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Evolutionary biology of Siphonostomatoida (Copepoda) parasitic on vertebrates Benz, George William 1993

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EVOLUTIONARY BIOLOGY OF SIPHONOSTOMATOIDA (COPEPODA)PARASITIC ON VERTEBRATESbyGEORGE WILLIAM BENZB.Sc., The University of ConnecticutM.Sc., The University of ConnecticutA THESIS SUBMITtED IN PARTIAL FULFILLMENT OF THEREQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHYinThE FACULTY OF GRADUATE STUDIES(Department of Zoology)We accept this thesis as conformingto the required standardTHE UNIVERSITY OF BRITISH COLUMBIAJuly 1993Copyright by George William Benz, 1993In 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, CanadaDate OC4Z€,C 25 (dI93DE-6 (2/88)11AbstractA phylogeny for the 18 families of Siphonostomatoida (Copepoda) parasitic onvertebrates is presented which considers these taxa a monophyletic group evolved fromsiphonostome associates of invertebrates. Discussion of the evolutionary biology ofthese families is presented using this phylogeny as a foundation for comparison.Siphonostomes typically attach at specific locations on their hosts. Although copepodmorphology can sometimes be used to explain realized niches, most copepoddistributions remain mysteriously confined. Distribution data suggest that the branchialchambers were the first regions of the vertebrate body to be colonized, and that theolfactory capsules of vertebrates may have been derived from some premandibularbranchial component which caused an evolutionary split in the copepod fauna infectingthe branchial chambers of noseless and jawless vertebrates. The general body surfaces ofvertebrates were probably colonized by taxa infecting the gills and olfactory capsules,and perhaps was facilitated by a new type larva possessing a frontal filament. Adults ofthese larvae appear to have developed two modes of extending this progress inattachment security throughout adulthood. One mode involved new methods ofpermanent attachment of mature females, while the second mode allowed both powerfulswimming and efficient suctoral attachment.Reduction in the number of molts required to reach adulthood is exhibited by somelineages, and seems to have been realized through amalgamation of free living naupliusand/or parasitic copepodid stages. The first copepodid serves as the initial infective stagethroughout all lineages.While most siphonostome taxa are monoxenous, at least some pennellids areheteroxenous. Evolution of two host life cycles perhaps was facilitated by a highlymobile young adult capable of infecting another host, and by the close ecologicalassociation of the intermediate and definitive hosts.Although not widespread, mesoparasitism has apparently evolved several times amongsiphonostome taxa infecting vertebrates. Phylogenetic data illustrate that once a lineagebecomes mesoparasitic, reversal to ectoparasitism is uncommon.Two siphonostome lineages have successfully invaded fresh water. This significantecological shift appears to have been facilitated by a number of morphological,developmental, and ecological traits.Preliminary studies suggest that siphonostomes have sometimes coevolved with theirvertebrate hosts while at other times they have colonized phylogenetically distant butecologically similar hosts. Overall, the speciation rate of these copepods seems to havelagged behind that of potential host taxa.II’Table of ContentsSection PageAbstract iiTable of Contents iiiList of Tables ViList of Figures viiAcknowledgements ixINTRODUCTION 1MATERIALS AND METHODS 2BIOLOGY OF SIPHONOSTOME FAMiLIES PARASITIC ON VERTEBRATES 5Eudactylinidae Biology 5Kroyeriidae Biology 8Hatschekiidae Biology 11Pseudocycnidae Biology 12Hyponeoidae Biology 13Lernanthropidae Biology 14Dichelesthiidae Biology 16Penneffidae Biology 18Sphyriidae Biology 23ivSection PageLernaeopodidae Biology 25Naobranchiidae Biology 30Tanypleuridae Biology 30Dissonidae Biology 31Pandaridae Biology 32Cecropidae Biology 37Trebiidae Biology 38Euryphoridae Biology 39Caligidae Biology 40SIPHONOSTOME RELATIONSHIPS 43Monophyletic Siphonostomatoida 44Monophyly of Siphonostomes Parasitic on Vertebrates 45Interfamilial Relationships Among Siphonostomes Parasitic on Vertebrates 