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Independent gradients of producer, consumer and microbial diversity in lake plankton Longmuir, Allyson A. 2006

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INDEPENDENT GRADIENTS OF PRODUCER, CONSUMER AND MICROBIAL DIVERSITY IN LAKE PLANKTON by  A L L Y S O N A. L O N G M U I R B . S c . Trent University, 2001  A T H E S I S S U B M I T T E D IN P A R T I A L F U L F I L L M E N T O F THE REQUIREMENTS FOR THE DEGREE OF  MASTER OF SCIENCE in THE FACTULTY OF GRADUATE STUDIES (Zoology)  T H E UNIVERSITY O F BRITISH C O L U M B I A April 2 0 0 6 © A l l y s o n A . Longmuir, 2 0 0 6  11  Abstract  Facilitation b e t w e e n trophic levels during food w e b a s s e m b l y c a n drive positive correlations in diversity b e t w e e n producers, c o n s u m e r s a n d d e c o m p o s e r s . H o w e v e r , the contribution of trophic interactions relative to local environmental factors in promoting s p e c i e s diversity are poorly understood with m a n y studies of food w e b a s s e m b l y only c o n s i d e r i n g two trophic levels. H e r e w e e x a m i n e correlations in diversity a m o n g z o o p l a n k t o n , phytoplankton a n d bacteria in the pelagic z o n e of 31 lakes in British Columbia.  W e s a m p l e d s p e c i e s diversity of z o o p l a n k t o n a n d phytoplankton through  morphological identification while bacterial genetic diversity w a s e s t i m a t e d by denatured gradient gel electrophoresis ( D G G E ) of 16s r D N A p o l y m o r p h i s m s . W e looked for correlations in diversity that were independent of the abiotic environment by statistically controlling for 18 limnological variables. N o strong correlation w a s found b e t w e e n the diversity of z o o p l a n k t o n , phytdplankton a n d bacteria. In addition, the p h y s i c a l factors that w e r e a s s o c i a t e d with s p e c i e s composition in o n e trophic level w e r e independent of those that were important for another. O u r results provide no support for the importance of direct f e e d b a c k s between p r o d u c e r s , c o n s u m e r s a n d d e c o m p o s e r s in maintaining diversity. Z o o p l a n k t o n , phytoplankton a n d bacterial c o m m u n i t i e s are structured independently from o n e another a n d r e s p o n d to different environmental v a r i a b l e s .  iii  Table of Contents Abstract  ii  T a b l e of C o n t e n t s  iii  List of T a b l e  iv  List of Figures  •  v  Acknowledgements  vi  Chapter 1  1  Chapter 2  G e n e r a l Introduction Biodiversity Patterns  1  Study System T h e s i s Objectives References  3 3 5  Independent gradients of producer, c o n s u m e r a n d microbial diversity in lake plankton Introduction Methods Results Discussion Conclusions References  Chapter 3 Appendix  General Conclusions  7 10 16 18 24 32 37 38  iv  List of Tables  T a b l e 1: R e s u l t s from multiple regression analysis for e a c h pelagic community. All variables left in the m o d e l s had a significance of < 0.10 following b a c k w a r d stepwise selection procedure  25  T a b l e 2: R e s u l t s for e a c h trophic level from the first two ordination a x e s of the C C A ordination  26  V  List of Figures  Figure 1: M a p of British C o l u m b i a with sites s a m p l e d  27  Figure 2: S p e c i e s richness relationships between z o o p l a n k t o n , phytoplankton a n d pelagic bacteria communities. Four of the s a m p l e s that are plotted for zooplankton a n d phytoplankton are m i s s i n g for bacteria s i n c e the D N A for those s a m p l e s would not s u c c e s s f u l l y amplify  28  Figure 3: B o x plot c o m p a r i n g the beta-diversity v a l u e s for z o o p l a n k t o n , phytoplankton a n d bacterial c o m m u n i t i e s . T h e v a l u e s for the phytoplankton community are significantly different than those for the z o o p l a n k t o n or bacterial communities  29  Figure 4 - Biplots of the first two C C A a x e s for the lake c o m m u n i t i e s . T h e biplots s h o w a s s o c i a t i o n s b e t w e e n the environmental gradients a n d the relative r i c h n e s s for e a c h c o m m u n i t y separately (A=zooplankton; B=phytoplankton; C=bacteria). Individual lakes are represented by the o p e n circles. A r r o w s represent correlations of the most important environmental v a r i a b l e s with the a x e s . Arrow length indicates the strength of a s s o c i a t i o n b e t w e e n the predictor variable a n d the s p e c i e s d a t a  30  Figure 5: Correlations of environmental loadings b e t w e e n c o m m u n i t i e s . point is the v a r i a n c e e x p l a i n e d by a particular environmental variable  31  Each  vi  Acknowledgements I would like to thank D a n u s i a Dolecki for her expertise in phytoplankton a n d zooplankton taxonomy; A n d r e a English for her efforts in field; and R o s s T h o m p s o n for his g u i d a n c e a n d innovation. T h e microbial work could not have b e e n c o m p l e t e d without the help of E m m a Hambly, J e s s i e C l a s e n a n d the r e s o u r c e s m a d e available by Curtis Suttle at U B C . A s well, e v e r y o n e at the U B C Department of F o r e s t S c i e n c e s G e n e t i c D a t a C e n t e r w a s extremely helpful with all things microbial. C o m m e n t s m a d e by J e s s i e C l a s e n , R u s s Markel, Sandra Nicol, John Richardson, Jordan Rosenfeld, Diane Srivastava, and S p e n c e r W o o d greatly improved the thesis.  In addition to all m e m b e r s of the S h u r i n lab, I would like to thank e v e r y o n e from the S r i v a s t a v a L a b (Katsky Venter, Brian S t a r z o m s k i , J a c k i e N g a i a n d B e n Gilbert) for being m u c h n e e d e d "lab mate stand-ins" during the early formative months of my thesis. A l e e z a G e r s t e i n and J e s s i c a Hill a l s o d e s e r v e my thanks a n d respect for supporting a n d understanding their often m o o d y office-mate. Finally, I would like to thank my a c a d e m i c advisor, J o n S h u r i n . O v e r the last two a n d a half y e a r s I h a v e not only a p p r e c i a t e d J o n ' s enthusiastic a n d creative a p p r o a c h to a d d r e s s i n g e c o l o g i c a l q u e s t i o n s but have a l s o b e e n grateful for his understanding a n d s e n s e of humor. I w i s h him great s u c c e s s in inspiring quiet a w e in all that follow.  1  Chapter 1: General Introduction Biodiversity Patterns  Patterns of diversity a n d the m e c h a n i s m s that c a u s e them are a n underlying t h e m e in ecology. S i n c e the diversity of s p e c i e s a n d community structure are fundamental features of e c o s y s t e m s , m a n y ecologists have f o c u s e d on both the g e n e r a l importance of diversity a n d how it is maintained in natural s y s t e m s . A d d r e s s i n g t h e s e questions of diversity h a s improved our understanding of the p a r a d o x d e s c r i b e d by G . E. Hutchinson (1961), w h e r e more s p e c i e s than e x p e c t e d are regularly found in habitats with relatively few limiting r e s o u r c e s .  In a n effort to determine the v a l u e of biodiversity, r e s e a r c h e r s h a v e t a k e n various viewpoints including those that c o n s i d e r e c o n o m i c , p h a r m a c e u t i c a l , a n d e c o s y s t e m function p a r a d i g m s (Lovejoy 1994). F r o m the perspective of c o m m u n i t y e c o l o g y s e v e r a l theories o n the importance of biodiversity h a v e b e e n d e v e l o p e d a n d d e b a t e d . E m e r s o n a n d K o l m (2005) a r g u e that a positive correlation exists b e t w e e n the number of s p e c i e s present a n d the rate at which speciation o c c u r s in a c o m m u n i t y implying the adaptive potential of a more diverse community. Quantifying biodiversity h a s a l s o resulted in d e b a t e s o n the relationship b e t w e e n e c o s y s t e m stability a n d diversity. If c o m m u n i t i e s are d o m i n a t e d by a great number of w e a k interactions, t h e s e will s e r y e to d a m p e n the effect of single strong interactions that m a y significantly disrupt the community. A d e c r e a s e in biodiversity m a y i n c r e a s e the a v e r a g e interaction strength ( M c C a n n 2000) a n d reduce community stability (Ives a n d H u g h e s 2001). A l t h o u g h more diverse c o m m u n i t i e s m a y be c o n s i d e r e d more stable, s o m e d e b a t e regarding the issue still remains (Worm a n d Duffy 2003). T h e relationship b e t w e e n biodiversity a n d s o m e form of e c o s y s t e m function (i.e. nutrient cycling, b i o m a s s or productivity) h a s recently b e e n extensively investigated a s a m e a n s to quantify the importance of biodiversity. T h e results of this body of work h a v e identified varying relationships b e t w e e n e c o s y s t e m functions, like productivity (Mittlebach et a l . 2001), a n d biodiversity.  2  W h e t h e r viewing biodiversity in the context of e c o s y s t e m function will benefit c o n s e r v a t i o n efforts remains questionable ( S r i v a s t a v a a n d V e l l a n d 2005).  In addition to the importance of biodiversity, the question of how diversity is maintained in natural s y s t e m s is u n r e s o l v e d . T h e body of work investigating the importance of biodiversity motivated m e to c o n s i d e r how the diversity of o n e group of o r g a n i s m s r e s p o n d s to the diversity of another group. During the d e v e l o p m e n t of e c o l o g y a s a scientific discipline, the problem of s p e c i e s diversity went from b e i n g a p p r o a c h e d a s a result of historical p r o c e s s e s to the o u t c o m e of e c o l o g i c a l interactions (Schluter a n d Ricklefs 1993). A l t h o u g h current a p p r o a c h e s to the problem often c o n s i d e r s o m e combination of both p r o c e s s e s (Shurih et a l . 2000), the relative importance of ecological interactions in determining community structure is difficult to determine.  Inter-specific  interactions, particularly competition, have b e e n p r o p o s e d a s a significant structuring force for most c o m m u n i t i e s (MacArthur 1972, D i a m o n d 1975). T h e availability of multiple r e s o u r c e s in a c o m m u n i t y w h e r e s p e c i e s are a l s o limited by p h y s i c a l factors introduces the potential for inter-specific tradeoffs b e t w e e n competitive abilities for a limiting r e s o u r c e a n d the range of optimal physical conditions (Levins 1979). T h i s spatial niche partitioning, a s well a s temporal heterogeneity in r e s o u r c e s a n d conditions, both serve a s m e c h a n i s m s by w h i c h diversity is maintained. C o n s i d e r i n g s p e c i e s c a n be constrained by both biotic a n d abiotic interactions, the f o c u s of C h a p t e r 2 is on the relative contribution of s p e c i e s interactions in explaining the diversity found in a natural s y s t e m . B y c o n s i d e r i n g a greater trophic complexity than s e e n in s i m p l e m o d e l s of only c o n s u m e r s a n d their r e s o u r c e s , additional constraints (i.e. limitation by predators) c a n be i m p o s e d o n a c o m m u n i t y of c o n s u m e r s . It s e e m s likely that s p e c i e s interactions c a n significantly promote diversity through both the pair-wise a s s o c i a t i o n s a s d e s c r i b e d in G r o v e r ' s (1993) a s s e m b l y rules a n d local p r o c e s s e s s u c h a s predation, competition a n d mutualism.  