, Dungan 1986) and influences of consumers (Lubchenco andGaines 1981, Hawkins and Hortnoll 1983, Farrell 1991).As initially pointed Out by Connell and Slatyer (1977), the influence of consumersis of critical importance to the course of succession, and several recent studies of76succession have involved manipulation of consumers (reviewed by Lubchenco and Gaines1981, Hawkins and Hartnoll 1983). These studies indicated that consumers often have astrong influence on the rate of succession, but that succession could be either accelerated(Lubchenco and Menge 1978, Sousa 1979, 1984, Day and Osman 1981, Lubchenco1983), unaffected (Turner 1983, Jernakoff 1985) or slowed (Dayton 1975, Sousa et al.1981, Peer 1986, Farrell 1991). Farrell (1991) recently formulated a general predictivemodel (Fig. B. 1) of the effect of consumers on the rate of succession. In his model, therate of succession is determined by a combination of two factors: Connell and Slatyer’s(1977) classic models of facilitation, tolerance and inhibition, and the successional status ofthe species whose abundances are reduced by consumers. According to Farrell’s model,succession can be accelerated only if consumers reduce early successional species in theinhibition model (one of the nine cases), and succession will be slowed in six other cases,leaving two cases with no effect of the consumer on the rate of succession. Farrell (1991)also provided examples of the tolerance and facilitation models in a high intertidalcommunity on Oregon coasts dominated by Balanus-Pelvetiopsis, in which the majorconsumer, the Lottia spp. (acmaeid limpets), slowed the community succession. In thischapter, I test some cases in Farrell’s model.Barnacles and limpets together have been frequently investigated for their role inshaping the intertidal community, since they are both common and they coexist. Theinteraction dynamics between barnacles and limpets have sometimes been studiedseparately from other components of the system (Choat 1977, Denley and Underwood1979, Creese 1982, Underwood et al. 1983). However, more recently, the three-wayinteractions of barnacles-limpets-algae have received increasing attention (Jernakoff 1983,Dethier and Duggins 1984, Sousa 1984, Dungan 1986, Van Tamelen 1987, Farrell 1988,1991). Facilitation of algal recruitment by barnacles has typically been reported as resultingfrom either of two processes. First, substratum alteration caused by barnacles couldenhance algal propagule settlement because barnacles provided both a secondary77substratum and a shelter from desiccation stress (Norton 1983, Farrell 1991). This is anexample of a direct positive interaction of barnacles on algae. Secondly, barnacles, as theygrow to a large size, may inhibit the foraging activities of limpets, providing algae withrefugia from their herbivores (Hawkins 1981, Hawkins and Hartnoll 1983, Dungan 1986,Van Tamelen 1987, Little et al. 1988). The effect of barnacles on algae in this case is anindirect positive interaction through limpets.Investigations on multiple interactions have often provided much information onthe variety of mechanisms of species interactions (such as indirect interactions); suchstudies are particularly useful for elucidating the mechanisms of succession. In particular,some recent work has attempted to separate indirect effects among the component speciesfrom the complex barnacle-limpet-algae interactions (Dungan 1986, Van Tamelen 1987,Farrell 1991). Indirect interactions occur when the effect of one species on another ismediated by a third species. For example, Van Tamelen (1987) found that limpetsindirectly facilitated barnacles by grazing algae which had a deleterious effect (e.g.,overgrowth) on barnacles. In natural communities, this type of interaction has sometimesbeen reported both among organisms in the same trophic level (e.g., Dethier and Duggins1984, Kastendiek 1982) and among those at different trophic levels (e.g., Underwood etal. 1983, Dungan 1986, Van Tamelen 1987, Farrell 1991).Although researchers have given increased attention to the mechanisms of indirectinteractions, their influence in conjunction with the mechanisms of succession, especiallyalgal succession, is not well known (but see Lubchenco 1983). In the context of barnaclelimpet-algal interactions, both Dungan (1986) and Van Tamelen (1987) providedinsufficient information to evaluate the mechanisms of replacement of different algal speciesin different successional stages. This problem also applies in part to Farrell’s (1991)study, in that he focused on succession of different barnacle species.The aim of this chapter is to assess the mechanisms of algal succession and thedirect and indirect interactions producing those mechanisms in the barnacle-limpet-algal78community on the upper intertidal shore. A factorial design with barnacles and limpetsremoved singly and in combination was used to test the following hypotheses (1 and 2) andanswer questions (3 and 4): 1) Hypothesis I: limpets, as herbivores, slow the rate of algalsuccession; 2) Hypothesis II: facilitation of algal settlement by barnacles is a direct positiveinteraction which is not associated with the presence of the limpet; 3) Are there any indirectinteractions between the component organisms? if there are, what are the mechanism(s) ofthe interaction(s)?; 4) Does the pattern of algal succession in this community fit any of themodels proposed by Connell and Slatyer (1977)?METHODSExperimental designThe experiment was initiated at Nudibranch Point in July 1991. Sixteen 25x25 cmplots were cleared using a pneumatic hammer/drill (Chicago Pneumatic 9AK Handril) witha chisel bit and a SCUBA tank as an air source. The first stage in the air-pathway wasadjusted down to 80 psi for the drill. For clearing plots, all organisms (includingholdfasts, barnacles, crustose algae, etc.) on the substratum were completely removed bychiseling off the rock surface. Care was taken to maintain the level of the cleared surfacesat similar heights to the adjacent uncleared substratum to minimize significant modificationof microhabitats. The denuded piots were rechecked the next day to remove any organismsthat had been overlooked. Each corner of the plot was marked by hammering in concretenails which were sometimes supported by cement.The experiment consisted of a randomized block design with four blocks. Eachblock contained a replicate of the following four treatments: (1) barnacles and limpetspresent (+bar +lim), (2) barnacles removed, limpet present (-bar +lim), (3) barnaclepresent, limpets removed (+bar -lim), and (4) barnacles and limpets removed (-bar -lim).79These four treatments constituted a complete factorial design. The immigration of limpets(Lottia spp. ) from the surrounding areas was greatly reduced by applying 2.5-3 cm widecopper-paint (57.7% metallic copper, Pettit Paint Ltd., Borough of Rockaway, NewJersey) barriers, which limpets did not cross (Cubit 1975, personal observation). Sinceprevious studies employing this paint reported little or no effect from the copper on algalrecruitment or growth (Sousa 1979, Lubchenco and Cubit 1980, Slocum 1980, Robles andCubit 1981, Farrell 1988,1991), this method has been frequently used to exclude limpetsin intertidal studies. Any invading limpet was manually removed from the exclusion plotsat each sampling date (usually at intervals of 8 weeks). However, it was observed that themajor littorinid, Littorina sp., of this habitat (Chapter 3) was free to invade the experimentalplots. Copper paint was ineffective as a barrier against some gastropod snails such asTegulafunebralis, Littorina scutulata, and L. plena (Mastro et al. 1982). Newly recruitedbarnacles in the exclusion plots were also removed manually at each sampling date byscraping or squashing individuals with a small flat screw driver (4 mm in width). Cautionwas taken not to affect other existing organisms such as benthic diatoms and holdfasts ofmacroalgae during the removal of barnacles.The abundance of recolonizing algae was measured bimonthly within the central20x20 cm area of each 25x25 cm plot to minimize potential marginal effects. A quadrat(20x20 cm) with lxi cm subplots marked off within the quadrat frame (usingmonofilament lines) was used to measure percent cover. Percent cover of each species wasobtained by counting the number of the subplots in which thalli occupied >50% of its area.The accuracy and repeatability of this technique has been tested by Dethier et al. (1993) andthey reported that this method was generally more accurate than the random-point-quadratmethod. Algal cover was enumerated only for those thalli with their holdfasts within theplots. Densities of barnacles and limpets were subsampled from randomly selected 2x2 cmsubplots and then estimated for their density per 20x20 cm plot.80Data AnalysisI used an analysis of variance (ANOVA) to analyze for treatment effects on each offour selected sampling dates (October 1992, April 1993, December 1993, and August1994), followed by Tukey’ HSD tests if ANOVA results were significant. These samplingdates were selected to represent the treatment effects on each algal species in all seasons.As well, by performing only four tests, the probability of a type I error was not greatlyincreased. The Bonferroni adjustment on the P value (p=O.Ol25 at alpha =0.05) was usedfor each of the four tests. If significant heterogeneity of variances existed among theANOVA cells (tested by using the Fmax test and Cochran’s tests, Winer 1971), percentcover data were arcsin-transformed and density data (for barnacles and limpets) were log-transformed prior to analysis. On some sampling dates for certain algal species (as noted inthe RESULTS), ANOVA could not be performed because the transformation did notreduce the heteroscedasticity to a nonsignificant (alpha=0.05) level. For these cases, I usednon-parametric statistics, a Kruskal-Wallis test and Mann-Whitney U test (Wilkinson et al.1992) on untransformed data. A test for normality was not performed because of aninsufficient sample size for the test (n=4). For ease of interpretation, untransformed datawere plotted in all figures. All data analyses were performed using SYSTAT, version5.2.1 for Macintosh (Wilkinson et al. 1992).RESULTSThe effects of factorial removal of barnacles and limpets on algal recovery areshown in Fig. 4.1 (for the treatment effects on each algal species) and Fig. 4.2 (for thealgal species interactions under each treatment). The recolonization and abundance ofephemeral algae was significantly different between the limpet-excluded and limpet presentplots. The herbivore heavily grazed on ephemeral algae and the grazing effect was81significant on the two fall and winter sampling dates (ANOVA, p=O.000 for October 1992,p=O.OO3 for December 1993) but not in the summer (August 1994, p=O. 184) and spring(April 1993, p=O.O22) dates (Fig. 4.1; A). The effect of limpets on ephemeral algaesubsequently influenced algal succession. In the absence of limpets, the abundance ofephemeral algae dramatically increased within two months in the second fall (October 1992)in both limpet- and barnacle/limpet-excluded plots (Fig. 4.2; C and D), and this highpercent cover of ephemerals was maintained until April 1993 (Fig. B.2). During thisperiod there were low percent covers of fucoids, which started to colonize (summer, 1993)when the ephemerals declined apparently due to seasonal events. No evidence for such aninteraction between fucoids and ephemeral algae was found in the two limpet-presenttreatments (Fig. 4.2; A and B). In December 1993, the ephemeral algae (mainly diatoms)became abundant again. However, the dominance of ephemeral algae was ended by Fucusdistichus the following spring (April 1994 for the limpet-excluded plots and June 1994 forthe barnacle/limpet-excluded plots) (Fig. 4.2; C and D). In the absence of limpets, it tookalmost 3 years for Fucus distichus, the late successional species, to dominate the space.This pattern can be compared to the two limpet-present treatments (Fig. 4.2; A and B),where fucoid domination was apparent in a year.In the control plots (+bar +lim), both Fucus and Pelvetiopsis colonized at an earlystage (e.g., October 1992) and outcompeted other species (e.g., ephemerals, Mazzaella) forthe entire experimental peiiod (Fig. 4.2; A). In the barnacle-excluded plots (-bar +lim),only Pelvetiopsis limitata was common and all other algae remained at a very low percentcover for the entire experimental period (Fig. 4.2; B).There was no obvious barnacle effect on algal abundance in the absence of limpets(Fig. 4.2; C and D). However, in the presence of limpets, barnacles facilitated thecolonization of Fucus distichus; this alga had only a very low percent cover under similarconditions but without barnacles (Fig. 4.1; C; Mann-Whitney U tests with +B+L and-B+L, p=O.Oll for October 1992, p=O.O2O for April 1993, p=O.Ol’7 for December 1993,82pO.O2l for August 1994). In the presence of limpets, Pelvetiopsis limitata was moreabundant in the barnacle-excluded plots than in the piots with barnacles (Fig. 1; D;ANOVA, pO.O 125). The effect of barnacles