48EVOLUTIONARY BIOLOGY OF SIPHONOSTOMES PARASITIC ONVERTEBRATES 63Trends in Larval Development 64Trends in Adult Natural History 69Trends in Host Associations 76Invasion of Fresh Water 80Temporal Oiigin of Siphonostomes Parasitic on Vertebrates 87SUMMARY AND CONCLUSIONS 90VSection PageREFERENCES 94TABLES 108FIGURES 111APPENDIX 168viList of TablesTable PageTable 1 Apomorphy list supporting Figure21.109Table 2 Numbers of copepod species infecting various body regions of somesharks in the western North Atlantic 110VIIList of FiguresFigure Page1 Examples of sexual dimorphism associated with the adult general habitus ofrepresentative siphonostome lineages infecting vertebrates 1122 Ecological summary cladogram of eudactylinid genera 1143 Nemesis on the gill filaments of lamnid sharks 1164 Kroveria carchariaelauci parasitic on gills of a blue shark 1185 Kroveria caseyi females embedded in the interbranchial septum of a night shark 1206 Sectioned elasmobranch gill illustrating niches inhabited by some siphonostomecopepods 1227 Lemanthropus pomatomi female from a gill filament of a bluefish 1248 Sectioned teleost gill illustrating niches inhabited by some siphonostome copepods 1269 Pennella instructa females embedded in swordfish 12810 Ecological summary cladogram of pennellid genera 13011 Ventral view of cephalothorax of Pandarus bicolor 13212 Second maxillae of some pandarid copepods 13413 Cephalothorax rim of two pandarid copepods 13614 Phyllothvreus cornutus attached to blue shark interbranchial septum 13815 Pandarus bicolor maxillipeds 14016 Perissopus oblonatus second antenna 14217 Attachment method of Perissopus dentatus 14418 Cluster of ovigerous female Alebion crassus below trailing edge of scallopedhammerhead dorsal fin 14619 Alebion lobatus copepodids infecting a sandbar shark 148viiiFigure Page20 Large gathering of female Caligus productus on roof of yellowfin tunabuccal cavity 15021 Hypotheses of phylogenetic relationships of siphonostome families parasitic onvertebrates 15222 Mouth tubes of two elasmobranch infecting pandarids 15423 Frontal glands on ventral surface of two adult female pandarids 15624 Sternal elements of two caligiform copepods 15825 Phvllothvreus cornutus female maxilliped 16026 Life cycle summaries for siphonostomes parasitic on vertebrates 16227 Ecological summary cladogram of siphonostomes parasitic on vertebrates 16428 Comparison of the gills and olfactory sacs of elasmobranchs 166ixAcknowledgementsSo many people made this work possible that it is difficult to single out individuals foracknowledgement. However, special salutes are due M. L. Adamson (The University ofBritish Columbia), G. A. Boxshall (British Museum of Natural History), D. R. Brooks(The University of Toronto), J. N. Caira (The University of Connecticut), F. G. Carey(Woods Hole Oceanographic Institute), J. G. Casey (The National Marine FisheriesService), R. F. Cressey (United States National Museum), 0. B. Deets (The University ofBritish Columbia), J-S. Ho (The University of California at Long Beach), W. E. Hogans(Atlantic Reference Centre, N.B.), K. Izawa (Mie University), Z. Kabata (formerly ofThe Pacific Biological Station), N. Kohier (The National Marine Fisheries Service), P. R.Last (CSIRO, Division of Fisheries), A. 0. Lewis (The University of British Columbia),H. W. Pratt, Jr. (The National Marine Fisheries Service), G. G. E. Scudder (TheUniversity of British Columbia), 0. B. Skomal (Massachusetts Division of MarineFisheries), and C. B. Stiliwell (formerly of The National Marine Fisheries Service) forhaving so generously provided that which the author lacked. This study was partiallysupported by University of British Columbia Graduate Fellowships and TeachingAssistantships to the author, as well as by operating grants from The Natural Sciencesand Engineering Research Council of Canada to M. L. Adamson (The University ofBritish Columbia) and D. R. Brooks (formerly of The University of British Columbia).1INTRODUCTIONSubclass Copepoda is composed of ten orders, together containing more than 10,000described species (Huys and Boxshafl, 1991). Over 2000 copepod species are consideredparasitic (Cressey, 1983); however, as differences among commensal, mutualistic, andparasitic lifestyles are not