3  Study System  Plankton is a fundamental c o m p o n e n t of pelagic f o o d - w e b s . A s d e s c r i b e d by F o r b e s (1887) m a k i n g u s e of a lake a s a study s y s t e m provides the r e s e a r c h e r with a n understanding that they "...will thus be m a d e to s e e the impossibility of studying any form completely, out of relation to the other f o r m s . . . " C o m m u n i t y interactions in pelagic f o o d - w e b s are c o m p l e x a n d c a n be g o v e r n e d by m a n y e c o l o g i c a l f o r c e s including r e s o u r c e limitation, competition a n d predation (Carpenter 1988). T h e relatively small size of planktonic o r g a n i s m s a n d the e a s e of s a m p l i n g the diversity of c o n s u m e r , primary p r o d u c e r a n d d e c o m p o s e r trophic levels within lake habitats m a k e them an ideal s y s t e m for this study. F o c u s i n g my r e s e a r c h question o n what is c o n s i d e r e d the relatively h o m o g e n e o u s yet diverse p e l a g i c z o n e of l a k e s I c a n directly a d d r e s s the paradox of the plankton put forth by H u t c h i n s o n (1961). T h i s multi-trophic community of z o o p l a n k t o n , phytoplankton a n d p e l a g i c bacteria w a s s a m p l e d in 31 l a k e s in southwestern British C o l u m b i a . Figure 1 in C h a p t e r 2 illustrates the location of the study sites.  Thesis Objectives  T h e primary objective of m y study w a s to investigate w h e t h e r a positive relationship exists b e t w e e n the diversity of phytoplankton, z o o p l a n k t o n a n d pelagic bacteria. Finding a positive correlation w o u l d provide e v i d e n c e for direct diversity f e e d b a c k s a c r o s s trophic. It is a l s o p o s s i b l e that a positive correlation m a y result from similar r e s p o n s e s of e a c h trophic level to local environmental gradients. After e x a m i n i n g initial correlations, the diversity in e a c h trophic level w a s tested to determine if they are r e s p o n d i n g similarly to local environmental gradients. T h e diversity of adjacent trophic levels w a s then be a d d e d to the m o d e l a s predicting variables only after controlling for significant environmental variables. T h e g o a l of u s i n g this m e t h o d of a n a l y s i s w a s to determine the amount of variation in the diversity of o n e trophic level e x p l a i n e d by the diversity of adjacent trophic levels relative to local environmental gradients. T h e relationships b e t w e e n the diversity found in e a c h trophic level are e x a m i n e d in C h a p t e r 2.  4  S t u d i e s of diversity f e e d b a c k s most often o c c u r in experimental s y s t e m s with randomly derived diversity gradients. I c h o s e to investigate the question with natural diversity a n d environmental gradients. M y interest in the importance of diversity f e e d b a c k s a c r o s s trophic levels is directly linked to the relevance of this question in a c o m m u n i t y of naturally coexisting o r g a n i s m s a s o p p o s e d to o r g a n i s m s that c o u l d potentially coexist a s a result of belonging to the regional s p e c i e s pool.  5  References Carpenter, S . R . (ed.), 1988. C o m p l e x Interactions in L a k e C o m m m u n i t i e s . Springer V e r l a g . D i a m o n d , J . M . 1975. A s s e m b l y of s p e c i e s communities. In E c o l o g y a n d Evolution of C o m m u n i t i e s , e d . M.L. C o d y a n d J . M . D i a m o n d , 3 4 2 - 4 4 4 . C a m b r i d g e , M A , Harvard University P r e s s . E m e r s o n , B . C . a n d K o l m , N. 2 0 0 5 . S p e c i e s diversity c a n drive s p e c i a t i o n . Nature 434: 1015-1017. F o r b e s , S . A . 1887. T h e lake a s a m i c r o c o s m . Bulletin of the Scientific A s s o c i a t i o n (Peoria, IL), pp 7 7 - 8 7 . G r o v e r , J . P. 1994. A s s e m b l y rules for communities of nutrient-limited plants a n d specialist herbivores. A m e r i c a n Naturalist 143: 2 5 8 - 2 8 2 . Hutchinson G . E . 1 9 6 1 . T h e paradox of the plankton. A m e r i c a n Naturalist 95: 137-145. Ives, A . R . a n d J . B . H u g h e s . 2 0 0 1 . G e n e r a l relationships b e t w e e n s p e c i e s diversity a n d stability in competitive s y s t e m s . A m e r i c a n Naturalist 159: 3 8 8 - 3 9 5 . Levins, R. 1979. C o e x i s t e n c e in a variable environment. A m e r i c a n Naturalist 114: 7 6 5 783. Lovejoy, T . E . 1994. T h e quantification of biodiversity: A n e s o t e r i c q u e s t or a vital c o m p o n e n t of sustainable d e v e l o p m e n t ? P h i l o s o p h i c a l T r a n s a c t i o n s : Biological S c i e n c e s 345: 8 1 - 8 6 . MacArthur, R . H . 1972. G e o g r a p h i c a l ecology: Patterns in the distribution of s p e c i e s . N e w York, Harper a n d R o w . M c C a n n , K . S . 2 0 0 0 . T h e diversity-stability debate. Nature 405: 2 2 8 - 2 3 3 . Mittelbach, G . G . , Steiner, C . F . , S c h e i n e r , S . M . , G r o s s , K.L., R e y n o l d s , H.L., W a i d e , R . B . , Willig, M . R . , D o d s o n , S.I. & G o u g h , L. 2 0 0 1 . W h a t is the o b s e r v e d relationship between s p e c i e s richness a n d productivity? E c o l o g y 82: 2 3 8 1 - 2 3 9 6 . S h u r i n , J . B . , J . E . H a v e l , M . A . Leibold a n d B. Pinel-Alloul. 2 0 0 0 . L o c a l a n d regional z o o p l a n k t o n s p e c i e s r i c h n e s s : a s c a l e - i n d e p e n d e n t test for saturation. E c o l o g y 81: 3062-3073. S r i v a s t a v a , D . S . a n d M . V e l l e n d . 2 0 0 5 . B i o d i v e r s i t y - e c o s y s t e m function r e s e a r c h : Is it relevant to c o n s e r v a t i o n ? A n n u a l R e v i e w of E c o l o g y , Evolution a n d S y s t e m a t i c s 36: 267-94.  6  Schluter, D. a n d R . E . Ricklefs. 1993. S p e c i e s Diversity: A n introduction to the problem. P a g e s 1-10 in R . E . Ricklefs a n d D. Schluter, e d s . S p e c i e s diversity in e c o l o g i c a l c o m m u n i t i e s . University of C h i c a g o P r e s s , C h i c a g o . W o r m , B. a n d J . E . Duffy. 2 0 0 3 . Biodiversity, productivity a n d stability in real food w e b s . T r e n d s in E c o l o g y a n d Evolution 18: 6 2 8 - 6 3 2 .  7  Chapter 2: Independent gradients of producer, consumer and microbial diversity in lake plankton  Introduction  T h e question of how s p e c i e s coexist in e c o s y s t e m s is a persistent t h e m e in community ecology. G . E. H u t c h i n s o n (1959) first pointed out that G a u s e ' s (1934) a x i o m of competitive e x c l u s i o n is in apparent contradiction with the high diversity found in apparently h o m o g e n e o u s habitats s u c h a s the pelagic z o n e s of l a k e s a n d o c e a n s . H e termed this contrast the p a r a d o x of the plankton (Hutchinson 1961). N u m e r o u s solutions to the p a r a d o x have b e e n p r o p o s e d , mostly dealing with the w a y s in which natural s y s t e m s violate the a s s u m p t i o n s of simplified m o d e l s predicting competitive e x c l u s i o n . T i l m a n a n d P a c a l a (1993) s u m m a r i z e the alternative solutions to H u t c h i n s o n ' s paradox. T h e theories fall into s e v e r a l c a t e g o r i e s : (1) population limitation by multiple r e s o u r c e s or local physical factors; (2) temporal or spatial heterogeneity in r e s o u r c e s a n d l o c a l p h y s i c a l factors; (3) interspecific trade-offs b e t w e e n competitive a n d colonization abilities; (4) non-equilibrium population d y n a m i c s ; a n d (5) interactions b e t w e e n trophic levels. H e r e w e f o c u s o n the last category, the role of facilitation b e t w e e n o r g a n i s m s at different trophic levels a n d the reciprocal effects of diversity between producers, consumers and decomposers.  Facilitation of diversity through multi-trophic interactions c a n o c c u r w h e n a n u m b e r of conditions are met. First, predators m a y promote diversity a m o n g c o m p e t i n g prey (keystone predation, P a i n e 1966) w h e n their impact is greatest for dominant competitors thereby preventing competitive e x c l u s i o n (Leibold 1 9 9 6 ) . S e c o n d , a diverse r e s o u r c e b a s e c a n i n c r e a s e the potential for niche partitioning a n d c o e x i s t e n c e a m o n g multiple c o n s u m e r s (Tilman 1988, S i e m a n n et a l . 1998, Interlandi a n d K i l h a m , 2000). A c c o r d i n g to t h e s e m e c h a n i s m s , the n u m b e r of potentially c o e x i s t i n g competitors is the s u m of the n u m b e r of limiting r e s o u r c e s a n d predators, provided that predators are differentiated in their prey preference. Third, positive f e e d b a c k s in diversity b e t w e e n c o n s u m e r s a n d prey d e p e n d o n sequential a s s e m b l y rules ( G r o v e r 1994).  8  That is, invasion of producers allows for colonization by s p e c i a l i z e d c o n s u m e r s , which promotes further i n v a s i o n by c o m p e t i n g p r o d u c e r s through k e y s t o n e predation. T h e ability of s p e c i e s to persist d e p e n d s o n the order in w h i c h they arrive in a community. A potentially unlimited n u m b e r of c o n s u m e r s a n d r e s o u r c e s c a n persist if e a c h colonizing prey is followed by a c o n s u m e r that w e a k e n s its effects on later competitors (Grover 1994). If t h e s e m e c h a n i s m s are important for maintaining diversity in nature, then w e expect to o b s e r v e correlations in diversity b e t w e e n c o n s u m e r s a n d their r e s o u r c e s .  Positive f e e d b a c k s in diversity m a y a l s o arise v i a facilitation b e t w e e n p r o d u c e r s a n d d e c o m p o s e r s ( R e y n o l d s et a l . 2 0 0 3 , V a n d e r Heijden et al.1998). D e c o m p o s e r t a x a m a y vary in their ability to mineralize organic c o m p o u n d s found in different plant s p e c i e s . P r o d u c e r s a n d m i c r o b e s m a y therefore b e joined in m u t u a l i s m s m e d i a t e d by nutrient recycling. A diverse d e c o m p o s e r community c a n i n c r e a s e the rate of nutrient c y c l i n g v i a the variable ability of different m i c r o b e s to mineralize different o r g a n i c c o m p o u n d s , therefore high producer diversity m a y d e p e n d o n high d e c o m p o s e r diversity ( N a e e m et a l . 