onlimpets and the effect of limpets on barnacles are shown in Fig. 4.3 and Table 4.1.Barnacle densities were greater in the limpet excluded plots (-i-bar -Jim) than in the limpet-present plots (+bar +lim) at the later successional stages (Independent t-tests, t(df6)=-3.0 15, p=O.O24 for August 1993, t(df=6)=-2.988, p=O.024. for October 1993). However,limpets were not significantly affected by the presence or absence of barnacles even thoughtheir number was slightly higher in the presence of barnacles (Table 4.1 and Fig. 4.3).The abundance of Mazzaella cornucopiae remained at less than 2% cover for theexperimental period, thus there was no treatment effect for this red alga (Fig. 4.1; B).Among the ephemeral algae, diatoms were initially the most abundant algae in the limpet-excluded plots, but were not seen when limpets were present (Table 4.2). A pattern similarto that for diatoms was observed for Urospora spp., indicating that limpets effectivelygrazed on microscopic and delicate filamentous algae.DISCUSSIONModels and the herbivore’s role in algal successionIn this community, limpets (mostly Lottia digitalis) selectively limited theabundance of ephemeral algae, and can be considered as a keystone species whichdetermines the sequence of algal succession. Dominant algae in the different treatments anddifferent successional stages are summarized in Fig 4.4. In the absence of limpets,succession began with abundant settlement of ephemeral algae, and ended with Fucusdistichus. However, in the presence of limpets, both Fucus and Pelvetiopsis appeared atthe early stages and the dominance of fucoids continued to the later stages. Limpets83grazing on ephemeral algae in this study speeded up the early successional sequence byreleasing fucoids from inhibition by ephemeral species. Therefore, both Fucus andPelvetiopsis predominated in the community from the early stages, and consequently thesuccession by-passed the early colonist (ephemeral algae) stage. Apparently, there was nospecies replacement in this process except for the slight dominance of Pelvetiopsis as itreplaced Fucus later in time (Fig. 4.2; A). Hypothesis I was rejected and succession of thiscommunity was accelerated by the herbivores. However, in Farrellts(1991) BalanusPelvetiopsis community (Facilitation Model) in Oregon, the limpets slowed the rate ofsuccession by negatively affecting a small barnacle (Chthamalus dalli) which Tacilitated’the larger and the later successional barnacle (Balanus glandula).In the high intertidal community at Nudibranch Point, early colonists (ephemeralalgae) inhibited the settlement of later colonists (fucoids), typical of the Inhibition Modelproposed by Connell and Slatyer (1977). This inhibition caused a considerable delay forspecies replacement between ephemeral algae (e.g., diatoms, Porphyra spp.) and fucoids(especially Fucus), but the delay disappeared in the presence of the herbivores (limpets).Ephemeral algae often cause inhibition of algal succession in rocky intertidal communities(Sousa 1979, 1984, Robles and Cubit 1981, Lubchenco 1983, Breitburg 1984). Sousa(1984) reported a similar result among a similar array of algal species in which the rapidincrease of Ulva, diatoms and Urospora in the early successional stage (e.g., for 12months after disturbance) inhibited the settlement of some later colonists such as Fucus,Mastocarpus and Pelvetiopsis. This occurred on a high shore of northern California whenlimpets were excluded. Lubchenco (1983) also reported that in the mid-intertidal of a NewEngland rocky shore, in the absence of Littorina littorea (a herbivorous snail), ephemeralalgae such as Ulva, Enteromorpha and Porphyra inhibited the appearance of the latersuccessional species, e.g., Fucus. The Inhibition model represents the dominant type ofsuccession in many marine habitats (Connell and Slatyer 1977, Sousa 1979, Breitburgé841984); experimental evidence for the Tolerance Model has been rarely reported (but seeFarrell 1991).However, facilitation was originally thought to occur as a result of earlysuccessional species altering the physical environment in ways favorable to latersuccessional species (Connell and Slatyer 1977). For this reason Connell and Slatyersuggested that facilitation might be more frequent in harsh physical environments. In highintertidal habitats, this paradigm was supported by Farrell (1991) in a Balanus-Pelvetiopsiscommunity. He found that the early successional barnacle, Chthamalus dalli, facilitated thelater successional barnacle, Balanus glandula. There was no evidence for facilitation byephemeral algae for fucoids during succession in my study. However, it is worth notingthat inhibition by ephemeral algae was seasonal and the intensity of inhibition seemed muchreduced in summer, because of both the life history characteristics of ephemeral algae andstrong desiccation (some ephemeral species (e.g., Porphyra spp.) persisted in the lowerpart of my study area). Nevertheless, this study adds a second example for the inhibitionmodel of succession occurring in the high intertidal zone, together with Sousa’s work.The results of my study show a different process occurring in a habitat similar tothat studied by Farrell. This difference probably occurred because Chthamalus was rare inmy study site and ephemeral algae were rare in Farrell’s site, even though tidal heights inboth studies are similar. In the high intertidal community at Nudibranch Point, algalsuccession follows an inhibition model, which may be rare in the physically stressful highintertidal (Connell and Slatyer 1977). The different results in the rate and the sequence ofsuccession in the presence or absence of limpets indicates that the consumption of algae bylimpets has a significant effect in this habitat. Thus, this evidence is another example ofsignificant biological interactions occurring in the high intertidal habitat, others of whichhave been shown elsewhere in this thesis.85Direct and indirect interactions during successionThe results of removing barnacles and limpets brought to light complex interactionsamong the component organisms related to the successional process. The major direct andindirect interactions affecting algal succession are shown in Fig. 4.5. Limpet’s grazing onephemeral algae constituted a direct negative interaction. In addition, barnacles enhancedFucus settlement; this is a direct positive interaction (facilitation). However, the barnacleeffect in general varied with the presence or absence of limpets. In the absence of limpets,there was no significant barnacle effect on algal abundance. When limpets were present,however, barnacles significantly facilitated the settlement and growth of F. distichus. Incontrast, the abundance of F. distichus was low in the barnacle-excluded plots and P.limitata was much more abundant. My results rejected the second hypothesis (that barnaclefacilitation of algal settlement is a direct positive interaction which is not associated withthe presence of limpets). If limpet grazing was more active in the barnacle-excluded plots,the high abundance of Pelvetiopsis implied that this alga was probably the less preferredprey of the other species, especially compared to Fucus. This speculation is based onindirect evidence (Fig. 4.5). The reason for the different responses of the two fucoids tobarnacles, or indirectly to limpets, was not explored in my study.The positive effect of limpets on fucoids is an indirect facilitation mediated byephemeral algae (Fig. 4.5). This indirect interaction may occur because the limpets preferto eat ephemeral algae rather than fucoids, but I did not test this preference directly.However, some evidence that the small acmaeid limpet (Lottia digitalis) selectively grazedon delicate filamentous, membranous algae and benthic diatoms (over larger perennialmacroalgae or even larger ephemerals such as Porphyra spp.) has been documented(Castenholz 1961, Nicotri 1977, Cubit 1984, Farrell 1988). In my study, the L digitaliswas also more effective on diatoms and Urospora spp. than other ephemerals (Table 4.2).86A similar mechanism of indirect interaction has been reported by Lubchenco (1983), but fora different herbivore, Littorina littorea.However, patterns of direct and indirect interactions among barnacles-herbivores-algae reported in other studies do not show a consistent pattern. The results of someselected studies (e.g., Dethier and Duggins 1984, Dungan 1986, Van Tamelen 1987) aresummarized in Fig. B.3. Dungan (1986) found that with similar organisms as in mystudy, barnacles indirectly facilitated algae by preempting space required by limpets whichgrazed on the algae. Van Tamelen’s (1987) results were different from those of Dungan(1986) in that algae (in his term, both micro- and macro-algae) had a deleterious effect onbarnacles by reducing their growth rate and increasing mortality; however, limpetsprovided an indirect benefit to barnacles by reducing algae. Mechanisms of indirectinteractions can be much more complicated by including different consumers (Vandermeer1980, Dethier and Duggins 1984) and/or different prey (Lubchenco 1983, Dethier andDuggins 1984, this study). Dethier and Duggins (1984) demonstrated an example ofcomplex interactions with two consumers (chiton and limpet) and two prey (diatoms andmacroalgae). They found that a chiton (Katharina tunicata) indirectly enhanced limpetabundance by reducing macroalgae which competitively inhibited benthic diatoms. Theconsequent increase of diatoms (caused indirectly by the chiton) provided both food andhabitat for the specialist consumer limpets.For the interaction between barnacles and limpets, this study suggested that limpetsapparently had a deleterious effect on barnacles, but barnacles had no effect on limpets.Lower densities of barnacles shown in the +bar +lim plots and in the +bar -lim plots(October 1992 - April 1993 in Fig. 4.3) could be the result of limpets bulldozing juvenilebarnacles (Dayton 1971, Underwood et al. 1983) and due to the seasonal increase ofephemeral algae which might overgrow and reduce barnacles (Denley and Underwood1979, Underwood et al. 1983, Farrell 1988, 1991, personal observation), respectively.87Differences in the role of each component organism in barnacle-limpet-algalassemblages found in previous studies and my study are primarily due to the heterogeneityof habitats and communities. For example, predominant algal species were different ineach study cited: Ralfsia crusts in Dungan’s, Ulva and Enteromorpha in Van Tamelen’s,Hedophylluin and diatoms in Dethier and Duggin&. Tidal heights were also different,suggesting that physical conditions are also different. Foster (1990) has reminded us not togeneralize results from one region to other regions that are less well described and whereexperiments have not been repeated. Therefore, conclusions about direct and indirectinteractions among even similar component species may be limited in their applicability tothat local habitat; this suggests the necessity of experimental replication over extendedgeographical areas.Nevertheless, the evidence for indirect interactions in this system providesecologically relevant information, in that the herbivores differently affected algae indifferent successional stages and thus facilitated the succession rate by reducing thepresence of the early successional group. This mechanism resulted in a “by-passing” of theearly colonist stage. The role of barnacles and limpets in this Mazzaeila-Fucus-Pelvetiopsiscommunity was viewed in the context of algal succession. It was unfortunate that theabundance of Mazzaella was too low to evaluate its interaction with the two invertebrates.The reason for the low abundance of Mazzaella in this experiment will be explained inChapter 5. Interaction dynamics between barnacles and limpets and algae shown here willbe applied to predict the patterns of community dynamics in Chapter 6.88REFERENCESBreitburg, D. L. (1984). Residual effects of grazing: inhibition of competitor recruitmentby encrusting coralline algae. Ecology 65: 1136-1143.Castenholz, R. W. (1961). The effect of grazing on marine littoral diatom populations.Ecology 42: 783-794.Choat, I. H. (1977). The influence of sessile organisms on the population biology of threespecies of acmaeid limpets. J. Exp. Mar. Biol. Ecol. 26: 1-26.Colinvaux, P. A. (1973). Introduction to ecology. Wiley, New York. 621 pp.Connell, J. H., Slatyer, R. 0. (1977). Mechanisms of succession in natural communitiesand their role in community stability and organization. Am. Nat. 111: 1119-1144.Creese, R. G. (1982). Distribution and abundence of acmaeid limpet Patelloida latistrigata,and its interaction with barnacles. Oecologia 52: 85-96.Cubit, 1. (1975). Interactions of seasonally changing physical factors and grazing affectinghigh intertidal communities on a rocky shore. Ph.D. Thesis. University of Oregon.Eugene, OregonCubit, J. D. (1984). Herbivory and the seasonal abundance of algae on a high rockyintertidal shore. Ecology 65: 1904-1917.Day, R. W., Osman, R, W. (1981). Predation by Petiria miniata (Asteroidea) onbryozoans: prey diversity may depend on the mechanism of succession. Oecologia51: 300-309.Dayton, P. K. (1971). Competition, disturbance and community organization: theprovision and subsequent utilization of space in a rocky intertidal community. Ecol.Monogr. 