often apparent without close inspection, the exact symbiotic statusof many copepod associations is unknown. Siphonostomatoida Thorell, 1859 contains over1550 species, of which some 1050 are generally regarded as parasites of vertebrates (almostexclusively fishes), about 500 are regarded as associates of invertebrates, and several specieshave no known host affiliation (Huys and Boxshall, 1991). Siphonostomatoida is basically amarine lineage, well-represented from abyss to surf, with only two families (both parasites offishes) containing freshwater representatives (see Kabata, 1979).Approximately 75 percent of all copepod parasites of fishes are siphonostomes (Yamaguti,1963; Kabata, 1982), and 18 of 40 siphonostome families are composed of species that canbe considered exclusive parasites of fishes. Taken together, these 18 families represent themost successful crustacean group parasitic on vertebrates, and as a whole they exhibit aninteresting diversity of morphological, ecological, and developmental traits.Morphologically within these families taxa range from those easily recognized assiphonostomes to others which have defied classification as crustaceans. Ecologicallydifferences regarding the preference to infect particular hosts and infection sites on the hostare evident. Even more noticeable are the facts that although most species are marineinhabitants some species are true freshwater residents, and that although most species areectoparasitic (i.e. they attach to the host in a superficial manner) some species aremesoparasitic (i.e. they attach by significantly penetrating the host while still leaving aportion of their body in full contact with the external environment). Also notable is that2while most taxa possess a one host life cycle, one family is well-known to contain specieswith a two host life cycle. Developmentally, differences in life cycles both within andamong siphonostome families parasitic on vertebrates exist, with these differencesconcerning the total number of life history stages, the number of stages which are capable ofinfecting the host, and the morphology of developmentally equivalent life history stages.The rich biological diversity displayed by the siphonostomes parasitic on vertebrates raisessome obvious evolutionary questions. Specifically, can primitive states and generalevolutionary trends be identified from the mixture of morphological, ecological anddevelopmental traits exhibited by these parasites, and how might such states and trends berelated to this group’s success?This thesis addresses the evolutionary biology of siphonostomes that infect vertebrates. Indoing so it attempts to interpret the biological significance of the morphological, ecological,and developmental diversity exhibited by these copepods with respect to an evolutionaryfoundation of familial relationships in hope of gaining a better understanding of the historywhich has resulted in the biological patterns which these widespread parasites display today.MATERIALS AND METHODSSynthetic by design, the infrastructure of this thesis is composed of this author’s personalobservations gathered over the past 14 years. During this period copepods were collectedfrom fishes with particular attention being paid to the specific identity of the host and theexact location of the copepods on the host. The bulk of these collections was taken fromfishes important to commercial and/or sport fisheries, and most of these were taken fromlarge oceanic gamefishes (both sharks and teleosts) caught in the western North Atlantic in3association with sportfishing tournaments and scientific research cruises. Specimens on loanfrom other personal and museum collections, as well as published information, were used toaugment data from the author’s collections.Copepods collected by the author were generally fixed in 10 percent (v/v) bufferedformalin and later transferred to 70 percent ethyl alcohol. For morphological studies,copepods were cleared and stained in lactic acid into which a small amount of lignin pinkwas dissolved, dissected using fine needle probes, and studied under a compound microscopeusing the wooden slide technique of Humes and Gooding (1964). Drawings of copepodswere often made with the aid of a camera lucida.Electron