2 0 0 0 ) . T h e r e v e r s e m a y a l s o b e important, w h e r e high producer diversity provides more opportunity for niche specialization a m o n g d e c o m p o s e r s . V a n der Heijden et a l . (1998) o b s e r v e d positive f e e d b a c k s b e t w e e n d e c o m p o s e r a n d primary producer diversity in m i c r o c o s m s simulating E u r o p e a n g r a s s l a n d s . Mycorrhizal fungi diversity p r o m o t e d the m a i n t e n a n c e of plant diversity. M i c r o b e s m a y a l s o act a s p a t h o g e n s or c o n s u m e r s of plants a n d thereby drive negative f e e d b a c k s that maintain diversity a m o n g p r o d u c e r s v i a the k e y s t o n e predation m e c h a n i s m ( B e v e r 1994). Interactions b e t w e e n plants a n d soil m i c r o b e s thereby s h o w both positive (via microbially m e d i a t e d r e s o u r c e partitioning) a n d negative (via soil b o r n e plant pathogens) f e e d b a c k s that c a n influence the m a i n t e n a n c e of l a r g e - s c a l e temporal a n d spatial gradients of s p e c i e s r i c h n e s s (reviewed by R e y n o l d s et a l . 2 0 0 3 ) . A l t h o u g h f e e d b a c k s in diversity a c r o s s trophic levels are a plausible m e c h a n i s m for s p e c i e s c o e x i s t e n c e , the importance of s u c h f e e d b a c k s relative to other drivers s u c h a s abiotic control is poorly understood in most e c o s y s t e m s .  9  If trophic level interactions are a n important m e c h a n i s m for promoting s p e c i e s c o e x i s t e n c e then diversity s h o u l d be positively correlated a c r o s s trophic levels. That is, high diversity of producers s h o u l d c o i n c i d e with high diversity a m o n g c o n s u m e r s a n d d e c o m p o s e r s . S i n c e positive f e e d b a c k s arise through sequential a s s e m b l y , diversity m a y vary a m o n g sites with different colonization histories. M o s t studies of diversity patterns a c r o s s trophic levels c o m e from terrestrial s y s t e m s a n d largely f o c u s on primary producer a n d herbivore interactions (Murdoch et a l . 1 9 7 2 , S i e m a n n et a l . 1998, H a d d a d et a l . 2 0 0 1 , H a w k i n s a n d Porter 2003). T e s t s for correlations in diversity a c r o s s trophic levels have recently b e e n performed in aquatic s y s t e m s . Irigoien et a l . (2004) found no correlation b e t w e e n diversity or richness of marine z o o p l a n k t o n a n d phytoplankton. A l l e n et a l . (1999) e x a m i n e d the richness of benthic macroinvertebrates, riparian birds, s e d i m e n t a r y d i a t o m s , fish, planktonic c r u s t a c e a n s a n d planktonic rotifers in a survey of 186 eastern North A m e r i c a n lakes a n d found that most r i c h n e s s correlations w e r e w e a k l y positive. D e c l e r c k et a l . (2005), p e r f o r m e d a similar survey of bacteria, ciliates, phytoplankton, z o o p l a n k t o n , fish, macro-invertebrates a n d water plants in 9 8 E u r o p e a n lakes, a n d a l s o found w e a k correlations in r i c h n e s s a c r o s s trophic levels. C o n v e r s e l y , S h u r i n a n d A l l e n (2001) found positive correlations in s p e c i e s richness of phytoplankton, z o o p l a n k t o n a n d fishes that w e r e independent of m e a s u r e d environmental variables in 5 0 A d i r o n d a c k L a k e s . C o n s e q u e n t l y , empirical correlations in diversity a c r o s s trophic levels have provided m i x e d support for the importance of f e e d b a c k s in maintaining diversity.  W e m e a s u r e d the diversity of phytoplankton, z o o p l a n k t o n a n d p e l a g i c bacteria in 31 lakes in south-western British C o l u m b i a to test for correlations in diversity. T h e lakes represented a broad range of environmental variables (e.g. productivity, salinity, pH) but were similar in s i z e (within the s a m e order of magnitude). P h y t o p l a n k t o n a n d z o o p l a n k t o n c o m p o s i t i o n a n d diversity were m e a s u r e d by m o r p h o l o g i c a l identification while bacterial diversity w a s determined by amplification of 16s r D N A followed by denaturing gel gradient electrophoresis ( D G G E ) .  10  If positive f e e d b a c k s b e t w e e n trophic levels maintain diversity in t h e s e c o m m u n i t i e s then w e e x p e c t to find positive correlations in diversity b e t w e e n trophic levels. H o w e v e r , s u c h a s s o c i a t i o n s m a y a l s o arise d u e to correlated r e s p o n s e s of different t a x a to s h a r e d environmental gradients. T h a t is, if the s a m e limiting abiotic factors influence different trophic levels, then lakes with similar physical conditions m a y contain similar n u m b e r s of s p e c i e s . T o control for variation in abiotic conditions, w e m e a s u r e d a suite of limnological variables in e a c h lake. In this w a y w e w e r e a b l e to test for correlations in diversity a m o n g trophic levels that were independent of environmental gradients. W e looked for correlations in diversity after accounting for variation that c o u l d be explained by m e a s u r e d abiotic v a r i a b l e s . S u c h correlations imply a direct effect of diversity in o n e trophic level o n that of another. Alternatively, the a b s e n c e of s u c h correlations s u g g e s t s that f e e d b a c k s through facilitation b e t w e e n trophic levels d o not play a detectable role in maintaining diversity.  Finally, w e c o m p a r e d patterns of beta-diversity (regional/local r i c h n e s s , a m e a s u r e of local distinctiveness) a c r o s s trophic levels. Finlay (2002) p r o p o s e d that microo r g a n i s m s are m o r e c o s m o p o l i t a n than m e t a z o a n s a s a result of rampant d i s p e r s a l , high population s i z e s a n d a s e x u a l reproduction. W e a s k e d w h e t h e r phytoplankton a n d bacteria c o m m u n i t i e s s h o w s m a l l e r differences in c o m p o s i t i o n a m o n g l a k e s than zooplankton.  Methods  Study  Region  W e s a m p l e d 31 l a k e s throughout a n a r e a of approximately 3 0 , 0 0 0 k m in the southern 2  interior a n d the mainland c o a s t of south-western British C o l u m b i a (Figure 1). T h e lakes r a n g e d in s u r f a c e a r e a from 2 0 to 3 9 5 hectares. L a k e s w e r e s e l e c t e d to represent the full range of local environmental conditions to produce b r o a d diversity gradients in the o r g a n i s m s s a m p l e d . E a c h lake w a s s a m p l e d o n o n e o c c a s i o n during the.day b e t w e e n late M a y a n d early S e p t e m b e r , 2 0 0 4 . At e a c h site w e m e a s u r e d p h y s i c a l (dissolved  11  o x y g e n , p H , conductivity, temperature, light, S e c c h i depth), c h e m i c a l (chlorophyll-a, total p h o s p h o r u s , total nitrogen, total o r g a n i c c a r b o n , a n d d i s s o l v e d o r g a n i c carbon), morphometric (elevation, latitude, longitude, surface a r e a , m a x i m u m depth), a n d biological (zooplankton, phytoplankton a n d pelagic bacteria) v a r i a b l e s . S e e A p p e n d i x for a list of lakes with c o r r e s p o n d i n g variables.  Physical  and chemical  variables  A depth profile w a s e s t a b l i s h e d for temperature, d i s s o l v e d o x y g e n , p H , conductivity a n d light ( P A R ) m e a s u r e d at o n e meter intervals from just b e l o w the s u r f a c e to the metalimnion. Vertical light attenuation for e a c h lake w a s d e t e r m i n e d a s the s l o p e of l o g irradiance (p,mol) v s . depth (m" ). W a t e r s a m p l e s w e r e collected at o n e meter 1  e  intervals from the s u b - s u r f a c e to the metalimnion using a tube s a m p l e r (3.5 c m diameter). S a m p l e s w e r e p o o l e d a c r o s s depths in the field a n d s u b - s a m p l e d for total organic c a r b o n ( T O C ) , d i s s o l v e d organic c a r b o n ( D O C ) , total p h o s p h o r u s (TP), total nitrogen (TN) a n d chlorophyll-a a n a l y s e s . T O C a n d D O C (filtered through W h a t m a n G F / F filters) s a m p l e s w e r e collected in dark, a c i d w a s h e d g l a s s jars a n d immediately stored on ice. T P a n d T N s a m p l e s w e r e collected in acid w a s h e d N a l g e n e bottles a n d frozen immediately after collection. C h l o r o p h y l l - a s a m p l e s w e r e c o l l e c t e d by filtering lake water through W h a t m a n G F / F filters, which were then w r a p p e d in foil a n d frozen for later a n a l y s i s , w h i c h o c c u r r e d within fourteen d a y s . Both T P a n d chlorophyll-a concentrations w e r e determined using standard limnological m e t h o d s ( W e t z e l a n d Likens 1991). T O C a n d T N concentrations were determined directly from liquid s a m p l e s u s i n g a S h i m a d z u T O C - V C S H a n a l y z e r (Kyoto, J a p a n ) with a detection limit 4 n g C L' . T h e D O C (mg C L" ) s a m p l e s w e r e a n a l y z e d using a D o h r m a n n P h o e n i x 8 0 0 0 1  1  U V - P e r s u l f a t e a n a l y z e r with a detection limit of 0.1 m g C L" . 1  Plankton  community  richness  Phytoplankton a n d z o o p l a n k t o n richness w e r e determined using morphological identification while bacterial richness w a s determined with m o l e c u l a r m e t h o d s . Phytoplankton w e r e c o l l e c t e d by p u m p i n g water s a m p l e s , a p p r o x i m a t e l y o n e liter per depth interval, through tubing lowered at o n e meter intervals through the photic z o n e .  12  S a m p l e s w e r e p o o l e d a c r o s s depths a n d thoroughly m i x e d . A 5 0 0 ml s u b - s a m p l e w a s then collected a n d immediately fixed in Lugol's iodine solution. Phytoplankton were identified to g e n u s or s p e c i e s under a n inverted m i c r o s c o p e at 100x, 2 0 0 x or 4 0 0 x magnification (depending on s a m p l e density) after settling s a m p l e s in 2 5 m l counting c h a m b e r s for approximately 2 4 hours.  In most c a s e s b e t w e e n 2 0 0 a n d 5 0 0 individual  cells were c o u n t e d . Z o o p l a n k t o n were collected by vertically hauling a plankton net (30cm diameter o p e n i n g , 1m long, 5 4 u m Nitex mesh) through the water c o l u m n to the surface from 1 m a b o v e the lake bottom. T h e c o n c e n t r a t e d s a m p l e w a s fixed in Lugol's solution. C r u s t a c e a n s a n d rotifers were identified a n d e n u m e r a t e d under a 6 0 x stereom i c r o s c o p e . A l l individuals w e r e c o u n t e d if the s a m p l e c o n t a i n e d f e w e r than approximately 2 5 0 a n i m a l s . W h e n more individuals w e r e e n c o u n t e r e d , s u b - s a m p l e s w e r e taken with a F o l s o m plankton splitter ( V a n G u e l p e n et a l . , 1982). Z o o p l a n k t o n t a x o n o m i c resolution w a s to the g e n u s or s p e c i e s level. Phytoplankton c o m m u n i t i e s w e r e s a m p l e d from the epilimnion w h e r e a s z o o p l a n k t o n w e r e c o l l e c t e d from the w h o l e water c o l u m n . M a n y z o o p l a n k t o n s h o w p r o n o u n c e d daily vertical migrations (Neill 1992), therefore s p e c i e s found at depth during the d a y m a y h a v e o c c u p i e d the epilimnion at night. O u r goal w a s to characterize the z o o p l a n k t o n , phytoplankton a n d bacterial c o m m u n i t i e s that coexist on a time s c a l e of d a y s . T h e bacterial c o m m u n i t y w a s s a m p l e d by lowering a length of weighted tubing, rinsed s e v e r a l times with site water, to the thermocline until o n e liter w a s collected. T h i s water w a s then filtered through a 0.42jj,m p o r e - s i z e d nitrocellulose filter to r e m o v e larger particles. Bacterial cells were collected on a 0.2|im p o r e - s i z e d nitrocellulose filter, w h i c h w a s immediately frozen in the field.  