41: 351-389.Dayton, P. K. (1975). Experimental evaluation of ecological dominance in a rockyintertidal algal community. Ecol. Monogr. 45: 137-159.Denley, E. J., Underwood, A. J. (1979). Experiments on factors influencing settlement,survival and growth of two species of barnacles in New South Wales. J. Exp. Mar.Biol. Ecol. 36: 269-293.Dethier, M. N., Duggins, D. 0. (1984). An “indirect commensalism” between marineherbivores and the importance of competitive hierarchies. Am. Nat. 124: 205-219.Dethier, M. N., Graham, E. S., Cohen, S., Tear, L. M. (1993). Visual versus random-point percent cover estimation: ‘objective’ is not always better. Mar. Ecol. Prog.Ser. 96: 93-100.Dungan, M. L. (1986). Three-way interactions: barnacles, limpets and algae in a SonoranDesert rocky intertidal zone. Am. Nat. 127: 292-3 16.Farrell, T. M. (1988). Community stability: effects of limpet removal and reintroduction ina rocky intertidal community. Oecologia 75: 190-197.89Farrell, T. M. (1991). Models and mechanisms of succession: an example from a rockyintertidal community. Ecol. Monogr. 61: 95-113.Foster, M. S. (1990). Organization of macroalgal assemblages in the Northeast Pacific: theassumptions of homogeneity and the illusion of generality. Hydrobiologia 192: 21-33.Hawkins, S. J. (1981). The influence of season and barnacles on the algal colonization ofPatella vulgata exclusion areas. J. Mar. Biol. Ass. U.K. 61: 1-15.Hawkins, S. J., Hartnoll, R. G. (1983). Grazing of intertidal algae by marineinvertebrates. Oceanogr. Mar. Biol. Annu. Rev. 21: 195-282.Horn, H. S. (1974). The ecology of secondary succession. Ann. Rev. Ecol. Syst. 5: 25-37.Jernakoff, P. (1983). Factors affecting the recruitment of algae in a midshore regiondominated by barnacles. J. Exp. Mar. Biol. Ecol. 67: 17-3 1.Jernakoff, P. (1985). The effect of overgrowth by algae on the survival of the intertidalbarnacle Tesseropora rosea Krauss. J. Exp. Mar. Biol. Ecol. 94: 89-97.Kastendiek, J. (1982). Competitor-mediated coexistence: interactions among three speciesof benthic macroalgae. J. Exp. Mar. Biol. Ecol. 62: 201-210.Little, C., Williams, G. A., Morritt, D., Perrins, J. M., Stirling, P. (1988). Foragingbehavior of Patella vulgata L. in an fish sea-lough. J. Exp. Mar. Biol. Ecol. 120:1-21.Lubchenco, J. (1983). Littorina and Fucus: effects of herbivores, substratum heterogeneityand plant escapes during succession. Ecology 64: 1116-1123.Lubchenco, J., Menge, B. A. (1978). Community development and persistence in a lowrocky intertidal zone. Ecol. Monogr. 48: 67-94.Lubchenco, J., Cubit, J. (1980). Heteromorphic life histories of certain marine algae asadaptations to variations in herbivory. Ecology 61: 676-687.Lubchenco, I., Gaines, S. D. (1981). A unified approach to marine plant-herbivoreinteractions. I. Populations and communities. Ann. Rev. Ecol. Syst. 12: 405-437.Mastro, E., Chow, V., Hedgecock, D. (1982). Littorina scutulata and Littorina plena:sibling species status of two prosobranch gastropod species confirmed byelectrophoresis. Veliger 24: 239-246.Nicotri, M. E. (1977). Grazing effects of four marine intertidal herbivores on themicroflora. Ecology 58: 1020-1032.Norton, T. A. (1983). The resistence to dislodgement of Sargassum inuticuin germlingsunder defined hydrodynamic conditions. J. Mar. Biol. Assoc. U.K. 63: 181-194.Peer, R. L. (1986). The effects of microcrustaceans on succession and diversity of an algalmicrocosm community. Oecologia 68: 308-314.90Robles, C. D., Cubit, J. (1981). Influence of biotic factors in an upper intertidalcommunity: dipteran larvae grazing on algae. Ecology 62: 1536-1547.Slocum, C. J. (1980). Differential susceptibiitty to grazers in two phases of an intertidalalga: advantages of heteromorphic generations. J. Exp. Mar. Biol. Ecol. 46: 99-110.Sousa, W. P. (1979). Experimental investigations of disturbance and ecological successionin a rocky intertidal algal community. Ecol. Monogr. 49: 227-254.Sousa, W. P. (1984). Intertidal mosaics: patch size, propagule availability, and spatiallyvariable patterns of succession. Ecology 65: 1918-1935.Sousa, W. P., Schroeter, S. C., Gaines, S. D. (1981). Latitudinal variation in intertidalalgal community structure: the influence of grazing vegetative propagation.Oecologia 48: 297-307.Turner, T. (1983). Complexity of early and middle successional stages in a rocky intertidalsurfgrass community. Oecologia 60: 56-65.Underwood, A. J., Denley, E. J., Moran, M. 1. (1983). Experimental analyses of thestructure and dynamics of mid-shore rocky intertidal communities in New SouthWales. Oecologia 56: 202-2 19.Van Tamelen, P. G. (1987). Early successional mechanisms in the rocky intertidal: the roleof direct and indirect interactions. J. Exp. Mar. Biol. Ecol. 112: 39-48.Vandermeer, J. (1980). Indirect mutualisms: variations on a theme by Stephen Levine.Am. Nat. 116: 441-448.Wilkinson, L., Hill, M. A., yang, E. (1992). SYSTAT: Statistics, version 5.2.1 edition.SYSTAT. Evanston, IL, USA.Winer, B. J. (1971). Statistical principles in experimental design. McGraw-Hill. NewYork.Table 4.1 The mean density ±SE (in 20x20 cm plot) of barnacles and limpets in eachnon-excluded treatment. Data are the mean of 14 sampling dates (April 1992- August1994; December 1993 data are missing), in each sampling date the density of barnacles andlimpets was averaged from the 4 replicate plots.BARNACLES LIMPETS+B+L ÷B-L +B+LMean 558.2 993.6 26.8 21.2SE 72.7 198.9 3.2 2.691Table4.2Themeanpercentcoverof thefivemostabundantephemeralalgaeineachtreatment.Dataarethemeanof13samplingdates(February1992-February1994),ineachsamplingdatethepercentcovervalueofeachspecieswasaveragedfromthe4replicateplots.+BAR+LIM-BAR+LIM+BAR-LIM-BAR-LIMSPECIES%±SESPECIES%±SESPECIES%±SESPECIES%±SEPorphyra6.1±3.46Porphyra1.4±0.75Diatoms17.8±5.99Diatoms25.0±7.49spp.spp.Scytosiphon1.0±0.03Scytosiphon0.3±0.04Porphyra7.1±4.82Porphyra7.2±4.93doyidotyispp.spp.Enteromorpha0.5±0.21Crustose0.2±0.06Urospora3.7±2.09Urospora3.1±1.65spp.algaespp.spp.Endockidia0.4±0.07Endocladia0.2±0.02Enteromorpha3.5±1.49Scytosiphon2.3±0.89muricatamuricataspp.dotyiCrustose0.1±0.00Mastocarpus0.1±0.03Mastocarpus0.7±0.35Callithainnion0.5±0.22algaepapillatuspapillatusspp.93(I)I0-J0E000c’Jza:w>0C)zwC-)a:w0A. Ephemeral algae—D---— +B+Lc—-- -B+L----0----. +B-L----ix-----B-LT10080.60.40•20•0.5..4.II I I I IB. Mazzaella3.2.0$ b bFig. 4.1 Effects of barnacle and limpet removal on each algal group. Data are means ±SE of four replicates. +B+L indicates both barnacle and limpet present, -B+L barnacleabsent, limpet present, +B-L barnacle present, limpet absent, and -B-L both barnacle andlimpet absent.•1:1F)-0000III-HF—”JI\\III-u:IIII[hIIIIPERCENTCOVERIN20x20cmPLOTSI\\)0)0000000p CD Cl) Cl)p 1 C.) 0)95(I)I0-J0EC)00c’Jzw>00I—zw0wA.+BAR+LIM—a---- EPHMAZ----o---- FUC----h---.- PELTT0T/LB.- BAR + LIMI I I I I I I I I I I I I I I I I I I60-40-20-08060•4020.0.% 00Fzw0w0I I I I I I I I I I I I I I I I I I II IT TI“1Fig. 4.2 continued.97LIMPETSFig. 4.3 The abundance of barnacles and limpets in the experimental plots (20 x 20 cm).Data are the mean densities ± SE per plot (n=4).BARNACLES—D— +B+L----o----• +B-LT3000-2500-2000-1500-1000-500-0-Ic’JEC-)00zCl)wI—(I)zwUIi i i i i i TçOi’98(Balanus glandula)Fig. 4.4 A summary of barnacle and limpet effects on algal succession. Dominant algaewere shown in each experimental condition with their relative abundance.Yearl &2EARLYYear 3LATE.b. iiLU0—IEphemeral Ephemeralalgae algaeDiatoms DiatomsPorphyra PorphyraFucus (more) Pelvetiopsis(lots)Pelvetiopsis(less) Fucus (few)+Fucus Fucusdistichus distichusFucus (more) Pelvetiopsis(lots)Pelvetiopsis(less) Fucus (few)+BARNACLES+BARNACLES99LEG ENDSolid line : strong interactionDashed line : weak interactionArrow head : negative interactionRound head: positive interactionClear point : indirect interactionDark point : direct interactionFig. 4.5 The summary of direct and indirect interactions shown between barnacles,limpets, fucoids and ephemeral algae in this study.A100CHAPTER 5EFFECTS OF SIZE OF EXPERIMENTAL CLEARINGS AND SEASON OFCLEARING ON ALGAL PATCH RECOVERYINTRODUCTIONThe species composition and abundance of organisms in many rocky intertidal andsubtidal communities is highly influenced by disturbance (Sousa 1984b, Connell andKeough 1985, Sousa 1985). Disturbance is defined here as any discrete event thatdecreases the amount of living biomass in an area and opens up space for the establishmentof new individuals or colonies. Investigators have extensively studied various aspects ofdisturbance on succession and community structure in marine habitats including frequency(Connell 1978, Sousa 1979a,b, Miller 1982), size (Osman 1977, Paine and Levin 1981,Keough 1984, Farrell 1989, Benedetti-Cecchi and Cinelli 1994), intensity (Sousa 1980,see Connell and Keough 1985 for references), location (Palumbi and Jackson 1982, Sousa1984a, Dayton et al. 1992), and time or seasonality (Foster 1975, Hawkins 1981, Turner1983a, Jara and Moreno 1984, Breitburg 1985, Kennelly 1987, Dayton et al. 1992,Benedetti-Cecchi and Cinelli 1994).The formation of gaps is of considerable significance to sessile organisms whichrequire open space. Organisms secure space by overgrowing or by spreading vegetativelyinto open space, or by growing from dispersed propagules. Various attributes of a newlycreated gap (i.e., its size, shape, location and time of creation) can affect subsequent patchcolonization and ensuing biological interactions (Sousa 1985). Species with particular lifehistories or reproductive strategies may colonize some areas but not others. For example,the centers of very large gaps are most likely to be colonized by species producingpropagules which travel relatively great distances. Such dispersal capability is lessimportant in smaller gaps, since most recolonizing propagules will be produced by101individuals established adjacent to the gap (Davis and Cantlon 1969, Osman 1977, Sousa1979b, Begon et al. 1990). This generalization has been examined experimentally inmarine habitats (Keough 1984, Sousa 1984a, Farrell 1989).The rate of colonization may vary with patch size because biological environmentsof patches may also vary with size. Sousa (1985) describes that the most obviousinfluence of patch size derives not from the size of a patch per se but from the manner inwhich the ratio of patch perimeter to area changes with patch size. For example, smallerpatches have a greater ratio of edge to area than larger patches. Therefore, the number ofpropagules received per unit area in smaller patches is greater than that of larger patches.His argument clearly supports the idea that smaller patches are colonized more rapidly thanlarger ones, and that this is particularly true when the distance of dispersal is small.However, smaller patches may be influenced by factors which negatively influencegermination of propagules or post-recruitment survivorship of newly-settled individualsand consequently slow the colonization process. These factors may include shading (Reedand Foster 1984, Kennelly 1989), scouring (Velimirov and Griffiths 1979, Kennelly 1989)and increased herbivory (Sousa 1 984a). In intertidal mussel beds, small clearings harboredhigher densities of grazers, particularly limpets, than do large patches because smallpatches provided a greater ratio of edge area for limpets which tended to aggregate at edges.