microscopy was used to augment observations made using light microscopy. Nospecial preparations were used to fix specimens for electron microscopy. Prior toexamination, specimens were critical point dried and sputter coated with gold using standardtechniques.To study the histological relationships between parasites and hosts, some copepods werefixed while still attached to host tissues. These samples were fixed in either 10 percent (v/v)buffered formalin or Bouin’s fixative. In the laboratory, these samples were dehydratedthrough a graded ethyl alcohol series, embedded in paraffin wax, and sectioned (10 jim)using a rotary microtome. Staining was in Delafield’s haematoxylin and eosin or Mallory’strichrome stain. Histological preparations generally followed the standard techniques foundin Humason (1972).A cladistic analysis (see Abbott nj,., 1985) was used to produce a cladogram ofphylogenetic relationships for the 18 families of siphonostomes parasitic on vertebrates. Acharacter set detailing the siphonostome parasites of vertebrates was constructed from4personal observations and published data (for a list of species and collections examinedduring the phylogenetic analysis of this thesis see Appendix 1). To determine character statepoiarity, the outgroup concept was used (see Stuessy and Crisci, 1984). A compositeoutgroup consisting of the siphonostome families associated with invertebrates was used todetermine character state polarity within the ingroup. When character states conffictedbetween outgroup candidates, the commonly accepted concept (e.g. see Boxshall .t L. 1984;Huys and Boxshall, 1991) that evolution has proceeded within Copepoda primarily byoligomerization (i.e. an evolutionary trend seen as a reduction in the number of bodysegments or other structural segments) was used to select the outgroup state. No effort wasmade to resolve relationships among siphonostome families associated exclusively withinvertebrates or among those with no known host affiliations. To arrive at a phylogeny thatseemed to possess at least some hope of reflecting reality, the ancient nature ofSiphonostomatoida and the evolution of parasitic lineages had to be considered. Thisresulted in championing assumptions that some lineages have undergone similar evolutionarytrends (i.e. parallel evolution) regarding body tagmosis, appendage segmentation, andappendage armament. These trends are associated with functional considerations (i.e.analogous use rather than homologous relationship), and none of the conventions used inidentifying them are new (see Kabata, 1979; Huys and Boxshall, 1991). The mostparsimonious cladogram was sought from all those possible from the set of character data.Table 1 provides descriptions of the apomorphic character states used in this analysis whichultimately determined the presented phylogeny.To evaluate evolutionary trends, developmental and ecological data gathered from personalfield observations and published reports were considered in light of or mapped onto theinterfamilial phylogeny of the siphonostomes parasitic on vertebrates or as appropriate ontopublished phylogenies detailing intrafamilial relationships. Mapping developmental andecological data onto a phylogeny simply involves the appropriate placement of these5observations on the phylogeny of a natural group of parasites with the intentions of analyzingthe historical connotations of the mapped information.Terminology used throughout the text conforms mostly with that adopted by Kabata(1979), Lincoln j j. (1982), and Huys and Boxshall (1991).BIOLOGY OF SIPHONOSTOME FAMILIES PARASITIC ON VERTEBRATESBrief synopses are provided below of morphological, developmental, and ecologicalinformation most pertinent to the phylogenetic analysis and evolutionary consideration of thesiphonostome families parasitic on vertebrates. These synopses are not intended to bethorough morphological diagnoses. Those interested in familial diagnoses for siphonostomesparasitic on vertebrates are referred to the following publications: Yamaguti, 1963; Kabata,1969b, 1979; Ho, 1987.Eudactylinidae BiologyEudactylinidae contains ten genera (see Deets and Ho, 1988). A synapomorphy defining thisfamily is unknown. However, most eudactylinids differ from