DNA  isolation  Bacterial D N A w a s obtained with a n extraction kit ( M o B i o Ultra C l e a n S o i l D N A Kit # 12800-50) a n d the resulting D N A w a s u s e d a s templates for the p o l y m e r a s e chain reaction ( P C R ) . T h e 16s r D N A from e a c h community w a s amplified with previously d e s c r i b e d primers ( M u y z e r et a l . 1993) d e s i g n e d to be specific to most bacteria. Four of the 31 bacterial s a m p l e s did not s u c c e s s f u l l y amplify. T h e amplified product w a s 200 b a s e pairs in s i z e a n d for this r e a s o n the primers u s e d included a 4 0 b p G C - c l a m p . T h e  13  amplification w a s performed with a P T C - 1 0 0 P r o g r a m m a b l e T h e r m a l Controller ( M J R e s e a r c h , Inc., W a t e r d o w n , M A . ) a n d the following final v o l u m e s : 2 0.125  JLLI  of D N A template,  of e a c h primer, 2.5 jul of d e o x y r i b o n u c l e o s i d e triphosphate, 2.5 jxl of 10x P C R  buffer, a n d 2 units of T a q D N A p o l y m e r a s e ( A m p l i T a q , R o c h e M o l e c u l a r S y s t e m s Inc.) T h e P C R b e g a n by incubating the s a m p l e s for 7 min at 9 4 ° C to d e n a t u r e the template D N A . T h e temperature w a s s u b s e q u e n t l y lowered to a n a n n e a l i n g temperature of 58°C for 1 min. P r i m e r e x t e n s i o n w a s then performed at 7 2 ° C for 3 min. T h e reactions ran for a total of 3 0 c y c l e s . T h e p r e s e n c e of amplified products w a s confirmed by electrophoresis in 2 % (wt/vol) a g a r o s e gels stained in ethidium b r o m i d e a n d v i e w e d on a U V transilluminator.  DGGE T h e richness of e a c h bacterial community w a s determined by the n u m b e r of b a n d s resulting from denatured gradient gel electrophoresis ( D G G E ) . D G G E s e p a r a t e s the16s r D N A s e q u e n c e p o l y m o r p h s b a s e d on their t e n d e n c y to d i s s o c i a t e at different concentrations of denaturants. T h i s is a c o m m o n t e c h n i q u e for m a k i n g c o m p a r i s o n s b e t w e e n bacterial c o m m u n i t i e s from environmental s a m p l e s ( M u y z e r et a l . 1993, Bell et al. 2 0 0 5 , L y a u t e y et a l . 2 0 0 5 ) . D G G E w a s performed a s d e s c r i b e d by M u y z e r et a l . (1993) using the D - C o d e U n i v e r s a l Mutation Detection S y s t e m ( B i o R a d ) . S i n c e more than o n e gel w a s required to run all the s a m p l e s , a n e n v i r o n m e n t a l s a m p l e (one of the s a m p l e d lakes), with a broad e n o u g h b a n d pattern to e n c o m p a s s the c o m m u n i t i e s s a m p l e d , w a s u s e d a s a m a r k e r to s t a n d a r d i z e b a n d patterns b e t w e e n g e l s . T h e g e l s u s e d w e r e 8 % polyacrylamide with a denaturant gradient ranging from 2 0 % to 5 5 % ( 1 0 0 % denaturant being 7 M u r e a a n d 4 0 % d e i o n i z e d f o r m a m i d e ) . E l e c t r o p h o r e s i s w a s run at a constant voltage of 2 0 0 V for 3 hours at 60°C in a buffer of 1x T r i s - A c e t a t e E D T A ( T A E ) . After electrophoresis, the gels w e r e stained with 4/vl of 10,000x S Y B R G r e e n (Molecular P r o b e s , O r e g o n ) iri 5 0 0 m l of 1x T A E a n d v i s u a l i z e d by U V transillumination.  14  Bacteria  Richness  T a x o n o m i c r i c h n e s s of the bacterial c o m m u n i t i e s w a s e s t i m a t e d by the n u m b e r of b a n d s present in the D G G E , a n d the relative a b u n d a n c e of e a c h t a x o n o m i c unit w a s estimated by the relative intensity of e a c h b a n d . G e l C o m p a r II software (Applied M a t h s , A u s t i n , T X ) w a s u s e d to identify b a n d s a n d estimate their intensity. A n u m b e r of a s s u m p t i o n s are n e c e s s a r y w h e n using D G G E b a n d i n g patterns to estimate t a x a richness a n d a b u n d a n c e . T h e first is that e a c h b a n d represents o n e distinct s e q u e n c e p o l y m o r p h i s m in the r D N A . C a s e s m a y exist w h e r e a b a n d contains D N A from several taxa or a single t a x a contributes more than o n e b a n d ( S e k i g u c h i et a l . 2001). T h e s e i s s u e s m a y lead to errors w h e r e D G G E either over- or u n d e r - e s t i m a t e s the genetic richness of the bacterial community. T h e s e c o n d issue is that P C R b i a s m a y lead to differences in b a n d intensity d u e to variation in the t e n d e n c y of different s e q u e n c e s to amplify. B a n d intensity m a y therefore be a n imprecise reflection of the relative a b u n d a n c e of different groups. However, all the i s s u e s with using D G G E to estimate c o m m u n i t y diversity h a v e a n a l o g s in morphological indices (cryptic s p e c i e s , t a x o n o m i c uncertainty d u e to phenotypic plasticity, variable s a m p l i n g efficiency for different s p e c i e s ) . D G G E offers o n e consistent m e a s u r e of the genetic diversity of the bacterial community for c o m p a r i s o n with other groups with m a n y of the s a m e limitations a s other diversity metrics.  Richness  and diversity  metrics  T h e a s s o c i a t i o n b e t w e e n the richness of e a c h trophic level a n d the matrix of environmental variables w a s tested by multiple regression a n a l y s i s using S A S (Version 5.1, S A S Institute Inc., C a r y , N C ) . T h e K o l m o g o r o v - S m i r n o v test w a s u s e d to test variables for normality. V a r i a b l e s were transformed (log or s q u a r e root transformations) to minimize deviations from normality. T h e m o d e l s to predict richness w e r e constructed by first testing e a c h environmental variable for relationships with r i c h n e s s in simple r e g r e s s i o n m o d e l s including both the first a n d s e c o n d order terms to allow for the possibility of non-linear r e s p o n s e s . Environmental v a r i a b l e s that h a d P - v a l u e s less than 0.10 in individual m o d e l s w e r e then entered together into the multiple r e g r e s s i o n m o d e l . A b a c k w a r d selection p r o c e d u r e w a s u s e d to select the best m o d e l to explain s p e c i e s  15  richness in z o o p l a n k t o n , phytoplankton a n d bacterial c o m m u n i t i e s . T o test for correlations in diversity a c r o s s trophic levels that are i n d e p e n d e n t of environmental variability, r i c h n e s s of the two other guilds were entered after the s e l e c t i o n procedure h a d c h o s e n the best m o d e l b a s e d on environmental v a r i a b l e s .  Univariate a n a l y s e s w e r e u s e d to identify a s s o c i a t i o n s b e t w e e n s p e c i e s r i c h n e s s a n d environmental gradients, a n d correlations in richness a c r o s s trophic levels. W e u s e d multivariate gradient a n a l y s e s to test for a s s o c i a t i o n s b e t w e e n c o m m u n i t y composition a n d abiotic factors, a n d to a s k whether c o m p o s i t i o n of the three trophic levels r e s p o n d e d to similar abiotic factors. All multivariate a n a l y s e s w e r e performed with C A N O C O 4.5 (ter B r a a k 1 9 8 8 ) . Direct gradient a n a l y s e s w e r e u s e d to e x a m i n e the relationship b e t w e e n community matrices a n d transformed environmental variables. T o determine the most appropriate ordination method (unimodal or linear) a detrended c o r r e s p o n d e n c e a n a l y s i s w a s c o m p l e t e d for e a c h s p e c i e s - b y - l a k e matrix (zooplankton, phytoplankton a n d bacteria). T h e gradient length term m e a s u r e s the b e t a diversity in c o m m u n i t y c o m p o s i t i o n . A gradient length b e t w e e n 3.0 a n d 4 . 0 indicates that either linear or unimodal m e t h o d s are r e a s o n a b l e , while a gradient v a l u e greater than 4.0 indicates that a unimodal method is appropriate ( L e p s a n d S m i l a u e r 2 0 0 3 ) . F o r both z o o p l a n k t o n a n d phytoplankton the largest gradient length of the first four D C A a x e s w a s greater than 3.0, while the largest gradient for the bacteria matrix w a s greater than 6.0. W e therefore u s e d a u n i m o d a l ordination m e t h o d , C a n o n i c a l C o r r e s p o n d e n c e A n a l y s i s ( C C A ) , for all three groups. C C A is a n ordination a n a l y s i s that u s e s the variation in the environmental matrix to explain the variation in the biotic matrix. T h e m a n u a l selection a n d r a n d o m permutation (reduced m o d e l , 9 9 9 r a n d o m permutations; ter B r a a k a n d S m i l a u e r 1998) p r o c e d u r e s in C A N O C O w e r e u s e d to c h o o s e the most p a r s i m o n i o u s ordination for e a c h trophic group. A biplot of sites a n d environmental gradients w a s c r e a t e d to v i s u a l i z e the results from the C C A . T h e importance of e a c h environmental variable c a n b e inferred by c o m p a r i n g correlations b e t w e e n environmental variables a n d the s p e c i e s a x e s . T o avoid the destabilization that c a n o c c u r a s a result of strong correlations a m o n g environmental v a r i a b l e s w h e n using c a n o n i c a l coefficients, inter-set correlations are reported here ( S r i v a s t a v a 1995). T o  16  test whether trophic levels w e r e affected by similar abiotic factors, w e tested for correlations b e t w e e n the loadings of e a c h environmental variable o n the s p e c i e s data a c r o s s groups. A large loading indicates a strong a s s o c i a t i o n b e t w e e n the s p e c i e s a n d abiotic variable. If different trophic levels r e s p o n d to the s a m e limnological factors, then the loadings of predictor variables s h o u l d be positively correlated b e t w e e n z o o p l a n k t o n , phytoplankton a n d bacteria.  Results  T h e lakes are c h a r a c t e r i z e d by a broad range of local environmental conditions (Appendix). For e x a m p l e , lakes ranged in elevation from approximately 5 0 m to 1 4 5 0 m . L a k e trophic status ranged from oligotrophic to eutrophic a c c o r d i n g to the concentrations of total nitrogen (<0.001 - 3.7 m g L" ) a n d C h l o r o p h y l l - a (7.0 -1287.7 mg 1  L" ). Total organic c a r b o n concentrations ranged from 0.61 to 6 9 . 7 7 m g L" . G r a d i e n t s 1  1  for m e a n v a l u e s of p H (6.54 - 9.17) a n d conductivity (7.9 - 8 7 4 /vS cm" ) w e r e a l s o 1  broad.  A total of 4 0 c r u s t a c e a n a n d rotifer z o o p l a n k t o n s p e c i e s w e r e identified (richness range a c r o s s lakes = 6 - 2 1 ; m e d i a n = 13) with the c l a d o c e r a n Daphnia  pulex present in 2 4 of  the 31 lakes, often dominating the zooplankton community. A l g a l c o m m u n i t y richness totaled 156 t a x a with individual lake s a m p l e s containing 7 to 5 2 t a x a (median = 26). S m a l l flagellates d o m i n a t e d most communities. T h e range of bacterial t a x o n o m i c richness a c r o s s lakes w a s 7 to 2 3 (median = 14) a n d the total n u m b e r of b a n d s w a s 6 0 .  