(Paine and Levin 1981, Sousa 1984a). A similar result has been reported from a highintertidal zone (Farrell 1989). Consequently, small patches may have a slow colonizationdue to increasing herbivory (Sousa 1985). Barnacles (e.g., Balanus) were influenced bydifferent sizes of disturbance in some studies. Farrell (1989) found that barnacles weremore abundant in large gaps probably due to less deleterious effects imposed by algae.However, it is difficult to compare the effect of patch size on the rate of recovery becausedifferent studies used different sizes of experimental clearing. In addition, two recentstudies dealing with this problem and using similar sizes of clearing produced conflictingresults. Farrell (1989) found that small gaps (4x4 cm) were colonized most rapidly,102followed by medium (8x8 cm) and larger gaps (16x16 cm) in the upper intertidal zones ofthe Oregon coast, U.S.A. Benedetti-Cecchi and Cinelli (1994) reported that the algalcolonization rate was highest in larger gaps (20x20 cm), followed by medium (lOxlO cm)and small (5x5 cm) gaps in a low intertidal habitat of Italy.Deterministic views of community succession using one dimensional models ofdisturbance (i.e., size) make it more complicated and difficult to predict the patterns ofcommunity dynamics than when two or three dimensional models of disturbance are used(i.e., frequency, seasonality, etc.) (Miller 1982, Malanson 1984). It is highly unlikely thatnatural disturbance occurs uniformly (e.g., same size or same intensity). Thus its naturaloccurrence may involve combinations of factors which could often be correlated (Sousa1980, Paine and Levin 1981, Miller 1982, Malanson 1984). For example, Paine and Levin(1981) reported that the largest clearings in mussel beds were created by winter stormwaves and such clearings were less frequent than small clearings produced by waves oflesser magnitude in any season. In this case, the interaction of size and seasoncharacterizes this disturbance. It is clearly important to determine the key characteristics ofdisturbances which are critical in understanding the dynamics of the communityinvestigated (for instance, see Sousa 1980, Breitburg 1985, Benedetti-Cecchi and Cinelli1994). Both individual factors of disturbance and their interaction are important forunderstanding patch recovery and succession (Miller 1982, Malanson 1984).The time or season at which a gap is created by disturbance is known to determineearly successional algal assemblages because of seasonal availability of propagules ofcertain species (Foster 1975, Paine 1977, Emerson and Zedler 1978, Hawkins 1981,Breitburg 1985, Kennelly 1987). Such initial variability may influence subsequentcolonization, so that the gaps created in different seasons become dominated by differentorganisms in later successional stages (Turner 1983b, Jara and Moreno 1984). In intertidalhabitats, Benedetti-Cecchi and Cinelli (1994) reported examples of significant seasonaleffects on recovery of patches, although these patterns varied with algal species and site.103However, other studies have negated the above theory, and indicated that the effect ofseason of disturbance on producing an initial colonization pattern became less evident assuccession proceeded and the patches were eventually dominated by the same perennialspecies (Sousa 1 979a, Hawkins 1981). More information from habitats at different tidalheights and with different algal assemblages are required for generalization.The objective of this chapter is to demonstrate the effects of size and season ofexperimentally cleared gaps on algal recolonization and within-patch dynamics in a highintertidal, Mazzae!la-Fucus-Pelvetiopsis dominated community. The study was designed toaddress the following questions. 1) Is the rate of algal recovery faster in a smaller patch(gap)? The answer for this question provides a comparison for the effect of gap size onrecovery rate with two recent studies (Farrell 1989, Benedetti-Cecchi and Cinelli 1994) byusing similar sizes of clearings. 2) Do different clearing seasons affect the dominance of aparticular species in this community? This question is asked to test the two contrastingviews on the effect of timing of disturbance on patch structure described earlier. 3) Whatspecies come in when a gap of certain size is created in a certain time of the year?Predictions about community structure following various combinations of the two aspectsof disturbance may be possible to some degree when the responses of each componentspecies are known using the interaction term of size and season of disturbance. 4) Arelimpets more abundant in small patches than large patches? Are barnacles more abundant inlarge patches than small ones? The answers to these questions test some of the hypothesesdescribed earlier.104METHODSExperimental designThe study was conducted at Prasiola Point. The experimental units consisted ofsquare piots of three different sizes (5x5, lOxlO and 20x20 cm). To test for seasonaleffects, small (5x5 cm) and medium (lOxlO cm) piots were cleared four times a yearsummer (August 1991), fall (October 1991), winter (February 1992) and spring (April1992); large plots (20x20 cm) were cleared only in July 1991. At the beginning of theexperiment, a permanent transect line was placed along the shore within the zone 3.4-4.2 mabove Lowest Normal Tide (LNT: Canadian Chart Datum). The position of the line wasmarked by hammering concrete nails or drilling bolts at every meter. The transect wasplaced only on mixed stands of the three species of interest, so that the line was sometimesdisconnected due to heterogeneity in algal assemblages on the rock substratum. Using 10cm intervals along the transect line, I numbered all potential plots for clearing small andmedium plots on both sides of the transect line. Four large plots (20x20 cm) were clearedaway from the transect line but within the same tidal zone. At each clearing season, fifteenplots of each small and medium size were chosen using a random number table. Whenselecting plots for clearing, I intentionally skipped some random numbers to avoid clearinga plot adjacent to a previously cleared one; thus, at least one uncleared plot existed betweencleared ones. I assumed that this method enabled me to treat data as though they wereunaffected by those from adjacent clearings. Four unmanipulated permanent 20x20 cmplots were also marked in order to monitor natural seasonal fluctuations of algal abundance.Plots were cleared by hand chiseling (for the small and medium plots) or by using acompressed-air powered drill with a chisel bit (for the large plots). This allowed me toremove all organisms (including holdfasts, barnacles, crustose algae, etc.) in the plots.105The denuded plots were rechecked the next day to remove any organisms that remained. Inthis way, completely new substrata were attained in every clearing.Recolonization by macroalgae was monitored bimonthly for two years. Quadratsof the same size as the experimental plots, with lxi cm subplots marked off within thequadrat frame (25, 100 and 400 subplots for small, medium and large quadrats,respectively), were used for measuring the abundance of organisms. Percent cover of eachspecies was estimated by counting the number of subplots in which a species occupied>50% of its area. This technique was consistently used for estimating algal percent coverin my study. Algal cover consisted of only those thalli with their holdfasts in the plot.Crustose algae could not be identified in the field; therefore, I treated them as a singleentity.Densities of barnacles and limpets were monitored at every sampling date.Barnacles became too numerous to count in the medium and large plots so subunits werecensused. Five and twenty randomly chosen 2x2 cm areas were censused in each mediumand large plot, respectively. Data from 4, 10 and 16 months after initiation, of summer-cleared plots, are presented to compare the distribution of the invertebrates in threedifferent patch sizes.Data analysisPercent cover of algal species from the same plot was measured repeatedly onsuccessive sampling dates and these values were thus correlated over time (dependentvariables). Therefore, data were analyzed using a repeated measures analysis of variance(RM-ANOVA). A three-way (Size x Season x Time) ANOVA with repeated measures onthe Time factor was separately applied for each of the three dominant algae and a singleadditional group consisting of ephemeral algae. Data from large plots (20x20 cm) were notincluded in the ANOVA because they were cleared in only one season. Therefore, the106effects of this latter treatment were deduced by inspection of graphical data. The repeatedmeasures of percent cover for each species did not exhibit homogeneity of variance for allpairs of measurements within subjects (“compound symmetry”; Gurevitch and Chester1986, Myers and Well 1991). This precludes use of a standard univariate RM-ANOVA toanalyze the within-subject hypotheses due to inflation of type I error rates (Myers and Well1991). In these cases, I presented both the probability values of Huynh-Feldt adjusteddegrees of freedom as well as the results of multivariate analysis of variance (MANOVA)where the assumption of sphericity was not required (Mead 1988, Myers and Well 1991).Cochran’s C test and Fmax test (Winer 1971) were used to check homogeneity ofvariance. In most cases, except for total algal cover data, this assumption was violated andtherefore appropriate transformations were used (Underwood 1981). Percent cover of eachalgal species was arcsine-transformed prior to analysis. Barnacle and limpet densities wererespectively log- and (n+l) square root-transformed. Transformation did not reduce theheterogeneity to nonsignificant levels in a few cases; for example, some data from the initialsample dates. Although these data were dropped from the repeated measures ANOVA’s,this procedure did not affect statistical results. Plots of residuals against estimated valueswere visually examined after each ANOVA to check if error terms were normallydistributed. The only exceptions were the barnacle and limpet data from large plots, due tosmall (n=4) sample size. All data were analyzed using SYSTAT, version 5.2.1 forMacintosh (Wilkinson et al. 1992).RESULTSUnman ipulated plotsMazzaella comucopiae and Fucus distichus were the most conspicuous species inunmanipulated plots during the study (mean cover, 30.2% and 25.2%, respectively; Fig.1075.1). Pelvetiopsis limitata (11.8%) was relatively abundant in the first year, but was lower(e.g., April and June 1993) in the second year. Ephemeral algae covered only 4.4% of theplots during this period. The abundance of most algae in unmanipulated plots showed asimilar seasonal pattern; it was highest in February to June and was lowest in August toDecember. Seasonal changes in algal abundance were greater in both fucoids andephemeral species than in M. cornucopiae (Fig. 5.1). Peaks in recruitment of both fucoidswere observed in October of 1991, 1992 and 1993 except for P. limitata in October 1992.The timing of maximal recruitment was in contrast to the peaks in percent covers of bothspecies, the latter occurring in April.Size effects of disturbanceTotal algal cover following summer clearing of each of the three plot sizes is shownin Fig. 5.2. The lOxlO cm plots had a significantly greater percent cover of total algae thanthe 5x5 cm plots. This pattern occurred also in other plots cleared in different seasons,except for those cleared in the fall (Table 5.1). The pattern was also consistent (nosignificant interaction between Time and Size) throughout the experimental period exceptfor winter-cleared plots (Table 5.1). Colonization in the 20x20 cm plots was the slowestamong the three sizes cleared in summer. Total algal cover in large plots remained less than5% until 14 months after clearing whereas 8 months after clearing the total algal coverreached 26.4% in small plots and 35.5% in medium plots (Fig. 5.2).Percent cover of both Fucus distichus and ephemeral algae was greatest in mediumplots (Size effects, p=O.OO1 and p=O.OO3, respectively; Table 5.2, Fig. 5.3). However,for Mazzaella cornucopiae and Pelvetiopsis limitata, differences in percent cover betweensmall and medium plots were not great (p=O.592 and pO.2O4, respectively). Although nostatistic was applied, it was obvious that percent covers of Mazzaella in small and mediumplots were much greater than that in large plots (Fig. 5.3). This alga never successfully108settled in large plots. Colonization by F. distichus occurred more rapidly in medium plotsthan in small and large plots (which it colonized at similar rates) although this pattern wasnot recognizable during the first 6 months (Fig. 5.3). However, ephemeral algae colonizedrapidly from early in the succession, especially in the medium plots. Ephemeral species inmedium and small plots consisted of a similar assemblage. In medium plots, crustosealgae, Cladophora colunibiana, Scytosiphon dotyi and Endocladia muricata were mostabundant (in decreasing abundance). Small plots were settled by crustose algae, S. dotyi,C. columbiana and Polysiphonia sp. In contrast, the ephemeral group in large plots wasdominated by Porphyra sp., followed by E. muricata and S. dotyi. I occasionally found afew small clumps of M. cornucopia, especially in spring, but these usually disappeared bythe next sampling dates. Pelvetiopsis limitata was the species least affected by the size ofthe disturbance; it showed similar cover in all three plot sizes over time.Seasonal effects of disturbanceIn medium and small plots, there was no difference in algal abundance among plotscleared in different seasons, except for P. limitata (pO.O2, Table 5.2; analysis includeddata through 16 months). The mean percent cover of P. lim.itata during the experimentfrom summer clearing averaged over the two sizes was 2.54%, which was significantlygreater than those from the winter (0.67%) and the fall clearings (0.45%) (Tukey’s HSD,p=O.049 and p=O.O22,respectively). Fucus had a high percent cover in summer clearedmedium plots (Fig. 5.5). In small plots, Mazzaeila showed relatively faster colonization insummer and fall cleared plots than in spring and winter cleared plots (Fig. 5.4).109Interactions of the disturbance factorsFor percent cover of ephemeral algae there was a significant interaction betweensize of plot and season of clearing (p=O.OO9; Table 5.2). The greater abundance ofephemeral algae in medium plots was found only in spring and summer-cleared plots,whereas a similar abundance of these algae occurred in the medium and small plots clearedin fall and winter (Figs. 5.4 and 5.5). This difference, however, was not consistent duringthe successional period (Time x Size x Season interaction, p=O.OO1); the largest differenceoccurred only in October 1992 (Figs. 5.4 and 5.5).Responses of algae to the different sizes and seasons of disturbance were quitevariable. For example, relatively high cover and rapid colonization of Mazzaella werefound in summer and fall clearings of the small plots. In contrast, the rate of colonizationof this alga was slower in medium fall-cleared plots (Figs. 5.4 and 5.5).Taking time into account, the interpretation of the effect of size of clearing on Fucuscolonization gave additional variation. The pattern of Fucus abundance (medium plots>small plots) was not consistent during the experiment (Time x Size in MANOVA, p=O.OOl;the probability value in the MANOVA was used when the nonsphericity within subjectswas severe); for example, the size effect was significant only in summer plots 10 monthsafter clearing (Fig. 5.3).In contrast, the seasonal effect on Pelvetiopsis abundance (summer> winter, fallclearings) was similar between medium and small plots (Size x Season interaction,p=O.l 12) and also was consistent over successional time (Time x Season interaction,p=O.337; Table 5.2, Figs. 5.4 and 5.5).110Barnacle and limpet densitiesThere were significant differences in barnacle density (ANOVA,F(231)=4.088,53.708, 19.36 1; p0. 