other siphonostome parasitesof vertebrates by possessing a fifth pair of thoracic legs associated with a free thoracicsegment rather than being incorporated into a genital complex (i.e. a body region formed bythe fusion of the fifth pedigerous segment and the genital somites). Some eudactylinidgenera exhibit cuticular flaps of varying shapes and sizes on the general body surface and/orappendages (e.g. Eudactvlinodes Wilson, 1932, Eudactvlina van Beneden, 1853, JushevusDeets and Benz, 1987). However, these flaps are not diagnostic for Eudactylinidae because6they are not universally possessed throughout the family (e.g. Protodactylina Laubier, 1966,Bariaka Cressey, 1966, Nemesis Risso, 1826, Carnifossorius Deets and Ho, 1988,Eudactvlinopsis Pillai, 1968, Eudactvlinella Wilson, 1932, Heterocladius Deets and Ho,1988). Except in Carnifossorius (see below) body segmentation anterior to the genital regionis conservative, with the cephalothorax incorporating the first pedigerous segment followedby four free pedigerous segments. Thoracic legs one-four are biramous, each ramus withtwo or three segments. Although vestigial, the fifth legs are large relative to those of othersiphonostome parasites of vertebrates. Following the genital region is an abdomenconsisting of one to four segments. First antennae exhibit 5 to 18 often ill-defined segments.The first antennae of Eudactvlinodes and Eudactvlina display large claws on the secondsegment and geniculate flexion (see Kabata, 1979; Deets and Ho, 1988) and probably assistin grasping the host. A rostrum occurs ventrally on the cephalothorax between the firstantennae of several eudactylinids. In Eudactvlina the rostrum consists of a basal plate with aposteroventrally directed tine (Kabata, 1979) while in Carnifossorius it consists of a basalplate only (Deets and Ho, 1988). Eudactylinid maxillipeds vary in shape between genera(see Kabata, 1979), with those of adult females generally ranging from subchelate to chelate.Sexual dimorphism is rather limited in Eudactylinidae (Fig. 1), and is often most pronouncedin the maxillipeds (typically subchelate in males (see Kabata, 1979)) and thoracic legs (oftenmore robustly armed and ornamented in males, including both longer setae and spines andgreater density of pinnae (see Kabata, 1979; Deets and Benz, 1987; Deets and Ho, 1988)).The first antenna of male Eudactvlinella i]Wilson, 1932 exhibits a curious geniculateterminus which possibly assists in grasping the female during copulation.Two eudactylinid genera display striking forms. Jushevus is notable because its firstthoracic segment bears dorsolateral styliform projections, and by possessing a genital somiterather than a genital complex. Jushevus is also unusual because it has short multiseriate eggsacs containing round eggs.7The Carnifossorius adult female displays a greatly elongated cylindrical body with acephalosome (i.e. the anterior portion of the body consists of five cephalic plus themaxiffiped bearing somites) followed by an expansive first pedigerous segment, pedigeroussegments two-four, a genital complex incorporating the fifth pair of legs, and an abdomen.Together these characteristics make Carnifossorius the most unusual member ofEudactylinidae. The modified habitus of Carnifossorius appears well-suited to itsmesoparasitic lifestyle which is unique among eudactylinids. In Jfli, the adult female isburied to about the level of the first thoracic legs (a distance representing 20 percent of herlength) in the interbranchial septa of her guitarfish host (Rhina ancvlostoma Bloch andSchneider, 1801). The massive anteriorly projecting chelate maxihipeds apparently serve aprimary role in attachment, as the straight tubular body itself does not seem totally capableof this function. Although males are currently undiscovered, they probably are ectoparasitic,more mobile, and exhibit relatively smaller and less modified bodies than females.The phylogeny provided by Deets and Ho (1988) serves as a working hypothesis forsystematic and ecological studies of Eudactyhinidae. Reductions in the number of abdominalsegments, in appendage segments, and in the number of armature elements associated withappendage segments was proposed (Deets and Ho, 1988) as an evolutionary process