R i c h n e s s of z o o p l a n k t o n , phytoplankton a n d bacteria w e r e uncorrelated a m o n g lakes (Figure 2) although there w a s a w e a k positive a s s o c i a t i o n b e t w e e n z o o p l a n k t o n a n d phytoplankton richness (R =0.04, P = 0.273). A c o m p a r i s o n of beta-diversity 2  (regional/local) a c r o s s trophic levels is s h o w n in Figure 3. T h e phytoplankton c o m m u n i t i e s h a d the highest a v e r a g e beta-diversity, 7.21 ( S E = 0.66), followed by bacteria (4.65; S E = 0.31) a n d zooplankton (3.79; S E = 0.21) c o m m u n i t i e s .  17  Phytoplankton beta-diversity w a s significantly greater than either z o o p l a n k t o n or bacteria, but z o o p l a n k t o n a n d bacteria did not differ from e a c h other ( A N O V A of log transformed v a l u e s ,  Models predicting  F , 8 2  2  species  =22.07, P<0.001).  richness  Abiotic variables a c c o u n t e d for 2 9 - 4 8 % of the variation in bacterial, phytoplankton a n d z o o p l a n k t o n richness (Table 1). T h e variables that best predicted z o o p l a n k t o n richness included the first a n d s e c o n d order terms for elevation, D O a n d T O C ( R = 0 . 4 0 , P = 2  0.034). Phytoplankton richness w a s best predicted by the first a n d s e c o n d order term for S e c c h i depth ( R = 0 . 2 9 , P = 0.006). T h e multiple r e g r e s s i o n m o d e l for bacterial 2  richness w a s the only a b i o t i c - b a s e d model improved by a d d i n g the r i c h n e s s variables from the other two guilds. B a c t e r i a richness w a s best predicted by the s e c o n d order term for light extinction, a n d the first a n d s e c o n d order terms for D O a n d phytoplankton richness. (R =0.48, P = 0.013). After accounting for the environmental v a r i a b l e s , the 2  relationship b e t w e e n bacteria a n d phytoplankton r i c h n e s s w a s non-linear with a negative first order term a n d positive s e c o n d order term. Of all the important environmental v a r i a b l e s , D O w a s the only o n e c o m m o n to more than o n e trophic level. H o w e v e r , z o o p l a n k t o n a n d bacteria s h o w e d opposite correlations with D O : the relationship b e t w e e n D O a n d z o o p l a n k t o n richness w a s positive while that with bacterial richness w a s negative. S e c o n d order terms w e r e included in the significant predicting variables for e a c h m o d e l , s u g g e s t i n g that community r e s p o n s e s w e r e often non-linear.  Community  composition  R e l a t i o n s h i p s b e t w e e n the c o m p o s i t i o n of e a c h p e l a g i c c o m m u n i t y a n d the environmental variables w e r e explored using c a n o n i c a l c o r r e s p o n d e n c e a n a l y s i s ( C C A ) . T h e initial a n a l y s e s included all lakes. H o w e v e r , the relationship b e t w e e n c o m m u n i t y c o m p o s i t i o n a n d the environmental gradients in the resulting ordinations w e r e strongly influenced by C u l t u s L a k e , a-highly eutrophic lake (chlorophyll-a concentration of 1287 m g I' ) with a n algal c o m m u n i t y d o m i n a t e d by colonial a n d filamentous c y a n o b a c t e r i a . 1  T h e disproportionate effect of C u l t u s L a k e o b s c u r e d the relationships b e t w e e n the abiotic variables a n d the s p e c i e s matrix; therefore, it w a s r e m o v e d from the a n a l y s e s in  18  the results that follow. T h e biplot for z o o p l a n k t o n s h o w s a n apparent outlier at the top, centre of the ordination. T h e removal of this community ( G r e e n L a k e ) did not significantly c h a n g e the relationships s o it w a s left in the a n a l y s i s . T h e m a n u a l selection p r o c e d u r e w a s u s e d to find the m o s t important e n v i r o n m e n t a l v a r i a b l e s explaining c o m m u n i t y c o m p o s i t i o n . T h e ordination a x e s e x p l a i n e d a m o d e r a t e amount of variation for e a c h community. T h e total amount of variation e x p l a i n e d by the first four ordination a x e s for z o o p l a n k t o n , phytoplankton a n d bacteria c o m m u n i t i e s is 2 4 . 2 % , 2 8 . 6 % a n d 3 2 . 8 % respectively. T h e variables most strongly correlated with the first axis were temperature (r = -0.63) in the c a s e of z o o p l a n k t o n , elevation (r = -0.51) a n d temperature (r = 0.47) for phytoplankton a n d S e c c h i depth (r = -0.45) for bacteria.  T h e loadings of the 18 environmental variables were unrelated b e t w e e n trophic levels (all r-values <-0.143, P > 0 . 5 7 2 , Figure 5), therefore c o m p o s i t i o n in z o o p l a n k t o n , phytoplankton a n d bacteria r e s p o n d e d to independent environmental gradients. A l t h o u g h the strength of a s s o c i a t i o n b e t w e e n s p e c i e s a n d e n v i r o n m e n t a l gradients are not correlated a c r o s s trophic levels, s o m e variables e m e r g e d a s important for multiple groups. T e m p e r a t u r e s h o w e d a strong loading for all groups. C h l o r o p h y l l - a a l s o s h o w e d a strong loading for both zooplankton a n d phytoplankton c o m p o s i t i o n , while m a x i m u m lake depth s h o w s a strong loading for phytoplankton a n d bacteria (Figure 5).  Discussion  O u r survey of B C lakes found that the richness a n d c o m p o s i t i o n of z o o p l a n k t o n , phytoplankton a n d bacterial c o m m u n i t i e s are largely i n d e p e n d e n t of o n e another a n d r e s p o n d to different environmental variables. Correlations in diversity a c r o s s trophic levels c a n arise either through f e e d b a c k s involving c o n s u m e r s that prevent competitive e x c l u s i o n , niche differentiation of c o n s u m e r s to utilize different r e s o u r c e s , m u t u a l i s m s b e t w e e n p r o d u c e r s a n d d e c o m p o s e r s through nutrient recycling, or c o m m o n r e s p o n s e s to the s a m e environmental gradients. O u r results provide no e v i d e n c e for a n y of t h e s e m e c h a n i s m s in the m a i n t e n a n c e of s p e c i e s r i c h n e s s . Instead, the patterns indicate that independent p r o c e s s e s control the r i c h n e s s of z o o p l a n k t o n , phytoplankton a n d bacteria. T h e  19  environmental gradients that w e r e a s s o c i a t e d with s p e c i e s r i c h n e s s w e r e different for e a c h trophic level. T h e only exception w a s d i s s o l v e d o x y g e n , w h i c h w a s positively correlated with z o o p l a n k t o n r i c h n e s s a n d negatively with bacterial r i c h n e s s . T h e limnological variables a s s o c i a t e d with community c o m p o s i t i o n a l s o s h o w e d no c o n s i s t e n c i e s a c r o s s the three guilds (Figure 3). T h e s e patterns s u g g e s t that diversity a c c u m u l a t e s independently in different parts of lake food w e b s , a n d that s p e c i e s diversity at o n e trophic level h a s little direct effect o n diversity at other trophic levels.  Trophic complexity h a s b e e n s u g g e s t e d a s a potential solution to the p a r a d o x of s p e c i e s c o e x i s t e n c e (Hutchinson 1 9 6 1 , T i l m a n a n d P a c a l a 1993). P r e v i o u s studies have found support for m e c h a n i s m s of inter-trophic facilitation of s p e c i e s diversity. Multiple r e s o u r c e s m a y support diverse c o n s u m e r s through n i c h e differentiation (Tilman 1988), a n d diverse c o n s u m e r s m a y promote prey c o e x i s t e n c e by preventing competitive e x c l u s i o n ( G r o v e r 1994, L e i b o l d 1996, Hillebrand a n d S h u r i n 2 0 0 5 ) . Interlandi a n d Kilham (2000) found that diversity of lake phytoplankton w a s c l o s e l y a s s o c i a t e d with the e v e n n e s s of two abiotic r e s o u r c e s (light a n d mineral nutrients). T h e contrast with our results m a y arise b e c a u s e resource diversity for heterotrophs ( m e s o z o o p l a n k t o n a n d bacteria) is m o r e difficult to quantify than that for primary p r o d u c e r s . Mineral nutrients a n d light are likely to represent e s s e n t i a l r e s o u r c e s for phytoplankton. H o w e v e r , different phytoplankton t a x a m a y be a substitutable r e s o u r c e for z o o p l a n k t o n that " p a c k a g e " nutrients in different ratios (Rothhaupt 2000). A s a result, heterotroph diversity m a y be l e s s c l o s e l y tied to autotroph diversity than are autotrophs a n d abiotic resources.  O u r results s u g g e s t that patterns of autotroph a n d heterotroph diversity m a y be consistently stronger in terrestrial rather than aquatic e c o s y s t e m s . H a d d a d et al. (2001) a n d S i e m a n n et a l . (1998) found positive correlations b e t w e e n s p e c i e s r i c h n e s s of terrestrial plants a n d insects in experimental g r a s s l a n d s . H a w k i n s a n d Porter (2003) found positive correlations b e t w e e n butterfly a n d plant diversity in s u r v e y s a c r o s s California, although the relationship d i s a p p e a r e d after a c c o u n t i n g for variation d u e to productivity a n d topography gradients. Their study s u g g e s t e d that correlations in  20  diversity a c r o s s trophic levels w e r e driven by a correlated r e s p o n s e to the environment rather than direct c a u s a l links. Positive f e e d b a c k s h a v e a l s o b e e n found b e t w e e n the diversity of soil m i c r o b e s a n d plant diversity in g r a s s l a n d m i c r o c o s m s ( V a n der Heijden et a l . 1998). O u r results a g r e e with the w e a k or a b s e n t r i c h n e s s correlations found in s e v e r a l other aquatic s y s t e m s (Irigoien et a l . 2 0 0 4 , D e c l e r c k et a l . 2 0 0 5 , A l l e n et al. 1999, but s e e S h u r i n a n d A l l e n 2001). T h i s general contrast in r i c h n e s s patterns b e t w e e n terrestrial a n d aquatic s y s t e m s implies that the m e c h a n i s m s of a s s e m b l y a n d community structure operate differently in the two s y s t e m s .  S e v e r a l p o s s i b l e explanations exist for the contrasting results b e t w e e n terrestrial a n d aquatic e c o s y s t e m s . First, there is a lack of s p e c i a l i z e d c o n s u m e r s in aquatic environments (Irigoien et a l . 2 0 0 4 , D e c l e r c k et a l . 2 0 0 5 , S t r o n g 1992). M a n y aquatic herbivores are filter f e e d e r s a n d therefore m a y lack the strong a s s o c i a t i o n s that terrestrial plants a n d herbivores h a v e a s a c o n s e q u e n c e of s p e c i a l i z e d diets or structural complexity. S e c o n d , D e c l e r c k et a l . (2005) s u g g e s t s that differences of s c a l e m a y explain the resulting i n c o n s i s t e n c i e s between aquatic a n d terrestrial s y s t e m s . M a n y experimental terrestrial studies are c o m p l e t e d o n relatively s m a l l local s c a l e s rather than regional or global s c a l e s . H o w e v e r , it is interesting to note that the large spatial s c a l e of H a w k i n s a n d Porter's (2003) study didn't o b s c u r e the initial strong positive correlations of California butterfly a n d plant diversity.  