1, in all cases; ANOVA was used on each sample date). Although therelative abundance of limpets at month 4 was higher in small patches (5.9 per 100 cm2)than in medium patches (2.7 per 100 cm2), the mean densities averaged over all threesample dates were similar for all patch sizes (4.8, 4.7, 4.1 per 100 cm2 in small, medium,large, respectively).DISCUSSIONSize effects of disturbanceIn this study the rate of patch colonization was influenced by the size ofdisturbance. The medium (lOx 10 cm) patches were colonized the fastest, followed by thesmall (5x5 cm) and large (20x20 cm) patches. The present results were different fromthose of the previous studies either by Farrell (1989) or by Benedetti-Cecchi and Cinelli(1994), and indicate that negative factors that inhibited patch colonization of both small andlarge plots were effective in my study.111In small piots, adult plants surrounding the small patches tend to shade out and/orwhiplash the cleared space, decreasing the attachment and growth of propagules of theirown or other species (Dayton 1975, Sousa 1979a, Velimirov and Griffths 1979, Reed andFoster 1984, Kennelly 1989). These competitive interactions between the species recentlysettled in a patch and the organisms surrounding that patch have been invoked asmechanisms limiting colonization of small gaps (Connell and Keough 1985, Sousa 1985).Fucus and Pelvetiopsis were the most likely species to shade or whiplash the cleared spacein small plots with respect to the size of fucoids (5-7 cm in length) and plots. It is possiblefor fucoids growing adjacent to the patch to cover completely the 5x5 cm plots at low tides;this was commonly observed in the field. Whiplashing fucoids at high tides mightdeleteriously affect the settlement of barnacles and their own recruitment in this habitat, Myresults clearly negated the hypothesis that smaller patches are colonized more rapidly,proposed by Sousa (1985), and indicated that the above deterrent factor(s) appear to bemore important in patch recovery of the 5x5 cm plots in this community than a potentialbenefit of the greater edge ratio. Sousa (1984a) reported that slow colonization in smallpatches was caused by increased herbivore density (i.e., limpets). I could not find a strongevidence for intensive herbivory in small plots in my data. Limpet abundance was similaramong the three patch sizes, with a slightly higher density occurring in small patches onlyduring early successional stages.Algal recovery in the large patches was not completely inhibited, but only delayedin comparison with colonization of small and medium patches. Whatever the mechanism(s)accounting for the delay in recolonization in large plots, its (their) effect was strong in thefirst year, but generally decreased as succession proceeded. The slow (or delayed)colonization in the large patches may be explained by the following factors; 1) relativelystronger heat stress and desiccation in the center area of large patches may cause highermortality of settling algae, 2) short dispersal distance of component species (e.g., fucoids)may be responsible for limitation of colonization, or 3) simply, the lower ratio of edge area112is responsible for the slow colonization. Based on the sizes of component species in thiscommunity, it is clear that much of the area in the 20x20 cm plots is directly exposed to sunlight. Consequently, zygotes and embryos of fucoids may undergo higher mortality due tosevere cellular dehydration (Davison et al. 1993). Although there are no numeric dataavailable on the dispersal distance of Fucus and Pelvetiopsis, this distance is thought to be‘very short’ (Sousa 1984a, Hoffman 1987, Farrell 1989, Menge et al. 1993).The intensity of the factors limiting colonization in my two extreme sizes of patchesmay decrease as patch size changes towards an intermediate one. Medium patches maysimply receive the advantages of the reduction of the negative factors of the two sizeextremes. Similarly, the intermediate disturbance hypothesis (Horn 1975, Connell 1978)suggests that an intermediate frequency of disturbance may allow the coexistence of specieswith different life history strategies, which in turn allows for the highest species diversity.Furthermore, Miller (1982) claimed that size of disturbance provides an extension of theintermediate disturbance hypothesis. He explained that patches of intermediate size mayequally allow colonization of both the ‘competitive species’, which cover a disturbed areaby dispersing or growing primarily from around the patch perimeter, and the ‘colonizingspecies’, which colonize rapidly through high growth and/or dispersal rate. In thiscommunity, the three dominant algae may not functionally fit to the above categories.However, medium patches in this study were generally recolonized by a relatively well-mixed combination of all groups including Mazzaella (rare in large patches) and Fucus (lowin small patches). However, it may still be difficult to generalize the effect of patch size onthe rate of colonization because the rate may vary with habitat and algal assemblage. Forexample, in Farrell’s study (1989), although colonization in 3 sizes of clearing and tidalheight were similar, he found that the effect of surrounding plants, which was a negativeone in small patches of my study, was a positive one in its effect on the settlement of otheror their own species. Furthermore, Mazzaella cornucopiae was absent in his study areas,but Endocladia muricata, which is rare in my site, was abundant and colonized in the large113patches. In Benedetti-Cecchi and Cinelli’s study (1994), the tidal height and algalassemblage were different from my study, and they found that most algal species (e.g.,Corallina, Polysiphonia) colonized by the settlement of propagules, so vegetativepropagation was unimportant. My result is the first report which experimentally supportsMiller’s hypothesis from intertidal habitats and calls for replicate studies in other habitats.The effect of timing of disturbanceThe differences in algal abundance among patches of similar age but produced atdifferent seasons were minor for most species. However, there was a trend that differentalgal species responded differently to the seasonal effect of disturbance. First of all, Fucusand Pelvetiopsis, which are characterized as being slow-growing, perennial, and dispersedby propagules (e.g., zygotes), tended to dominate patches created just before’ (e.g., 2month) their recruitment peaks, compared to patches made at other times. As a result,summer clearings (August 1991) created 2 months before the recruitment peak of fucoids(Oct. 1991; Fig. 5.1) gave rise to greater cover of Pelvetiopsis in both small and mediumplots than plots cleared in any other season. Fucus showed a similar pattern but only in themedium patches. New substrata created just before’ the peak of reproduction may collectgreater numbers of fucoid propagules with no interference from previously-settled species.For these species, the time of gap creation is important because the initial recruitment maydetermine the later succession, as shown in other studies (Turner 1983b, Jara and Moreno1984). Jara and Moreno (1984) reported that plots cleared in spring were dominated byephemeral algae but, if cleared in fall, plots were filled by barnacles; these results were dueto seasonal availability of spore and inhibition between settled organisms and later species.On the other hand, for species such as Mazzaelki which propagate mainlyvegetatively, the timing of clearing generally did not influence dominance of this alga in theplots. However, in medium patches the abundance of Mazzaella in winter-cleared patches114(made 2 months before the abundance peak) was slightly greater than in the other patchescleared in different seasons. In this study, seasonal effects of disturbance were highlyspecies-specific; season-of-clearing had more effect on species dispersing by propagulesand less on species reproducing by vegetative ingrowth. Also, this study was supportiveof the generalization that the abundance of a species is most enhanced by disturbance if it iscreated when the propagules of the species are available for settlement (Denley andUnderwood 1979, Sousa 1979a, Hawkins 1981, Breitburg 1985, Kennelly 1987).Responses of barnacles and limpets to the size of disturbanceThe abundance of barnacles was influenced by patch size, and this may be due tothe deleterious effects of the algal canopy. Several authors have found that algal coverreduces barnacle settlement, or decreases their survival, by scouring young barnacles(Hawkins 1983, Woodin and Jackson 1979) or overgrowing their apertures (Farrell 1991,Dayton 1974). In contrast, it has been reported that barnacles are more abundant underalgal canopies due to a decrease in desiccation-caused mortality (Dayton 1971, Farrell1989). In this study, the negative effects of macroalgae on barnacles appeared to be moreimportant in controlling barnacle densities in the small patches. Both fucoids (4-7 cm)seemed ‘large’ enough to ‘whiplash’ young barnacles in the 5x5 cm plots. Mazzaellacornucopiae sometimes appeared to kill barnacles as it overgrew them; this might beanother factor responsible for the low density of barnacles in small patches.Limpet abundance was not influenced by clearing size; mean densities during thesuccession were similar in all patch sizes. Therefore, the relationship between limpetgrazing and algal colonization as related to patch size in this study did not support theresults obtained from the other studies. Some studies have found that limpet densitiesdecrease with increasing patch size in mussel beds (Suchanek 1978, Sousa 1984a) and inan upper intertidal zone (Farrell 1989), because limpets tend to aggregate at patch edges.115Therefore, small piots with a greater unit boundary area might collect a relatively greaterdensity of limpets (Farrell 1989). Some authors claimed that increased limpet density insmall patches were responsible for slower colonization of this patch (see Sousa 1985 forreferences). In this study, limpet densities were highest in small patches, but only initially;thus the density distribution of limpets among patch sizes showed high variability throughtime.Responses of individual algal species to disturbanceThe progression of species settlement and replacement in a disturbed patch can bepredicted to some degree when disturbance is analyzed by a multi-dimensional model.Several models have predicted the species diversity of patches by incorporating somecharacteristics of disturbance together rather than considering each one separately (Miller1982, Malanson 1984). This study has shown patterns of succession followingdisturbance on the basis of a two dimensional view, the size of disturbance and the time atwhich the disturbance occurred.What species come in when a gap of certain size is created in a certain season? Theanswer to this question can now be predicted with some certainty for this community. Thefollowing four cases are the possible predictions about community structure made by usingthe results of this chapter. 1) if a small gap is created in fall, the gap will be dominatedonly by Mazzaella. 2) if a small gap is formed in summer, the gap will be dominated byboth Mazzaella and Pelvetiopsis. However, it is expected that the canopy-forming fucoidmay finally exclude the short, turf-forming red alga by shading (Chapter 2). 3) if amedium gap is made in summer, Mazzaella and ephemeral algae will dominate space earlyin succession (e.g., <6 months), but later Fucus will gradually colonize and become a codominant. The patch may be a mixture of the 3 algal species, and their relative proportionwill fluctuate seasonally. A similar pattern of patch dynamics is expected in a medium gap116created in other seasons. 