withinEudactyllnidae and was generally corroborated by other seemingly independentmorphological changes.As indicated by extant taxa, Eudactyhinidae appears to have originated on elasmobranchfishes and throughout its history has at least once invaded teleosts (see Deets and Ho, 1988).Mapping ecological characters onto the phylogeny of Deets and Ho (1988) shows thatectoparasitism is the predominant and primitive lifestyle within the lineage and thatmesoparasitism is a derived activity (Fig. 2). Without exception, eudactyhinids are parasites8of the branchial and olfactory regions of their hosts. The olfactory sacs represent asecondarily acquired niche (Fig. 2). Preliminary data show that on the gills and within theolfactory sacs various eudactylinid species are conservative regarding specific attachmentlocations (Fig. 3; also see Benz 1980; Benz and Adamson, 1990).Developmental data for Eudactylinidae is incomplete. Copulation posture of Nemesisrobusta van Beneden, 1851 has been seen on several occasions (Wilson, 1932; Carli andBruzzone, 1978; Benz and Adamson, 1990). During copulation males use their maxillipedsto grasp females in a manner similar to that in which both sexes grasp their hosts. Except asnoted above for Jushevus, eudactylinid egg sacs are straight and contain slightly compressedeggs that are arranged uniseriately. Only two papers contain reports on eudactylinid larvae(Wilson, 1922; Kabata, 1976), and both deal with an unremarkable nauplius stage.Kroyeriidae BiologyKroyeriidae contains three genera: Prokroveria Deets, 1987, Kroeverina Wilson, 1932, andKroveria van Beneden, 1853. Although kroyeriids are easily identified by a combination ofunexclusive characters (see Deets, 1987), a synapomorphy defining this family is unknown.Kroyeriids have a small dorsoventrally flattened cephalothorax incorporating the firstpedigerous segment followed by three small free thoracic segments, a long tubular genitalcomplex, and a small one- to three-segmented abdomen. First antennae are seven- to nine-segmented. Second antennae are chelate, a notable condition found elsewhere amongsiphonostomes only in Penneffidae and Pseudohatschekia Yamaguti, 1939 (a dubiousmember of Hatschekiidae (see Kabata, 1979)). Maxiffipeds are subchelate and relativelyunmodified. Thoracic legs one-four are relatively unmodified, biramous, trimerous, withright and left pairs connected by interpodal bars. Leg setae are well-developed and enable at9least some of these copepods to swim freely as adults (Benz, 1986; Benz and Dupre, 1987).A small degree of sexual dimorphism is seen in kroyeriids (Fig. 1), with males being smaller(mainly due to the smaller size of the genital complex) and displaying more densely pinnatesetae (possibly indicating greater mobility).In addition to the aforementioned shared but not unique characteristics, some kroyeriidgenera exhibit interesting novelties. Kroveria species display a pair of dorsal stylets whicharticulate with the posterior of the cephalothorax via a ball and socket-type joint. Thesedorsal stylets can be moved and presumably assist in temporary attachment by proppingthese copepods against the gill lamellae in the face of respiratory water flow (Fig. 4; see alsoBenz and Dupre, 1987). The dorsal stylets are reminiscent of similar structures found onJusheyus and male Eudactvlinopsis (both Eudactylinidae). Dorsal stylets of Kroveriaspecies, however, differ from the dorsal styliform projections of Jusheyus in that the latterproject from the first free thoracic segment rather than the cephalothorax and they do notarticulate via a well-developed ball and socket joint (see Deets and Benz, 1987). However,Deets and Benz (1987) noted that the body segmentation of Jushevus was difficult tointerpret, and that Jusheyus may possess a cephalosome rather than a cephalothorax. Shouldthis be true, the dorsal styliform projections of Jusheyus could be interpreted as an ancestralstate to the dorsal stylets of Kroveria. Unfortunately comparison of the lateralcephalothoracic spines of male Eudactvlinopsis to the dorsal stylets of Kroveria is preventedby a somewhat superficial description of Eudactvlinopsis and a lack of study material.Although their exact attachment location has not been