O u r results provide no indication for a direct or consistent effect of c o n s u m e r diversity on producer c o e x i s t e n c e . T h i s result d o e s not imply that c o n s u m e r s h a v e no impact o n the diversity of their prey; rather that c o n s u m e r s a n d primary p r o d u c e r s in lakes are not linked in tight pair-wise a s s o c i a t i o n s a s e n v i s i o n e d by G r o v e r (1994). A n u m b e r of other studies h a v e found strong predator effects on prey diversity that range from positive to negative ( C h a s e et al. 2002). F o r e x a m p l e , S h u r i n (2001) found that fish a n d insect predators r e d u c e d z o o p l a n k t o n diversity in isolated p o n d c o m m u n i t i e s but i n c r e a s e d it w h e n immigration from the regional pool w a s a l l o w e d . Z o o p l a n k t o n predators c a n a l s o h a v e indirect effects on phytoplankton composition by modifying nutrient cycling (Vanni a n d Findlay 1990). Proulx a n d M a z u m d e r (1998) u s e d m e t a - a n a l y s i s to s h o w that  21  predators tend to reduce prey diversity at low productivity a n d i n c r e a s e it in eutrophic s y s t e m s . Similarly, W o r m et a l . (2002) found that the effects of c o n s u m e r s o n m a c r o a l g a e diversity in rocky s h o r e c o m m u n i t i e s shifted from negative to positive a s productivity i n c r e a s e d . O u r results s u g g e s t that although particular predators m a y h a v e major effects on prey c o e x i s t e n c e , the number of predator t a x a per se d o e s not consistently e n h a n c e or r e d u c e prey diversity.  O u r results a l s o s u g g e s t that genetic diversity of the bacterial c o m m u n i t y r e s p o n d s to different gradients in the p h y s i c a l environment than either z o o p l a n k t o n or phytoplankton richness. T h i s contrasts with the c o n c l u s i o n s of H o r n e r - D e v i n e et a l . (2003) that patterns of bacterial diversity a c r o s s environmental gradients " m a y be qualitatively similar to t h o s e o b s e r v e d for plants a n d a n i m a l s . " T h e r e w e r e a l s o differences between the abiotic v a r i a b l e s important to bacterial diversity in our study c o m p a r e d with other studies. W e found that light attenuation a n d D O w e r e the best abiotic predictors of bacterial richness (Table 1).  R e c h e et a l . (2005) found that lake a r e a w a s related to  bacterial r i c h n e s s ( m e a s u r e d by the n u m b e r of D G G E b a n d s ) , although our l a k e s c o v e r e d a s m a l l e r s i z e range. Broughton a n d G r o s s (2000) d i s c o v e r e d a positive correlation b e t w e e n bacterial community c o m p o s i t i o n a n d primary productivity.  Our  results s h o w productivity, m e a s u r e d a s T P , a s o n e of the v a r i a b l e s d e s c r i b i n g variation in the bacterial community. H o w e v e r , a significant relationship b e t w e e n productivity a n d bacterial diversity d o e s not a p p e a r to c h a r a c t e r i z e all aquatic b a c t e r i a c o m m u n i t i e s s i n c e the relationship is variable a m o n g different bacterial l i n e a g e s (Horner-Devine et al. 2003).  D i s c r e p a n c i e s b e t w e e n our study a n d other bacterial diversity relationships m a y arise for s e v e r a l r e a s o n s . First, different m e t h o d s of D N A - b a s e d c o m m u n i t y fingerprinting ( A R I S A , T - R F L P , D G G E ) are c o m m o n l y u s e d to determine bacterial diversity. M e t h o d specific b i a s m a y contribute to contrasting results. S e c o n d , m e t h o d s like D G G E that c o n s i d e r all t a x a present (i.e. do not discriminate b e t w e e n active a n d dormant taxa) m a y not accurately represent the functionally active community. H o w e v e r , the s a m e is true for morphological diversity metrics. Finally, genetic diversity in prokaryotes m a y be  22  unrelated to s p e c i e s diversity. S p e c i e s diversity a n d genetic diversity are often controlled by the s a m e p r o c e s s e s (i.e. drift, immigration, r e s p o n s e to habitat heterogeneity) a n d s h o w positive correlations in nature (Vellend 2 0 0 5 ) . O u r m e a s u r e of bacterial diversity m a y therefore reflect indices b a s e d on m o r p h o l o g i c a l or functional a s p e c t s of the microbial community.  W e found that different limnological variables w e r e a s s o c i a t e d with r i c h n e s s in phytoplankton, z o o p l a n k t o n a n d bacteria. D O , T O C a n d elevation best predicted z o o p l a n k t o n r i c h n e s s , while s e c c h i depth w a s m o s t important for phytoplankton richness a n d light, D O a n d phytoplankton richness for bacteria. In contrast, previous studies h a v e found p H to b e a n important controlling factor of z o o p l a n k t o n ( Y a n et a l . 1996; Arnott et a l . 2 0 0 1 ; S h u r i n et al. 2000) phytoplankton (Arnott et a l . 2001) a n d bacterial r i c h n e s s (Fierer a n d J a c k s o n 2006). L a k e a r e a w a s not a strong predictor of local richness in contrast to s e v e r a l previous studies ( D o d s o n 1 9 9 2 ; A l l e n et a l . 1999). T h i s m a y b e e x p l a i n e d by the s m a l l e r r a n g e in s u r f a c e a r e a r e p r e s e n t e d by our data. Although z o o p l a n k t o n richness i n c r e a s e d with T O C , m e a s u r e s of productivity in general w e r e not strong predictors of either z o o p l a n k t o n or phytoplankton r i c h n e s s . T h e a s s o c i a t i o n s b e t w e e n most of the independent variables a n d the r i c h n e s s of e a c h guild were significant with the inclusion of the quadratic for the i n d e p e n d e n t variable, w h i c h gives a n indication to the importance of nonlinear r e s p o n s e s of t a x a r i c h n e s s to environmental gradients. S i m i l a r r e s p o n s e s to gradients of primary productivity ( D o d s o n et a l . 2000) a n d total p h o s p h o r u s (Declerck et al.2005) h a v e b e e n found for various g r o u p s of aquatic o r g a n i s m s . A l t h o u g h w e s a m p l e d a relatively b r o a d productivity gradient, our results differ with productivity patterns c o m m o n in aquatic s y s t e m s (Mittelbach et a l . 2 0 0 1 ; D e c l e r c k et a l . 2005). T h i s s u g g e s t s that aquatic c o m m u n i t i e s c a n be strongly controlled by a h e t e r o g e n e o u s collection of environmental gradients a s o p p o s e d to a single productivity gradient.  Z o o p l a n k t o n or phytoplankton s p e c i e s richness m o d e l s w e r e not significantly i m p r o v e d by including r i c h n e s s from the other two trophic levels. B y contrast, b a c t e r i a richness w a s negatively related to phytoplankton richness after a c c o u n t i n g for variation d u e to  23  light a n d D O . T h e m o d e l for bacteria richness s h o w e d a n i m p r o v e m e n t (from R = 0 . 4 0 2  to R = 0 . 4 8 , P=0.013) by including z o o p l a n k t o n a n d phytoplankton r i c h n e s s in the 2  selection p r o c e s s with phytoplankton remaining a s a significant predicting variable in the final m o d e l . T h i s result contrasts other findings in aquatic studies w h e r e no richness a s s o c i a t i o n s were found b e t w e e n t h e s e two trophic levels ( D e c l e r c k et a l . 2004). T h e s l o p e of the phytoplankton-bacteria relationship is negative ( z = -1.164) a n d the relationship is relatively w e a k a s calculated by the semi-partial correlation coefficient using the partial s u m of s q u a r e s (r= 0.232). A l t h o u g h this is not a particularly strong interaction, the negative relationship implies that a m e c h a n i s m other than facilitative nutrient cycling m a y be important. F o r e x a m p l e , heterotrophic or mixotrophic bacteria c a n c o m p e t e with phytoplankton for d i s s o l v e d mineral nutrients (Rothaupt a n d G u d e 1992). O u r d a t a doesn't provide insight into the proportion of autotrophic to heterotrophic t a x a in the bacterial community, but this competitive m e c h a n i s m m a y be playing a significant role.  O u r survey found significantly higher beta diversity in phytoplankton than in zooplankton or bacteria. T h i s pattern contrasts with other studies, w h i c h h a v e found lower spatial turnover in m i c r o - o r g a n i s m s than in m e t a z o a n s ( H o r n e r - D e v i n e et al. 2 0 0 4 , G r e e n et a l . 2004). Finlay (2002) s u g g e s t e d that,microbes are c o s m o p o l i t a n a n d s h o w lower beta diversity than m a c r o - o r g a n i s m s b e c a u s e high levels of d i s p e r s a l a m o n g habitats h o m o g e n i z e their c o m m u n i t i e s . Both G r e e n et al. (2004) a n d H o r n e r - D e v i n e et a l . (2004) found lower beta-diversity a n d shallower s p e c i e s - a r e a c u r v e s in m i c r o - o r g a n i s m s (prokaryotic a n d eukaryotic) than multicellular o r g a n i s m s . A l t h o u g h bacterial betadiversity in our d a t a w a s lower than that of phytoplankton, it w a s not different from z o o p l a n k t o n beta-diversity (Figure 3). This implies that freshwater bacteria a n d z o o p l a n k t o n s h a r e a similar d e g r e e of d i s p e r s a l limitation. Alternatively, the 1 6 S subregion of the g e n o m e m a y be highly c o n s e r v e d , leading to relatively low diversity at the site w e e x a m i n e d .  24  Conclusions U n d e r s t a n d i n g the control of diversity in natural s y s t e m s is c o m p l i c a t e d by the range of potential p r o c e s s e s a n d interactions that m a y affect c o e x i s t e n c e . T h e lack of strong richness a s s o c i a t i o n s a c r o s s trophic levels d o e s not n e c e s s a r i l y m e a n that trophic-level interactions are unimportant a s agents of diversity. T h e results s u g g e s t that although trophic interactions m a y play a significant role in maintaining diversity, tight pair-wise a s s o c i a t i o n s b e t w e e n c o n s u m e r s , producers a n d d e c o m p o s e r s d o not drive positive f e e d b a c k s in community a s s e m b l y . T h e specialist herbivores a s s u m e d by G r o v e r ' s (1994) c o m m u n i t y a s s e m b l y rules m a y be a b s e n t from p e l a g i c c o m m u n i t i e s . Rather, a few strongly interacting g r a z e r s , p r o d u c e r s a n d d e c o m p o s e r s m a y play dominant roles in driving diversity patterns. Other solutions to the p a r a d o x of the plankton (spatial or temporal heterogeneity, non-equilibrium dynamics) m a y explain the high diversity o b s e r v e d in the p e l a g i c z o n e s of lakes.  