4) If a large gap is created in summer, the patch will recoverrelatively slowly, but fucoids are expected to dominate the gap with only a seasonalappearance of ephemeral algae. Mazzaella may not appear for at least first 3 years afterdisturbance (Chapter 4).To predict the natural dynamics of this Mazzaella-Fucus-Pelvetiopsis dominatedcommunity, at least two other factors must be known; frequency of disturbance size and themechanisms of interspecific interactions of the dominants (shown in Chapter 2). if largepatch sizes occur less frequently, and smaller sizes are more frequent in natural habitats(Sousa 1979b, Paine and Levin 1981, Farrell 1989), the population of M. cornucopiae willremain as a co-dominant in this community. Although the size frequency of disturbancewas not measured in this study, the three sizes of my experimental plots were similar tothose found to occur naturally (e.g., Oregon coasts, Farrell 1989). In a single-species-dominated community, the sequence of succession within a patch can be deterministic andthen lead to the monopolization of space within the patch by one competitively dominantand/or long-lived species. However, for multi-species dominated communities informationis required on the competitive abilities of all the component species in order to betterunderstand the within-patch dynamics. In Chapter 6, I present a more precise predictionabout community structure with the insight of interspecific interactions of componentorganisms which I achieved from the study in Chapter 2.117REFERENCESBegon, M., Harper, J. L., Townsend, C. R. (1990). Ecology: individuals, populationsand communities (2nd ed.). Blackwell Scientific Publications. London. 945 pp.Benedetti-Cinelli, L., Cinelli, F. (1994). Recovery of patches in an assemblage ofgeniculate coraline algae: variability at different successional stages. Mar. Ecol.Prog. Ser. 110: 9-18.Breitburg, D. L. (1985). Development of a subtidal epibenthic community: factors affectingspecies composition and the mechanisms of succession. Oecologia 65: 173-184.Connell, J. H. (1978). Diversity in tropical rain forests and coral reefs. Science 199: 1302-1310.Connell, J. H., Keough, M. J. (1985). Disturbance and patch dynamics of subtidal marineanimals on hard substrata. In: Pickett, S. T. A., White, P. S. (eds.) The ecology ofnatural disturbance and patch dynamics. Academic Press. Orlando. pp. 125-151.Davis, R. M., Cantlon, J. E. (1969). Effect of size area open to colonization on speciescomposition in early old-field succession. Bull. Torr. Bot. Club 96: 660-673.Davison, I. R., Johnson, L. E., Brawley, S. H. (1993). Sublethal stress in the intertidalzone: tidal emersion inhibits photosynthesis and retards development in embryos ofthe brown alga Pelvetiafastigiata. Oecologia 96: 483-492.Dayton, P. K. (1971). Competition, disturbance and community organization: theprovision and subsequent utilization of space in a rocky intertidal community. Ecol.Monogr. 41: 35 1-389.Dayton, P. K. (1974). Dispersion, dispersal and persistence of the annual intertidal alga,Postelsiapalmaeformis Ruprecht. Ecology 54: 433-438.Dayton, P. K. (1975). Experimental evaluation of ecological dominance in a rockyintertidal algal community. Ecol. Monogr. 45: 137-159.Dayton, P. K., Tegner, M. J., Parnell, P. E., Edwards, P. B. (1992). Temporal andspatial patterns of disturbance and recovery in a kelp forest community. Ecol.Monogr. 62: 421-445.Denley, E. J., Underwood, A. J. (1979). Experiments on factors influencing settlement,survivorship and growth of two species of barnacles in New South Wales. J. Exp.Mar. Biol. Ecol. 36: 269-293.Emerson, S. E., Zedler, J. B. (1978). Recolonization of intertidal algae: an experimentalstudy. Mar. Biol. 44: 3 15-324.Farrell, T. M. (1989). Succession in a rocky intertidal community: the importance ofdisturbance size and position within a disturbed patch. J. Exp. Mar. Biol. Ecol.128: 57-78.Farrell, T. M. (1991). Models and mechanisms of succession: an example from a rockyintertidal community. Ecol. Monogr. 61: 95-113.118Foster, M. S. (1975). Algal succession in a Macrocystis pyrifera forest. Mar. Biol. 32:313-329.Gurevitch, J., Chester, J. S. T. (1986). Analysis of repeated measures experiments.Ecology 67: 25 1-255.Hawkins, S. J. (1981). The influence of season and barnacles on the algal colonization ofPatella vulgata exclusion areas. J. Mar. Biol. Ass. U.K. 61: 1-15.Hawkins, S. J. (1983). Interactions of Patella and macroalgae with settling Semibakinusbalanoides (L.). J. Exp. Mar. Biol. Ecol. 71: 55-72.Hoffmann, A. J. (1987). The arrival of seaweed propagules at the shore: a review. Bot.Mar, 30: 151-165.Horn, H. S. (1975). Markovian processes of forest succession. In: Cody, M. L.,Diamond, J. M. (eds.) Ecology and evolution of communities. Harvard UniversityPress. Cambridge, Mass. pp. 196-211.Jara, H. F., Moreno, C. A. (1984). Herbivory and structure in a midlittoral rockycommunity: A case in southern Chile. Ecology 65: 28-38.Kennelly, S. J. (1987). Physical disturbances in an Australian kelp community. I.Temporal effects. Mar. Ecol, Prog. Ser. 40: 145-153.Kennelly, S. J. (1989). Effects of kelp canopies on understorey species due to shade andscour. Mar. Ecol. Prog. Ser. 50: 123-130.Keough, M. J. (1984). Effects of patch size on the abundance of sessile marineinvertebrates. Ecology 65: 423-437.Malanson, G. P. (1984). Intensity as a third factor of disturbance regime and its effect onspecies diversity. Oikos 43: 411-413.Mead, R. (1988). The design of experiments. Cambridge University Press. Cambridge.Menge, B. A,, Farrell, T. M., Olson, A. M., Van Tamelen, P., Turner, T. (1993). Algalrecruitment and the maintenance of a plant mosaic in the low intertidal region on theOregon coast. J. Exp. Mar. Biol. Ecol. 170: 91-116.Miller, T. E. (1982). Community diversity and interactions between the size and frequencyof disturbance. Am. Nat. 120: 533-536.Myers, J. L., Well, A. D. (1991). Research design and statistical analysis. HarperCollinspublishers Inc. New York. 713.Osman, R. W. (1977). The establishment and development of a marine ephifaunalcommunity. Ecol. Monogr. 47: 37-63.Paine, R. T. (1977). Controlled manipulations in the marine intertidal zone and theircontributions to ecological theory. Spec. Publ., Acad. Nat. Sci. Philadelphia No.12: 245-270.119Paine, R. T,, Levin, S. A. (1981). Intertidal landscapes: disturbance and dynamics ofpattern. Ecol. Monogr. 51: 145-178.Palumbi, S. R., Jackson, I. B. C. (1982). Ecology of cryptic coral reef communities. 2.Recovery from small disturbance events by encrusting bryozoa: the influence of“host” species and lesion size. J. Exp. Mar. Biol. Ecol. 64: 103-115.Reed, D. C., Foster, M. S. (1984). The effects of canopy shading on algal recruitment andgrowth in a giant kelp forest. Ecology 65: 937-948.Sousa, W. P. (1979a). Experimental investigations of disturbance and ecologicalsuccession in a rocky intertidal algal community. Ecol. Monogr. 49: 227-254.Sousa, W. P. (1979b). Disturbance in marine intertidal boulder fields: the non-equilibriummaintenance of species diversity. Ecology 60: 1225-1239.Sousa, W. P. (1980). The responses of a community to disturbance: the importance ofsuccessional age and species’ life histories. Oecologia (Berlin) 45: 72-81.Sousa, W. P. (1984a). Intertidal mosaics: patch size, propagule availability, and spatiallyvariable patterns of succession. Ecology 65: 19 18-1935.Sousa, W. P. (1984b). The role of disturbance innatural communities. Ann. Rev. Ecol.Syst. 15: 353-391.Sousa, W. P. (1985). Disturbance and patch dynamics on rocky intertidal shores. In:Pickett, S. T. A., White, P. S. (eds,) The ecology of natural disturbance and patchdynamics. Academic Press. Orlando. pp. 101-124.Suchanek, T. H. (1978). The ecology of Mytilus edulus L. in exposed rocky intertidalcommunities. J. Exp. Mar. Biol. Ecol. 31: 105-120.Turner, T. (1983a). Complexity of early and middle successional stages in a rockyintertidal surfgrass community. Oecologia 60: 56-65.Turner, T. (1983b). Facilitation as a successional mechanism in a rocky intertidalcommunity. Am. Nat. 121: 729-738.Underwood, A. J. (1981). Techniques of analysis of variance in experimental marinebilogy and ecology. Oceanogr. Mar. Biol. Ann. Rev. 19: 513-605.Velimirov, B., Griffiths, C. L. (1979). Wave-induced kelp movement and its importancefor community structure. Bot. Mar. 22: 169-172.Wilkinson, L., Hill, M. A., yang, E. (1992). SYSTAT: Statistics, version 5.2.1 edition.SYSTAT. Evanston, IL, USA.Winer, B. J. (1971). Statistical principles in experimental design (2nd ed.). McGraw-Hill.New York.Woodin, S. A., Jackson, J. B. C. (1979). Interphyletic competition among marinebenthos. Am. Zool. 19: 1029-1043.Table5.1Theeffectofsizeofexperimental clearings(5x5andlOx10cm) ontotalalgalcover.Aseparaterepeatedmeasuresanalysisof variancewasappliedondatafromeachseason.Largeplots(20x20 cm)werenotincludedinanalysis,asdiscussedintext.SourceofvariationiStatisticSpring+SummerfallWinterBetweensubjectSize1MS5872.27125.62782.47191.0F4.58*4.98*1.816.32*Error28MS1281.01431.81537.21138.2WithinsubjectTime7MS4112.23565.12685.73116.7F29.1814.2413.2418.41TimexSize7MS246.7211.1405.4560.2F1.750.841.203.31*Error196MS140.9250.3202.8169.3MultivariaterepeatedmeasuresanalysisEffectTimeWL-i-+0.1910.1660.3850.31F12.0815.805.03**6.98*TimexSizeWL++0.5990.6430.6240.57F1.911.751.902.37UnivariatewithinsubjectsFandprobabilityvalueswereadjustedusingtheHuynh-Feldtestimator(epsilon=0.5134, 0.4716,0.6971,0.5752forspring,summer,fall,winter,respectively).Systat (Wilkinsonetal.1992) providesautomaticallyadjustedFvaluesandtheprobabilities inthecaseofnonsphericity.+14replicatespersizeofclearingwereusedforanalysisduetomissingdata.+-i-Wilks’lambda.*p.<0.05;**p.00Fw0Wi00030EC.)0o20•(\\JccW(I)I—Dcc 100Wcc0Fig. 5.1 Seasonal changes of algal percent cover and the number of fucoid recruits inunmanipulated plots (20x20 cm) at Prasiola Point for two years. Data are the mean ±SE offour replicates. EPH for ephemeral algae, MAZ for Mazzaella cornucopiae, FUC forFucus distichus, PEL for Pelvetiopsis limitata.----O----RJC---—&---- PEL IJI IocIbI I124w>00I—zw0w0MONTHS AFTER CLEARINGFig. 5.2 Recolonization of total algae in three different sizes of clearing. Large clearings= 20x20 cm, medium clearings = lOxlO cm, small clearings = 5x5 cm. Plots cleared in thesummer (August 1991) were only compared for the size effect on patch recovery. Data arethe mean ±SE of fifteen replicates for small and medium plots and of four replicates forlarge plots.2 4 6 8 10 12 14 16 18 20- i—-I I I I -I I I2 4 6 8 101214161820MONTHS AFTER CLEARINGFig. 5.3 Patch recovery of each dominant algae, Mazzaella, Fucus, Pelvetiopsis, andephemeral algae in three different sizes of clearing. Data shown are from the summer-cleared (August 1991) plots. Data are the mean ±SE of fifteen replicates for small andmedium piots and of four replicates for large plots.Mazzaella125FucusIT30-20-10-0-30-20-10.0-Ui>00IzUi0Ui0I I I I I IPelvetiopsisI I I I I I IEphemeral algaeI—C--— LARGE--—0—-- MEDIUM----0---- SMALLTTI I I I I I I I I I2 4 6 8 101214161820126Fucus—U--—-- SPRING.0.----- SUMMER----0---- FALL----&--- WINTERFig. 5.4 The effect of season of clearing on algal recovery of each species in small plots(5x5 cm). The time for each seasonal clearing is August 1991 (for summer), October 1991(for fall), February 1992 (for winter) and April 1992 (for spring). Data are the mean ±SEof fifteen replicates.MazzaellaI30-20-10.w> 0-0C-)I—zw0a:U] -20-10-0-TII I I I I I I I I I I IPelve tiopsisIlillIllIll IIEphemeral algaeT HIoc vWF,Fig. 5.5 The effect of season of clearing on algal recovery of each species in mediumplots (lOxlO cm). See Fig. 5.4 for captions and the number of replicates.Mazzaella127FucusT I TT30•2010.> 0•0C.)I—zwC) 30.w02010.0-11I I I I I I I III II IPelvetiopsisI I I I I I I I IEphemeral algae-D-----0--------.---.-:SPRINGSUMMERFALLWINTERIITB. LIMPETFig. 