documented, Eudactvlinopsis, likeKroveria species, resides on the gills of an elasmobranch (Pillai, 1968). The presence oflateral cephalothoracic spines in male Eudactvlinopsis could represent a convergence withKroveria analogously serving a temporary attachment role linked to the greater mobility andless powerful attachment appendages of Eudactvlinopsis males versus females. This10conjecture is supported by the observation that female Eudactvlinopsis have chelatemaxilhipeds which appear more powerful than the subchelate maxillipeds of the males.Kroveria species also display interpodal stylets on the mterpodal bars of legs one-four.These stylets, which do not articulate but which can be erected by movements of theinterpodal bars, seem to provide a series of paired ventral tines that could be used like thedorsal stylets to prop these copepods against the host substrate in the face of water flow.Prokroveria and Kroeverina display a pair of rostral processes at the anterior of thecephalothorax (see Deets, 1987). These processes are rudimentary in Prokroveria and aremost developed in the lineage of Kroeverina infecting sharks, where they form two closelyapplied upturned horns (see Deets, 1987). The function of these structures is unknown.However, each of the two Kroeverina lineages (one infecting batoids the other infectingsharks) has distinctive second antennae (Deets, 1987). The chelate second antennae ofkroyeriids serve as the primary attachment appendages (Fig. 4), and possibly the dissimilarsecond antennae of these two lineages reflect differences in modes of attachment and that theenlarged rostral processes of the shark infecting lineage are somehow associated with theseattachment differences.All kroyeriids infect chondrichthyan fishes. Prokroveria and all Kroveria species except K.casevi Benz and Deets, 1986 inhabit (respectively) the gill lamellae of chimeras and sharks,while Kroeverina species reside between the olfactory lamellae of elasmobranchs. Thebranchial chambers and olfactory sacs of chondrichthyans are quite similar environments(see below), each being composed of an orderly arrangement of narrowly spaced epitheliallamellae between which water flows in a one-way pattern (Benz, 1984, in preparation). Thelong thin kroyeriid habitus conforms well to such tight environments (Fig. 4).11Kroveria casevi is unusual among kroyeriids in that it is a mesoparasite (Benz and Deets,1986). Up to 80 percent of these relatively gigantic adult females (some reaching 60.5 mmlong) can be found tortuously buried in the interbranchial septa of their shark hosts (Figs 5and 6). Both the dorsal stylets and interpodal bars ofL casevi seem relatively smaller (seeBenz and Deets, 1986) than those of other congeners. These observations lend addedevidence of an attachment role for these structures in ectoparasitic kroyeriids. Kroveriacasevi is most remarkable because it possesses the typical array of Kroveria swimming andattachment structures even though they hardly seem necessary for a parasite that is so deeplyembedded in its host. The j caseyi male is relatively small and ectoparasitic. Presumablymating occurs prior to the growth period which ultimately transforms the female into itslarge mesoparasitic form.Almost nothing is known of kroyeriid development. Egg sacs are straight and containslightly compressed eggs arranged uniseriately. Benz and Deets (1986) gave a description ofKroveria caseyi nauplii that hatched upon fixation of adult females. Carli and Bruzzone(1973) reported keeping newly hatched nauplii of K.. carchariaeglauci Hesse, 1879 alive inthe laboratory for three days.Hatschekiidae BiologyHatschekiidae contains six genera: Hatschekia Poche, 1902 with 78 species, ProhatschekiaNunes-Ruivo, 1954 with six species, Congericola van Beneden, 1851 with three species,monotypic Pseudocongericola Yu, 1933, monotypic Bassettithia (Wilson, 1922), andmonotypic Wynnowenia Boxshall, 1987. Uniting the family, male and female hatschekiidslack maxillipeds and possess second maxillae with bifid claws. The hatschekiid generalhabitus is more (e.g. Hatschekia gracilis Yamaguti, 1954) or less (e.g. jj cepolae Yamaguti,121939) elongated and cylindrical in cross section. When body segmentation is distinct (e.g.Wvnnowenia) the general