25  T a b l e 1 - R e s u l t s from multiple regression a n a l y s i s for e a c h p e l a g i c community. All variables left in the m o d e l s had a significance of < 0.10 following b a c k w a r d s t e p w i s e selection procedure. Parameter value  Partial R  F  P  elevation elevation DO DO TOC TOC  -1.021 0.016 5.876 -0.391 19.274 -4.928  0.136 0.093 0.087 0.084 0.142 0.124  5.63 3.81 3.62 3.47 5.89 5.13  0.026 0.062 0.069 0.074 0.023 0.032  Secchi Secchi  77.998 -19.736  0.255 0.277  10.78 11.74  0.003 0.002  light DO DO Phyto. richness Phyto. richness  3.380 -5.832 0.369 -1.164  0.247 0.171 0.131  9.94 6.89 5.27  0.005 0.016 0.032  0.232  9.31  0.006  0.197  7.93  0.010  Source  Zooplankton richness R =0.3982 2  2  2  2  Phytoplankton richness R =0.2915  2  2  2  2  Bacteria richness R =0.4775 2  2  0.020 2  26  T a b l e 2 - R e s u l t s for e a c h trophic level from the first two ordination a x e s of the C C A ordination.  Axis 1 Eigenvalue  Axis 2  Variation explained  Eigenvalue  Variation explained  Zooplankton  0.408  10.90%  0.250  6.70%  Phytoplankton  0.375  12.10%  0.224  7.20%  Bacteria  0.354  9.90%  0.256  7.10%  ure 1 - M a p of British C o l u m b i a with sites s a m p l e d .  28  22 CO CO  -r  CD CZ  SZ o  Ian  c o Q. O  o N  •  A  20 -  •  18 16 -  •  u 12 -  •  10 86• 4 • 0  ••  ••  •  • • •  mm  •  10  • 20  • • •  •  ••  • •  •  •  •  • •  •  50  30  60  Phytoplankton richness CO CO  c  50  -r  CD  sz o  40 -  i _ £Z  o c  30 -  20 -  CCS  Q. O  10 -  sz CL  o -I  (  10  12  14  16  18  20  22  24  22  24  Bacteria richnesss  22 -p CO CO  20 -  CD £Z  SI o  Ian  c o o No  18 16 14 12 10 864 -10  12  14  16  18  20  Bacteria richness Figure 2 - S p e c i e s richness relationships between z o o p l a n k t o n , phytoplankton a n d pelagic bacteria c o m m u n i t i e s .  29  Zooplankton  Phytoplankton  Bacteria  Figure 3 - B o x plot c o m p a r i n g the beta-diversity v a l u e s for z o o p l a n k t o n , phytoplankton a n d bacterial c o m m u n i t i e s . T h e v a l u e s for the phytoplankton c o m m u n i t y are significantly different than those for the zooplankton or bacterial c o m m u n i t i e s .  30  AXIS 1 (eigenvalue = 0.408)  AXIS 1 (eigenvalue = 0.375)  A X I S 1 (eigenvalue = 0.354)  Figure 4 - Biplots of the first two C C A a x e s for the lake c o m m u n i t i e s . T h e biplots s h o w a s s o c i a t i o n s b e t w e e n the environmental gradients a n d the relative r i c h n e s s for.each community separately (A=zooplankton; B=phytoplankton; C=bacteria). Individual lakes are represented by the o p e n circles. A r r o w s represent correlations of the most important environmental variables with the a x e s . A r r o w length indicates the strength of a s s o c i a t i o n b e t w e e n the predictor variable a n d the s p e c i e s d a t a .  0.22  o c _co  •  A  •  CL 0.12  o  0.10  SZ Q_  0.08  Temperature  •  0.14  ••  •  0.06  •  0.04 0.05  31  Chla.  • • 0.15  0.10  •  • •• • 0.20  0.25  0.30  0.28  B  0.26 0.24 CO  0.20 CD 0.18 o CO 0.16  fJQ  M a x depth • •  •  0.22  •  •  • •  Temperature •  0.14  •  0.12  •  • •  •  •  • • • 0.08 0.04 0.06 0.08 0.10 0.12 0.14 0.16 0.18 0.20 0.22 0.10  0.28  Phytoplankton -I  0.26 • 0.24 CO 0.22 0.20 CD 0.18 o CO 0.16 CO 0.14  Temperature  • • • -  0.12 0.10 • 0.08 i.05  0.10  0.15  0.20  0.25  0.30  Zooplankton  Figure 5 - Correlations of environmental loadings b e t w e e n c o m m u n i t i e s . E a c h point is the v a r i a n c e e x p l a i n e d by a particular environmental variable. V a r i a b l e s with large loadings in two trophic levels are labeled.  32  References A l l e n , A . P., T. R. Whittier, P. R. K a u f m a n n , D. P. L a r s e n , R. J . O ' c o n n o r , R. M . H u g h e s , R. S . S t e m b e r g e r , S . S . Dixit, R. O . Brinkhurst, A . T. Herlihy, a n d S . G . P a u l s e n . 1999. C o n c o r d a n c e of t a x o n o m i c richness patterns a c r o s s multiple a s s e m b l a g e s in l a k e s of the northeastern United S t a t e s . C a n a d i a n J o u r n a l of F i s h e r i e s a n d A q u a t i c S c i e n c e s 56: 7 3 9 - 7 4 7 . Arnott, S . E., J . J . M a g n u s o n , a n d N. D. Y a n . 1998. C r u s t a c e a n z o o p l a n k t o n s p e c i e s richness: single- a n d multiple year estimates. C a n a d i a n J o u r n a l of F i s h e r i e s a n d A q u a t i c S c i e n c e s 55: 1 5 7 3 - 1 5 8 2 . Arnott, S . E., N. D. Y a n , W . Keller and K. Nicholls. 2 0 0 1 . T h e influence of droughti n d u c e d acidification o n the recovery of plankton in S w a n L a k e ( C a n a d a ) . E c o l o g i c a l Applications 11: 7 4 7 - 7 6 3 . B e l l , T., J . A . N e w m a n , I.P. T h o m p s o n , A . K . Lilley a n d C . J . v a n d e r G a s t . 2 0 0 5 . B a c t e r i a a n d island biogeography - R e s p o n s e . S c i e n c e 309: 1 9 9 8 - 1 9 9 9 B e v e r , J . D. 1994. F e e d b a c k b e t w e e n plants a n d their soil c o m m u n i t i e s in a n old field community. E c o l o g y 75: 1 9 6 5 - 1 9 7 7 . Broughton, L. C . a n d K. L. G r o s s . 2 0 0 0 . Patterns of diversity in plant a n d soil microbial communities a l o n g a productivity gradient in a M i c h i g a n old-field. O e c o l o g i a 125: 4 2 0 427. C h a s e , J . M . , P . A . A b r a m s , J . P . G r o v e r , S ! Diehl, P. C h e s s o n , R . D . Holt, S . A . R i c h a r d s , R . M . Nisbet a n d T . J . C a s e . 2 0 0 2 . T h e interaction b e t w e e n predation a n d competition: a review a n d synthesis. E c o l o g y Letters 5: 3 0 2 - 3 1 5 . Declerck, S . , J V a n d e k e r k h o v e , K. Muylaert, J . M . C o n d e - P o r c u n a , K. V a n Der G u c h t , C . P e r e z - Martinez, T. L a u r i d s e n , K. S c h w e n k , G . Zwart, W . R o m m e n s , J . L o p e z R a m o s , E. J e p p e s e n , W . V y v e r m a n , L. B r e n d o n c k a n d L. D e M e e s t e r . 2 0 0 5 . Multigroup biodiversity in shallow lakes along gradients of p h o s p h o r u s a n d water plant cover. E c o l o g y 86: 1 9 0 5 - 1 9 1 5 . D o d s o n , S . I. 1992. Predicting c r u s t a c e a n zooplankton s p e c i e s r i c h n e s s . Limnology and O c e a n o g r a p h y 37: 8 4 8 - 8 5 6 . D o d s o n , S . , S . E . Arnott a n d K.L. C o t t i n g h a m . 2 0 0 0 . T h e relationship in lake c o m m u n i t i e s between primary productivity a n d s p e c i e s r i c h n e s s . E c o l o g y 81: 2 6 6 2 2679. Fierer, N. a n d R . B . J a c k s o n . 2 0 0 6 . T h e diversity a n d b i o g e o g r a p h y of soil bacterial communities. P N A S 103: 6 2 6 - 6 3 1 .  33  Finlay, B . J . 2 0 0 2 . G l o b a l d i s p e r s a l of free-living microbial eukaryote s p e c i e s . S c i e n c e 296: 1 0 6 1 - 1 0 6 3 . G a u s e , G . F . 1934. T h e struggle for e x i s t e n c e . W i l l i a m s a n d W i l k e n s , Baltimore, M d . G r e e n , J . L . , A . J . H o l m e s , M . W e s t o b y , I. Oliver, D. B r i s c o e , M . Dangerfield, M . Gillings a n d A . J . Beattie. 2 0 0 4 . Spatial scaling of microbial eukaryote diversity. Nature 432: 747-750. G r o v e r , J . P. 1994. A s s e m b l y rules for communities of nutrient-limited plants a n d specialist herbivores. A m e r i c a n Naturalist 143: 2 5 8 - 2 8 2 . H a d d a d , N. M . , D. T i l m a n , J . H a a r s t a d , a n d J . M . H. K n o p s . 2 0 0 1 . C o n t r a s t i n g effects of plant richness a n d composition o n insect c o m m u n i t i e s : a field experiment. A m e r i c a n Naturalist 158: 1 7 - 3 5 . S H a w k i n s , B.A.. a n d E . E . Porter 2 0 0 3 . D o e s herbivore diversity d e p e n d o n plant diversity? T h e c a s e of C a l i f o r n i a butterflies. A m e r i c a n Naturalist 161: 4 0 - 4 9 . Hillebrand, H. & S h u r i n , J . B. 2 0 0 5 Biodiversity a n d aquatic food w e b s . In Aquatic food webs: an ecosystem approach (ed. A . B e l g r a n o , U . M . S c h a r l e r , J . D u n n e & R. E . U l a n o w i c z ) , pp. 184-197. Oxford, U K : Oxford University P r e s s . H o r n e r - D e v i n e , M . C , M . A . L e i b o l d V . H S m i t h a n d B. J . M . B o h a n n a n . 2 0 0 3 . Bacterial diversity patterns along a gradient of primary productivity. E c o l o g y Letters 6: 613-622. Horner-Devine, M.C., M. Lage, J . B . Hughes and B . J . M . Bohannan. 2004. A t a x a - a r e a relationship for bacteria. Nature 432: 7 5 0 - 7 5 0 . Hutchinson G . E . 1959. H o m a g e to S a n t a R o s a l i a or why are there s o m a n y kinds of a n i m a l s ? A m e r i c a n Naturalist 93: 145-159. Hutchinson G . E . 1 9 6 1 . T h e paradox of the plankton. A m e r i c a n Naturalist 95: 137-145. Interlandi, S . J . a n d S . S . K i l h a m . 2 0 0 0 . Limiting r e s o u r c e s a n d the regulations of diversity in phytoplankton c o m m u n i t i e s . E c o l o g y 82: 1270 - 1 2 8 2 . Irigoien, X . , J . H u i s m a n a n d R . P . Harris. 2 0 0 4 . G l o b a l biodiversity patterns of marine phytoplankton a n d z o o p l a n k t o n . Nature 429: 8 6 3 - 8 6 7 . Leibold, M . A . 1996. A graphical model of keystone predators in food w e b s : trophic regulation of a b u n d a n c e , i n c i d e n c e , and diversity patterns in c o m m u n i t i e s . A m e r i c a n Naturalist 147: 7 8 4 - 8 1 2 . L e p s , J . a n d P. S m i l a u e r . 2 0 0 3 . Multivariate a n a l y s i s of e c o l o g i c a l d a t a using C A N O C O . C a m b r i d g e University P r e s s , C a m b r i d g e , U K .  34  Mittelbach, G . G . , C . F. Steiner, S . M . S c h e i n e r , K. L. G r o s s , H. L. R e y n o l d s , R. B. W a i d e , M . R. Willig, S . I. D o d s o n , and L. G o u g h . 2 0 0 1 . W h a t is the o b s e r v e d relationship b e t w e e n s p e c i e s richness a n d productivity? E c o l o g y 82: 2 3 8 1 - 2 3 9 6 . M u r d o c h , W . W . , F. C . E v a n s , a n d C . H. P e t e r s o n . 1972. Diversity a n d pattern in plants a n d insects. E c o l o g y 53: 8 1 9 - 8 2 9 . M u y z e r , G . , E . C . D e W a a l a n d A . G . Uitterlinden. 1 9 9 3 . Profiling of c o m p l e x microbial populations by denaturing gradient gel electrophoresis a n a l y s i s of p o l y m e r a s e chain reaction-amplified g e n e s c o d i n g for 16s r R N A . A p p l . E n v i r o n . Microbiol. 59:695-700. N a e e m , S . , D. H a h n , and G . S c h u u r m a n . 2 0 0 0 . P r o d u c e r - d e c o m p o s e r c o d e p e n d e n c y modulates biodiversity effects. Nature 403: 7 6 2 - 7 6 4 . Neill, W . E . 1992. Population variation in the ontogeny of predator-induced vertical migration of c o p e p o d s . Nature 356: 5 4 - 5 7 . P a i n e , R. T. 1966. F o o d w e b complexity a n d s p e c i e s diversity. A m e r i c a n Naturalist 100: 65-75. Proulx, M . a n d A . M a z u m d e r . 1998. R e v e r s a l of grazing impact on plant s p e c i e s richness in nutrient-poor v s . nutrient-rich e c o s y s t e m s . E c o l o g y 79: 2 5 8 1 - 2 5 9 2 . R e c h e , I., E. P u l i d o - V i l l e n a , R. M o r a l e s - B a q u e r o , a n d E . O . C a s a m a y o r . 2 0 0 5 . D o e s e c o s y s t e m s i z e determine aquatic bacterial r i c h n e s s ? E c o l o g y 86: 1 7 1 5 - 1 7 2 2 . R e y n o l d s , H. L , A l i s s a P a c k e r , J a m e s D. B e v e r , a n d Keith C l a y . 2 0 0 3 . G r a s s r o o t s ecology: Plant-microbe-soil interactions a s drivers of plant c o m m u n i t y structure a n d d y n a m i c s . E c o l o g y 84: 2 2 8 1 - 2 2 9 1 . Rothhaupt, K . O . 