5.6 Barnacle and limpet densities in the three sizes of patch at three sampling dates(4, 10, 16 months after clearing). Data are the mean ±SE of fifteen replicates for small andmedium piots and of four replicates for large plots. When results of ANOVA on three sizeswere significant, results of Tukey’s HSD tests were labeled (e.g., S LM indicates thatdensity in small patch is significantly greater than that of either large or medium patch).N/S for p>O.05.128A. BARNACLE20(150100c’JEC)C0a:waC’)wF-(I)zwID108642MONTHS AFTER CLEARING129CHAPTER 6PREDICTIVE MODELS FOR COMMUNITY STRUCTURE FOLLOWINGENVIRONMENTAL CHANGESThe objectives of this chapter are to synthesize the major interactions among all thecomponent species in the community and to predict the structure of the community whenthe presence or density of individual components is altered.THE MECHANISMS AND COMPLEXITY OF SPECIES INTERACTIONSThe results presented in this thesis demonstrate that there are detectable biologicalinteractions among all component species in the community and that these interactions canhave important consequences for the specific patterns of distribution and abundance of eachorganism. The major interactions among the component species are summarized in Fig.6.1.Competition was the predominant interaction occurring between algal species (A,G, H, J, N, 0). Competitive interactions in this community largely comprised twodifferent mechanisms: preemption (A, J, and G) and shading (H). In the absence oflimpets ephemeral algae rapidly covered the substratum at the early successional stage andprevented the settlement of the later colonists such as fucoids. However, the seasonalappearance and fluctuating abundance of the ephemeral algae allowed fucoids to graduallyinvade space; thus the fucoids eventually outcompeted the ephemerals. Therefore, theinteraction (A) occurs under two conditions: at the early successional stage and in theabsence of limpets. As long as a disturbance occurs and succession proceeds in the gap,the first condition will occur. Reduced limpet density can occur as a result ofenvironmental impacts (such as introduction of certain predators, harvesting by humans).130The possible consequence of this situation on community structure is discussed in the nextsection of this chapter, where key species in this community are considered. The effect ofspace preemption by Mazzaella on fucoid recruitment (G) was measured in a maturecommunity, unlike the interaction (A). Low recruitment of the two fucoids within theMazzaella beds indicated that a dense turf of this red alga blocked fucoid recruits and/orinhibited the growing recruits (0), although removal of Mazzaella turf did not significantlyincrease fucoid recruitment. This indicates that the outcome of an interaction may not beconsistent in the natural habitats and that such an outcome is often correlated with otherfactors which sometimes are not easily detectable. The interaction (J) between Mazzaellaand the post-recruitment stage of Fucus requires two assumptions to explain why thelifespan of Fucus within the Mazzaella turf was relatively short. The first assumption wasthat there was limited space for holdfast expansion as Fucus grew because the basal crustsof the Mazzaella turf preempted space. The second was that the relatively wider thallus ofFucus (compared to Pelvetiopsis) might be subjected to a greater drag force by waveaction. Therefore, the outcome of interaction (J) is a combination of space preemption andof a physical factor.Both fucoids affected Mazzaella by forming a canopy (H) when the fucoidssuccessfully settled and grew to an adult plant within or near Mazzaella beds. The shadingeffect of high intertidal species of fucoids on other neighbor species is rarely reported (butsee Schonbeck and Norton 1980) in algal interactions. The interaction (N) has beenobserved later in the successional sequence, as the percent cover of Pelvetiopsis decreasedas that of Fucus coincidentally increased in a few plots. The mechanism for this interactionis unknown. A similar pattern between these two morphologically similar species has beenobserved in Sousa’s (1984) work. Based on Sousa’s result, Chapman (1995) proposed ageneralization for the common sequence of succession in high shores of the northeastPacific, e.g., diatoms -> Ulva -> Pelvetiopsis -> Fucus. However, the mechanism of theinteraction between Fucus and Pelvetiopsis was not described in either Sousa’s research or131this thesis. My impression is that Pelvetiopsis is a better adapted species to the stressfulhigh intertidal habitat than Fucus, since Pelvetiopsis grew independently of the presence ofMazzaella and barnacles. A difference, if present, between these two species would be thatFucus might have a more successful reproductive strategy (e.g., more output ofpropagules) and faster growth rate than Pelvetiopsis. To date, this is a pure speculation.In Chapman?s recent review (1995), there are no data available on these variables.With the information from this study, I suggest two general features of algalinteractions: reversal of competitive dominance and the importance of morphologicalcharacters. First, reversal of competitive dominance can be a common phenomenon amongbenthic macroalgae. This was the case of interactions between ephemeral algae and fucoids(A and 0) and between Mazzaella and fucoids (G and H), hence in four cases out of sixstudied. Reversal occurred as succession proceeded or the life history stages ofcompetitors changed, or sometimes due to facilitation by a herbivore (L). This bidirectional competition was one of the reasons that the species maintains its diversity in thesystem. Second, competitive dominance was related to morphological characteristics ofplants. The common characteristics of species capable of space preemption were fastgrowth, spreading habit and/or turf-forming, whereas species capable of shading werelarge and/or of erect form. These results provide useful evidence for the relationshipbetween plant traits and competitive dominance which has not been extensively investigatedin algal competition (Olson and Lubchenco 1990). Herbivory by both limpets (B) andsnails (L) had some similarities. First, both herbivores expressed selectivity for food;limpets preferred ephemeral algae and snails preferred Mazzaella. Second, herbivory wasclosely related to competitive interactions among the prey species. More importantly fortheir role at the community level, limpets facilitated algal succession and snails influencedin part the reversal of the competitive direction.Facilitations or positive interactions occurred in the system and these can be dividedinto two types depending on their mechanisms: direct and indirect interactions. Direct132facilitation was observed at three places. The interaction (K) was based on fieldobservation and other studies (Boulding and Van Alstyne 1993) in which a dense turf ofMazzaella provided a refuge for snails against wave impact and desiccation. In interaction(1), Mazzaella enhanced Fucus survivorship for those individuals which grew at the edge ofthe Mazzaelkz turf. The preceeding two cases of direct facilitation were mechanically relatedto amelioration of harsh physical conditions. However, in the interaction (F), barnaclesdirectly facilitated Fucus settlement; this was not related to physical stress, but rather to thepresence of limpets. This facilitation was effective only when limpets reduced ephemeralalgae which inhibited Fucus settlement. In other words, the intensity of the barnacle’sfacilitation of Fucus (F) was less strong than the intensity of competition (A) betweenephemerals and Fucus because the effect of the facilitation was not detectable in the absenceof limpets. Both indirect facilitations (C) were coffelated with grazing. Limpets facilitatedfucoid colonization by reducing the abundance of the competitors of Fucus, ephemeralalgae. Snails also enhanced fucoid recruitment by reducing the percent cover of Mazaella,a species which also inhibited fucoid recruitment.Some evidence has been observed that algae had a deleterious effect on barnacles(D). Ephemeral algae (e.g., benthic diatoms, Enteromorpha spp.) were observed toovergrow, and eventually cause mortality of, barnacles, but this interaction required aprecondition of no limpets existing in the system. However, the vegetatively propagatingand laterally growing Mazzaella was often found to overgrow barnacles which grew in thevicinity of its turf, despite the presence of limpets. Barnacles also suffered from theforaging activity of limpets (E), which might bulldoze the propagules of barnacles.In conclusion, the overview of major interactions among all component speciesindicates that the current structure of the community is a consequence of a complex andnon-hierarchical interaction network, which includes reversal of dominance and indirectinteractions. The non-hierarchical interactions among algal species, and their well-balanced133responses to disturbance (e.g., different capabilities of recovery against the different sizesof disturbance), suggest a high likelihood of maintaining diversity in this algal community.PREDICTIONS OF THE EFFECTS OF POTENTIAL ENVIRONMENTALIMPACTS ON THE COMMUNITY STRUCTUREA primary goal of empirical studies in ecology is to validate and increase theprecision of predictive models for the structure of communities, so that potentialenvironmental impacts might be assessed (Dayton 1971, Paine 1974, Menge 1976,Underwood et al. 1983). Environmental impacts which may come in a predictable way(e.g., seasonal desiccation or predator fluctuation) or stochastically (e.g., oil spills, storms)may result in a considerable reduction or depletion of certain species in the system. Such achange will influence other species which are directly or indirectly linked to that organism,and will eventually lead to reorganization of the community. However, predicting thestructure of a community after a particular disturbance remains difficult, even if patterns ofinteractions among all major component species are known, because the outcome ofbiological interactions is variable in time and space, as demonstrated in many experimentalresults. Thus, it is difficult to examine the relative intensity of interactions in a non-hierarchical interaction network. Nonetheless, it may be instructive to assess how far thepresent experimental analysis of this community has allowed accurate predictions to bemade about the fate of the community in response to diverse disturbances, or simply as toits persistence through time.Below, I finish my thesis with some predictive models about the effect of potentialenvironmental impacts on community structure. Possible scenarios of community-levelresponses leading to reorganization of existing components were predicted in the light ofthe results of my in situ experiments. The predictions for cases 1 to 3 were made on theestablished (mature) community, while for cases 4 and 5 the predictions are for a newlyformed patch.134CASE 1: Absence of limpets in the system.The first response of the community to the removal of limpets may be a dramaticincrease of ephemeral algae. Subsequently, abundance of Pelvetiopsis, Fucus andbarnacles will decrease due to the competitive superiority (possibly temporary) ofephemeral algae for space. The reduction by ephemeral algae may also be applicable toMazzaella (Olson 1985, 1992). Competition for space between the ephemeral algae andother component species will be more intense during the growing season of ephemerals(October to April) than at other times of the year. Therefore, the recruitment of fucoids inOctober (the peak of recruitment for both fucoids) can be severely affected by ephemeralalgae (especially benthic diatoms; Fig. B.2) rapidly preempting space. The maintenance ofthe fucoid population will be highly dependent upon the seasonal gap in abundance of theephemeral algae (May to September) and upon at least some of the fucoid recruitsgerminating in this season. With the increasing abundance of ephemeral algae, Mazzaellawould be more affected than any other dominant macroalgae because it is smaller thanfucoids and reproduces largely vegetatively. The abundance of barnacles will graduallyincrease especially when ephemeral algae are low in summer. Therefore, the communitywill be dominated by Ephemerals-Fucus-Pelvetiopsis and the relative abundance of thesethree components will be influenced by the degree of reduction of limpet density. Barnacleabundance is expected to fluctuate with the seasonal cycle of ephemeral algae.CASE 2: Absence of Mazzaella in the system.The existence of Mazzaella in the system has a negative effect on fucoid recruitmentand a positive effect on Fucus survival. Unlike the effect of ‘total pruning’ of Mazzaellablades (Chapter 2), the complete removal (including basal crusts) of this alga willapparently cause increasing recruitment of both fucoids. Particularly, direct facilitation ofFucus recruitment by barnacles (F) becomes possible because limpets exist in the system(see further explanation in the previous section of this chapter). However, for post-135recruitment survivorship, Fucus is at a relative disadvantage compared to Pelvetiopsisbecause no habitat amelioration by Mazzaella is available. The relative abundance of Fucusand Pelvetiopsis in the community becomes a function of the relative intensity of the twointeractions (F and I); I did not determine whether competition between these fucoids existsor not (except for the interaction (N)). Since there is evidence that the barnacle, Balanusglandula, enhanced the recruitment of Pelvetiopsis limitata (Farrell 1991), it is assumed thatthe interaction (F) may also apply to Pelvetiopsis at my study sites even though the datawere not available from this study. If this assumption holds, Fucus abundance would beaffected by the interaction (M) because of the absence of Mazzaella’ s protection; therefore,Pelvetiopsis wiil be relatively more abundant than Fucus in the system. The density ofbarnacles wifi increase because there is no Mazzaella overgrowth, but the density of snailswill be much reduced in the habitat because no preferred food and no refuge exist. So, inthe absence of Mazzaella the community will be reshaped into a Pelvetiopsis-barnacledominated structure.CASE 3: Absence of Fucus in the system.Mazzaelkj abundance will probably increase because of the reduced shading effectby Fucus. However, the abundance of Pelvetiopsis will be variable depending on itsrelationship with Fucus and the relative intensity of direct and indirect interactions. IfPelvetiopsis is competitively inferior to Fucus (the interaction N), the abundance ofPelvetiopsis will increase. If they are in a mutualistic relationship (mutually increasedsurvivorship under strong desiccation and wave impact), Pelvetiopsis density will decreasewhen Fucus is absent. On the other hand, increased Mazzaella will negatively and directlyaffect Pelvetiopsis (G). Therefore, the possible outcomes in the case of Pelvetiopsis areunclear, indicating the need for information on this Fucus-Pelvetiopsis interaction. Asimilar uncertainty will appear in the case of the absence of Pelvetiopsis.136CASE 4: No Mazzaella when a small/medium (25-100 cm2) gap is formed insummer.A possible scenario of succession is shown in Fig. 6.2. In the fall following thedisturbance, limpets and ephemeral algae may be the first organisms appearing in the gap.Ephemeral algae (e.g., diatoms) will, however, be minimal due to grazing by limpets. Inwinter, limpets still control the abundance of ephemeral algae but Porphyra spp. mayappear in small amounts because they seem to be a less prefered species than diatoms(Table 4.2). This negative effect of limpets on ephemerals may indirectly facilitatebarnacles although limpets are also capable of grazing on young barnacles (Dayton 1971,Underwood et al. 1983, this study). As barnacles become larger in the spring, barnaclesmay enhance (facilitate) settlement of all algal species (especially fucoids). The indirectfacilitation of fucoids by limpets may occur by limpets grazing on ephemeral algae whichinhibit fucoid settlement. In summer months, ephemeral algae will disappear but perennialfucoids will remain. At this time limpets, excluded by barnacles in the patch, may migrateto a lower zone to forage for alternative foods (Olson 1992). A possible reduction of theFucus population, due to both strong desiccation and the absence of Mazzaella, can beexpected. The patch will ultimately be dominated by Pelvetiopsis-Fucus-barnacles.However, occasional inhibition of fucoids on barnacles can be expected as fucoids grow onthe tests of barnacles; increased drag forces on adult fucoids (especially Fucus) mayremove both plants and barnacles (Jernakoff 1985, Farrell 1991). Further invasion ofephemerals will be minimal because of fucoid preemption of space and a possiblereintroduction of limpets. Thus, limpets may not recover their initial abundance in the plotsbecause the patch is already full of perennial fucoids and adult barnacles.CASE 5: No limpets when a large gap (e.g., 400 cnz2) is formed in winter.A likely scenario of succession is shown in Fig. 6.3. In the spring following thedisturbance, only a few ephemeral algae will appear in the plot along with a few juvenile137barnacles. Barnacle density will be slightly increased in the summer but no otherorganisms may be visible. However, in the fall, a rapid colonization of some ephemeralalgae (probably diatoms) will occur along with a few recruits of fucoids. At this time,diatoms may effectively interfere with all other organisms in the plots by preventing newsettlement of other algae and by killing existing barnacles (Castenholz 1961), In the latespring (April-June), as ephemeral algae decrease, barnacles may re-establish on thesubstratum and facilitate fucoid (maybe Fucus) colonization. Where space is limited,competition between fucoids and ephemeral algae may occur. In the summer, presumablydesiccation-resistant Pelvetiopsis would be more abundant than Fucus; this pattern mightvary depending on microhabitat conditions (e.g., slope, direction, wave-exposure).Barnacles may benefit from the fucoid canopy in that the latter reduces heat and desiccation(Dayton 1971, Farrell 1989). Ephemeral algae retain a low abundance. This summerstructure will alternate with the other patterns which are typical in fall, winter and spring.The typical community organization in the latter seasons may be that Fucus, and ephemeralalgae with similar abundance, compete for space. Fucus may inhibit both Pelvetiopsis (asin the interaction N in Fig 6.1) and also barnacles by pulling the latter off the rocksubstratum when it (Fucus) is removed by drag force (Jernakoff 1985, Farrell 1991). IfMazzaella invades the plot, this alga will be kept in check by both fucoids (the interaction Hin Fig. 6.1).The accuracy of the above predictions on community reorganizations under variousenvironmental conditions can be affected by at least the following three factors: 1) theunpredictability of the timing or intensity of recruitment of any component species, 2) theproximity of reproductive adult plants, and 3) the spatial variability of the type and intensityof biological interactions. The unpredictability of recruitment events has been pointed outas a factor influencing spatial pattern in marine community structure (Paine 1979,Underwood et al. 1983, Sousa 1984, Reed et al. 1988). In the present study, therecruitment of Pelvetiopsis was unexpectively low in the October 1992, which was138considered as the time for recruitment of this alga (Fig. 5.1). The variation in patchcolonization and early species composition may depend largely on the proximity ofreproductive plants (Sousa 1984). It may be difficult to predict structure with any accuracyif the vegetation surrounding a gap created by a disturbance is monospecific, because thedistance of spore dispersal of some species (e.g., Fucus, Pelvetiopsis) is known to be <1m (Menge et al. 1993). Also, my data indicate that there were some possibilities that thetype and intensity of biological interactions can be changed depending on wave-exposuregradients (e.g., Mazzaella-Fucus interaction). As suggested by Underwood et al. (1983),for future experimental manipulations in the study of intertidal communities, examination ofthe range of potential interactions at the various naturally occurring densities is necessary toconstruct more powerful predictive models. The interactions and mechanisms reported inthis thesis improve our understanding of the functional relationship among the differentspecies in this assemblage and enable such predictions to be made for a common highintertidal community.139REFERENCESBoulding, B. 0., Van Aistyne, K. L. (1993). Mechanisms of differential survival andgrowth of two species of Littorina on wave-exposed and on protected shores. I.Exp. Mar. Biol. Ecol. 169: 139-166.Castenholz, R. W. (1961). The effect of grazing on marine littoral diatom populations.Ecology 42: 783-794.Chapman, A. R. 0. (1995). Functional ecology of fucoid algae: twenty-three years ofprogress. Phycologia 34: 1-32.Dayton, P. K. (1971). Competition, disturbance and community organization: theprovision and subsequent utilization of space in a rocky intertidal community. Ecol.Monogr. 41: 351-389.Farrell, T. M. (1989). Succession in a rocky intertidal community: the importance ofdisturbance size and position within a disturbed patch. J. Exp. Mar. Biol. Ecol.128: 57-78.Farrell, T. M. (1991). Models and mechanisms of succession: an example from a rockyintertidal community. Ecol. Monogr. 61: 95-113.Jernakoff, P. (1985). The effect of overgrowth by algae on the survival of the intertidalbarnacle Tesseropora rosea Krauss. J. Exp. Mar. Biol. Ecol. 94: 89-97.Menge, B. A. (1976). Organization of the New England rocky intertidal community: roleof predation, competition, and environmental heterogeniety. Ecol. Monogr. 46:355-393.Menge, B. A., Farrell, T. M., Olson, A. M., Van Tamelen, P., Turner, T. (1993). Algalrecruitment and the maintenance of a plant mosaic in the low intertidal region on theOregon coast. J. Exp. Mar, Biol. Ecol. 170: 91-116.Olson, A. M. (1985). Early succession in beds of the red alga, Iridaea cornucopiae Post. &Rupr. (Gigartinaceae): Alternate pathways. M.S. Thesis. Oregon State University.Olson, A. M. (1992). Evolutionary and ecological interactions affecting seaweeds. Ph. DThesis. Oregon State University. Corvallis, OregonOlson, A. M., Lubchenco, J. (1990). Competition in seaweeds: linking plant traits tocompetitive outcomes. 3. Phycol. 26: 1-6.Paine, R. T. (1974). Intertidal community structure. Experimental studies on therelationship between a dominant competitor and its principal predator. Oecologia15: 93-120.Paine, R. T. (1979). Disaster, catastrophe and local persistence of the sea palm Postelsiapalmaeformis. Science 205: 685-687.Reed, D. C., Laur, D. R., Ebeling, A. W. (1988). Variation in algal dispersal andrecruitment: the importance of episodic events. Ecol. Monogr. 58: 32 1-335.Schonbeck, M. W., Norton, T. A. (1980). Factors controlling the lower limits of fucoidalgae on the shore. J. Exp. Mar. Biol. Ecol. 43: 13 1-150.Sousa, W. P. (1984). Intertidal mosaics: patch size, propagule availability, and spatiallyvariable patterns of succession. Ecology 65: 1918-1935.Underwood, A. J., Denley, E. J., Moran, M. J. (1983). Experimental analyses of thestructure and dynamics of mid-shore rocky intertidal communities in New SouthWales. Oecologia 56: 202-2 19.140SolidlineDashedlineArrowheadRoundheadClearpointDarkpointstronginteractionweakinteractionnegativeinteractionpositiveinteractionindirectinteractiondirectinteractionFig.6.1Thesummaryofinteractionsamongthemajorcomponentorganismsshowninthisstudy.PELandFUCintheupperdiagramindicatePelvetiopsisandFucusattherecruitment stage,whilethoseinthelowerindicatethefucoidsafter recruitment stage.Small lettersaretheabbreviationsfor typesofinteraction:(co)for competition,(fa)forfacilitation,(gr) forgrazing,(ov)forovergrowth,(pr)forpreemption,(pt)forprotection,(re)forrefuge, (sh)for shading.IEPHfIPELf.NcoS55 Oco5WAVEIMPACT..-DESICCATIONAlM_________________LEGENDFUCf————_&coA-EPH4Solidline:stronginteractionDashedline:weakinteractionArrowhead:negativeinteractionRoundhead:positiveinteractionClear point:indirectinteractionDarkpoint:directinteractionFig.6.2Apredictivemodel forcommunitystructure,intheabsenceof Mazzaella,whenasmall/mediumgap(e.g.,5x5tolOx 10cm)is createdinsummer.Thesizeofthecircles representstherelativeabundanceofcomponentspecies.FALLI)4?SUMMERWINTER‘>SPRING‘LEGENDFALLSolidlineDashedlineArrowheadRoundheadClear pointDarkpointI IS SI *S S .stronginteractionweakinteractionnegativeinteractionpositiveinteractionindirectinteractiondirectinteractionFig.6.3Apredictivemodelforthecommunitystructure,intheabsenceoflimpets,whenalargegap(e.g.,20x20cm) iscreatedinwinter.Thesizeofcirclerepresentstherelativeabundanceofcomponentspecies.SPRINGESUMMERFALLWINTERS>SPRING‘>SUMMERLEGENDFALLWINTERSPRING(J144APPENDIX AANOVA tables for the natural densities of snails from Chapter 3Table Al Summaries of ANOVAs on the natural density of snails at Prasiola Point. A.densities of snails in monospecific patches of the three dominant algae. B. densities ofsnails in general habitats (3 transect lines).A. ANOVA table- monospecific patchesSource MS.Species 2 151.49 163.79 0.0000Time 8 30.83 33.34 0.0000Species*Time 16 4.35 4.71 0.0000Error 108 0.92B. ANOVA table - general habitatsSource MS.Transect 2 13.75 7.81 0.0006Time 8 15.81 8.98 0.0000Transect*Time 16 3.31 1.88 0.0278Error 132 1.76145Ui>0UiCl)UiC)Iii0Cl)Figure B.1 Farrell’s model for the effect of consumers on the rate of succession ( -consumers increase the rate of succession, 0 - no effect, + - consumers decrease therate of succession) cited from Farrell (1991).APPENDIX BSupplementary data and results from other studies in Chapter 4MODEL OF SUCCESSIONCC C.).2ci)0 CU.I- U-EarlySuccessionalSpeciesEquivalentLaterSuccessionalSpecies0 +(I)I—0-J0E000C”zw>0C-)zw0wA. +B-L146-------0 Porphyra-0 Urospora----h---- Enteromorpha- --- -- Mastocarpus—D-—— Diatoms80-60-40-200-80-60-40-20-0.I I IB. -B-L0- Porphyra----0---- Urospora----h---- Scytosiphon— ——— —- Callithamnion—C--—-- Diatomsç. obFig. B.2 Dynamics of ephemeral algae in limpet-excluded piots (-L), with(+B) and without (-B) barnacles.147NVan Tamelen (1987)Dethier & Duaciins (1984)LEGENDSolid line : direct interactionDashed line : indirect interactionArrow head : negative interactionRound head : positive interactionALG1 : microalgaeALG2 : macroalgaeCHI : chitonBAR : barnacleLIM : limpetDunaan (1986)VFig. B.3 Direct and indirect interactions shown in other studies."@en ; edm:hasType "Thesis/Dissertation"@en ; vivo:dateIssued "1995-11"@en ; edm:isShownAt "10.14288/1.0088097"@en ; dcterms:language "eng"@en ; ns0:degreeDiscipline "Botany"@en ; edm:provider "Vancouver : University of British Columbia Library"@en ; dcterms:publisher "University of British Columbia"@en ; dcterms:rights "For non-commercial purposes only, such as research, private study and education. Additional conditions apply, see Terms of Use https://open.library.ubc.ca/terms_of_use."@en ; ns0:scholarLevel "Graduate"@en ; dcterms:title "Intertidal community structure, dynamics and models : mechanisms and the role of biotic and abiotic interaction"@en ; dcterms:type "Text"@en ; ns0:identifierURI "http://hdl.handle.net/2429/7148"@en .