2 0 0 0 . Plankton population d y n a m i c s : food w e b interactions a n d abiotic constraints. F r e s h w a t e r B i o l o g y 45: 105-109 Rothaupt, K . O . a n d H. G u d e . 1992. T h e influence of spatial a n d temporal concentration gradients on p h o s p h a t e partitioning b e t w e e n different s i z e fractions of plankton: further e v i d e n c e a n d p o s s i b l e c a u s e s . Limnology a n d O c e a n o g r a p h y 37: 7 3 9 - 7 4 9 . S e k i g u c h i , H., N. T o m i o k a , T. N a k a h a r a , a n d H. U h i y a m a . 2 0 0 1 . A single b a n d d o e s not a l w a y s represent single bacterial strains in denaturing gradient gel electrophoresis a n a l y s i s . B i o t e c h n o l o g y Letters 23: 1 2 0 5 - 1 2 0 8 . S h u r i n , J . B . , J . E . H a v e l , M.A. Leibold a n d B. Pinel-Alloul. 2 0 0 0 . L o c a l a n d regional z o o p l a n k t o n s p e c i e s richness: A s c a l e - i n d e p e n d e n t test for saturation. E c o l o g y 81: 3 0 6 2 - 3 0 7 3 .  35  S h u r i n , J . B. 2 0 0 1 . Interactive effects of predation a n d d i s p e r s a l o n z o o p l a n k t o n c o m m u n i t i e s . E c o l o g y 82: 3 4 0 4 - 3 4 1 6 . S h u r i n J . B. a n d E. G . A l l e n 2 0 0 1 . Effects of competition, predation, a n d d i s p e r s a l on s p e c i e s richness at local a n d regional s c a l e s . A m e r i c a n Naturalist 158: 6 2 4 - 6 3 7 S i e m a n n E., D. T i l m a n , J . H a a r s t a d , a n d M . Ritchie. 1998. E x p e r i m e n t a l tests of the d e p e n d e n c e of arthropod diversity on plant diversity. A m e r i c a n Naturalist 152: 7 3 8 - 7 5 0 . S r i v a s t a v a , D. S . 1995. A q u a t i c vegetation of N o v a S c o t i a n l a k e s differing in acidity a n d trophic status. A q u a t i c B o t a n y 51: 181 -196. Strong, D. R. 1992 A r e trophic c a s c a d e s all wet? Differentiation a n d donor control in s p e c i o s e e c o s y s t e m s . E c o l o g y 73: 7 4 7 - 7 5 4 . ter B r a a k , C . J . F. 1988. C A N O C O - a n e x t e n s i o n of D E C O R A N A to a n a l y z e s p e c i e s environment relationships. Vegetatio 75: 159-160. ter B r a a k , C . J . F., a n d P. S m i l a u e r . 1998. C A N O C O reference m a n u a l a n d u s e r ' s guide to C A N O C O for W i n d o w s : software for c a n o n i c a l c o m m u n i t y ordination, version 4. M i c r o c o m p u t e r P o w e r , Ithaca, N e w York, U S A . T i l m a n , D. 1988 Plant strategies a n d the d y n a m i c s a n d structure of plant c o m m u n i t i e s . M o n o g r a p h s in population biology. Princeton, N J : Princeton University P r e s s . T i l m a n , D., a n d S . P a c a l a . 1993. T h e m a i n t e n a n c e of s p e c i e s richness in plant c o m m u n i t i e s . P a g e s 1 3 - 2 5 in R. Ricklefs a n d D. Schluter, e d s . S p e c i e s diversity in e c o l o g i c a l c o m m u n i t i e s . University of C h i c a g o P r e s s , C h i c a g o . V a n d e r Heijden, M . G . A . , K l i r o n o m o s , J . D . , Ursic, M . , Moutoglis, P., Streitwolf-Engel, R., Boiler, T., W i e m k e n , A . a n d I.R. S a n d e r s . 1998. Mycorrhizal fungal diversity determines plant biodiversity, e c o s y s t e m variability a n d productivity. Nature 396: 6 9 - 7 2 . V a n G u e l p e n , L , D . F . markle, & D . J . D u g g a n . 1982. A n evaluation of a c c u r a c y , precision, a n d s p e e d of s e v e r a l z o o p l a n k t o n s u b s a m p l i n g t e c h n i q u e s . J o u r n a l du C o n s e i l International pour I'Exploration de la M e r 40: 2 2 6 - 2 3 6 V a n n i , M . J . a n d D.L. Findlay. 1990. T r o p h i c c a s c a d e s a n d phytoplankton community Structure. E c o l o g y 71: 9 2 1 - 9 3 7 . V e l l e n d , M . 2 0 0 5 . S p e c i e s diversity a n d genetic diversity: parallel p r o c e s s e s . A m e r i c a n Naturalist 166: 1 9 9 - 2 1 5 . Wetzel, R . G . a n d L.E. Likens. 1991. Limnological analyses. Springer-Verlag, N e w York, Inc.  36  W o r m , B., H.K. L o t z e , H. Hillebrand a n d U. S o m m e r . 2 0 0 2 . C o n s u m e r v e r s u s resource control of s p e c i e s diversity a n d e c o s y s t e m functioning. Nature 4 1 7 : 8 4 8 - 8 5 1 . Y a n , N.D., Keller, W . , S o m e r s , K . M . , P a w s o n , T . W . , a n d G i r a r d , R . E . 1996. R e c o v e r y of c r u s t a c e a n z o o p l a n k t o n c o m m u n i t i e s fromacid a n d metal contamination: c o m p a r i n g manipulated a n d reference l a k e s . C a n a d i a n J o u r n a l of F i s h e r i e s a n d A q u a t i c S c i e n c e 53: 1 3 0 1 - 1 3 2 7 .  37  Chapter 3: General Conclusions and Summary T h e primary goal of this study w a s to look for e v i d e n c e of diversity f e e d b a c k s a c r o s s trophic levels through positive correlations between z o o p l a n k t o n , phytoplankton a n d pelagic bacteria in British C o l u m b i a n lakes. T h e s e c o n d g o a l w a s to determine the r e s p o n s e of e a c h trophic level to environmental gradients a n d reveal a n y similarities in r e s p o n s e s to environmental gradients. Finally, the last g o a l w a s to determine if diversity could explain a n y of the remaining variation after controlling for significant environmental v a r i a b l e s .  Correlations b e t w e e n the diversity of e a c h trophic level did not provide a n y e v i d e n c e for direct f e e d b a c k s b e t w e e n t h e s e guilds. T h e lack of strong positive relationships implies not only that tight pair-wise interactions b e t w e e n s p e c i e s (i.e. p r o d u c e r a n d c o n s u m e r ) do not dominate this community, but a l s o that t h e s e o r g a n i s m s do not s h a r e a c o m m o n , significant r e s p o n s e to a n y environmental gradient. T h e environmental loadings from the ordination a n a l y s e s a l s o support the i d e a that e a c h guild r e s p o n d s differently to local environmental gradients. H o w e v e r , temperature did h a v e a relatively high loading for e a c h trophic level.  A s with m a n y q u e s t i o n s in ecology, the m a i n t e n a n c e of diversity is a p r o b l e m to which no single m e c h a n i s m c a n provide a completely satisfactory a n s w e r . A s d i s c u s s e d in C h a p t e r 2, experimental e v i d e n c e leads us to expect that s p e c i e s interactions a c r o s s trophic levels play a significant role in influencing the diversity f o u n d in natural s y s t e m s . M y d a t a d o e s not imply strong, direct interactions are playing a significant role in structuring the diversity in t h e s e communities. It is likely, however, diversity is driven by m a n y w e a k interactions d i s p e r s e d throughout t h e s e c o m m u n i t i e s in addition to local environmental factors. T e a s i n g out the most relevant a n s w e r s to e c o l o g i c a l problems in the uncontrolled environment of natural s y s t e m s is difficult. H o w e v e r , furthering our k n o w l e d g e of the importance of diversity a n d the m e c h a n i s m s that maintain diversity s h o u l d incorporate d a t a from both experimental manipulations a n d o b s e r v a t i o n s of naturally coexisting c o m m u n i t i e s .  38  Appendix  Maximum d e p t h (m)  Chlorophyla (ug/L)  Secchi depth (m)  mean pH  120o 20.100'  17  20.3  4.25  8.04  49o 40.961'  120o 36.252'  19  61.89  9  8.45  615  50o 06.584'  122o 58.747'  13.7  27.8  8  7.36  395  602  50o 33.653'  122o 40.381'  33  18.57  2.7  7.12  30  1002  49o 52.179'  120o 34.095'  16  30.87  7.2  6.75  119o 29.649'  10.4  44.88  4  7.52  78:3  2.5  8.87  Lake  Area (ha)  Elavation (m)  Allan  129.8  Allyson  Latitude  Longitude  1245  51° 13.800'  71  879  Alta  100  Birkenhead  Bluey  Bolean  78  1450  50o 31.905'  Courtney  74  1009  50o 00.377'  120o 36.390'  10 •  35  823  50o 51.479'  121o 03.379'  4  1287.67  1.5  9.17  Deadman  49  862  51o 07.516'  120o 52.738'  23  205.88  2.2  7.58  490 Dry  35  825  38.668'  120o 36.724'  12  27.19  8  8.45  Glimpse  95  1175  50o 14.794'  120o 17.344'  15.5  148.86  4.5  8.38  Green  205  633  50o 09.703'  119o 55.568'  38  7.03  1  7.17  Hammer  68  1255  50o 14.656'  120o 42.430'  9.5  35.33  4  7.66  Harper  28  368  50o 44.383'  119o 42.753'  22  27.36  6  7.97  Hathume  134  1418  49o 59.273'  120o 02.591'  9  177.03  3  8.05  490 Kawkawa  80  50  23.241'  121o 24.264'  15  61.89  5.5  8.43  Cultus  .  39  Murray  35  1115  49o 48.113'  121o 00.303'  17.7  75.92  6  8.14  Phope  116  1100  50o 18.026'  120o 19.019'  20  122.44  5.5  8.61  Pillar  38  880  50o 35.371'  1190 38.045'  14  33.47  6  8.17  Plateau  38  1220  50o 19.390'  120o 15.335'  12.3  142.17  4.5  8.5  Pressy  60  1029  51 o 22.693'  121o 01.832'  26.9  67.44  3.5  8.57  Salmon  115  926  500 16.242'  119o 59.976'  10.3  53  3.5  8.18  Salsbury  78  388  49o 22.123'  122o 13.507'  17.5  79.43  4.75  6.54  Scott  34  1239  51 o 14.765'  120o 45.612'  13  65.86  3  7.54  Silver  40  338  49o 18.997'  121o 24.801'  12.5  36.39  7.8  7.51  Snohoosh  83  832  510 05.598'  120o 05.598'  23.5  48.29  T u c el nuit  20  293  49o 11.637'  119o 32.24V  8  129.33  3  8.33  Vidette  36  827  510 9.666'  120o 53.768'  26  260.56  4.5  8.25  490 Weaver  81  249  20.808'  1210 52.129'  31  26.11  6.5  7.43  Windy  37  1425  59.404'  119o 55.335'  7.5  98.86  3.8  7.41  Yellow  35  750  49o 20.087'  119o 45.998'  35  96.38  1.5  8.75  490  7.84  40  light attenuation (/ymol)  DOC (mg/L)  TP  ifjS)  mean DO (mg/L)  TOC (mg/L)  TN (mg/L)  11.5  108  6.1  2.27  8.70  0.45  9.36  0.17  Allyson  16.9  268  6.48  6.22  0.01  6.26  0.00  Alta  20.7  114  7.7  3.23  2.40  0.01  1.72  0.00  Birkenhead  16.9  28  9.1  1.99  1.20  0.07  0.63  0.00  Bluey  18.6  342  8.2  4.14  4.09  0.04  7.45  0.18  Bolean  13.9  46  4  1.71  3.68  0.20  10.02  0.00  Courtney  20.2  874  6.24  2.25  16.06  0.16  21.67  1.56  Cultus  18.4  620  9.2  1.08  4.57  1.56  69.77  3.66  Deadman  12  83  5.9  1.06  11.27  0.14  14.34  0.08  Dry  16.8  289  5.29  2.19  2.79  5.34  0.00  Glimpse  16  251  7.4  2.36  5.11  0.21  13.54  0.47  Green  13.7  47  8.6  0.94  1.01  0.13  3.36  0.00  Hammer  17.5  17.5  4.4  1.53  0.09  14.34  0.67  Harper  15.8  201  5.6  2.13  11.97  0.08  14.06  0.30  Hathume  15.1  75  5.1  1.3  7.79  0.26  15.44  0.54  Kawkawa  18.5  101  10.9  3.54  3.03  2.16  0.00  Murray  16.2  75  7.7  3.33  0.08  4.69  0.04  mean temperature (°C)  mean Conductivity  Allan  Lake  ,.  41  Phbpe  16.8  285  8.2  3.26  6.29  0.25  14.37  0.54  Pillar  16.4  145  6.8  2.44  7.05  0.09  8.84  0.15  Plateau  16.5  238  8.3  2.46  14.01  0.08  15.81  0.63  Pressy  11.3  535  3.4  0.97  19.30  23.44  1.52  Salmon  16.8  133  5.6  1.27  12.18  1.43  14.41  1.19  Salsbury  14.4  7.9  8.8  1.65  4.77  0.00  4.55  0.03  Scott  13.7  90.2  3.9  1.08  Silver  12.7  36.2  7.1  2.44  3.42  0.11  0.61  0.00  Snohoosh  13.3  97.9  6  1.29  10.51  0.08  23.41  0.41  T u c el nuit  24.4  349  6.7  1.85  4.94  0.10  7.94  0.40  Vidette  12.3  319  6.9  2.31  6.91  0.05  10.86  0.20  Weaver  17.5  33  9.6  4.24  1.71  0.05  18.30  0.24  Windy  14.2  17.5  1.27  8.30  0.14  9.22  0.18  Yellow  17.8  397  1.89  10.21  0.10  V  7.7  0.26  

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