habitus is composed of a cephalothorax incorporating the firstpedigerous segment followed by up to three free thoracic segments, a genital complex, andan abdomen. When body segmentation is obscure the general habitus can range from acephalothorax followed by an indistinctly segmented thoracic neck and trunk (e.g.Hatschekia linearis Wilson, 1913), to merely a cephalothorax and trunk (e.g. ji modestaKabata, 1965). The location of the thoracic legs is important in delimiting body regions ofindistinctly segmented species. First antennae are uniramous, three- to nine-segmented.Second antennae form unciform claws. Three to five pairs of thoracic legs may be present,existing as biramous multimerous, biramous unimerous, or vestigial structures (see Kabata,1979, 1991; Jones, 1985; Boxshall, 1987). Egg sacs are straight and the slightly compressedeggs are arranged uniseriately. Males are generally similar to albeit smaller than femalesbecause of their relatively smaller genital complexes. Lacking maxillipeds, hatschekiidmales use their second antennae to grasp females during copulation (see Jones, 1985).Almost nothing is known of the life history of Hatschekiidae. Conericola,PseudoconericoIa, Bassettithia, and Wynnowenia are all gill parasites of conger eels(Congridae) or pike conger eels (Muraenesocidae) found throughout the world’s oceans (seeBoxshall, 1987). Prohatschekia and Hatschekia are found on the gills of numerous teleosts,especially in marine waters of lower latitudes (see Yamaguti, 1963; Jones, 1985; Kabata,1991).Pseudocycnidae BiologyPseudocycnidae contains three genera: Cvbicola Bassett-Smith, 1898 with three species,Pseudocvcnoides Yamaguti, 1963 with two species, and monotypic Pseudocvcnus Heller,131865. A synapomorphy defining this family is unknown. The adult female is relatively longand cylindrical, often without well-defined segmental boundaries. The first pedigeroussegment is incorporated into the cephalothorax, while the fourth and fifth leg bearingsegments are amalgamated with the genital components to form a genital complex. Theabdomen is small, sometimes with large posterolateral caudal rami (e.g. Pseudocvcnus).First antennae are uniramous and often indistinctly segmented. Second antennae exhibitunciform terminal claws, second maxillae are brachiform, and maxillipeds are subchelate.Three to five pairs of modified legs are present. Legs one and two are typically biramousand unimerous, with rami issuing stubby naked setae. Third legs are usually uniramous andunimerous, and fourth and fifth legs are often vestigial and represented by a small cuticularbump with a short spiniform seta. Egg sacs are straight, with compressed eggs arrangeduniseriately. Males are generally similar to albeit smaller than females because of theirrelatively smaller genital complexes. Pseudocvcnus males are notable in exhibiting aconspicuous lateral projection on each side of the genital complex bearing the flageffiformfourth legs.Besides Wilson’s (1922) report of Cybicola buccatus (Wilson, 1922) nauplii, nothing isknown of the larval development of pseudocycnids. Family representatives are foundthroughout the world’s oceans as gill parasites mainly of scombrids (Scombridae).Hyponeoidae BiologyHyponeoidae contains two monotypic genera: Hvponea Heegaard, 1962 and TautochondriaHo, 1987. A synapomorphy defining this family is unknown. Adult female hyponeoidsdisplay a roughly rectangular cephalothorax incorporating the first pedigerous segment, andappear generally similar to lernanthropids. Unlike lernanthropids, however, hyponeoids14have a well-delimited thoracic neck and relatively large indistinctly segmented abdomenswhich bear lateral processes from their anterior portions. Between the cephalothorax andabdomen a relatively large genital trunk issues a number of blunt processes. First antennaeare uniramous and indistinctly six-segmented. Second antennae are uniramous and formpowerful curved claws. Second maxillae are brachiform and notable in that the brachiumdistally bears one spiniform seta. Maxillipeds are subchelate. Thoracic legs one(incorporated into the cephalothorax) and two (on the thoracic neck) are present as smallbiramous unimerous structures with spiniform setae. Egg sacs are spiral shaped with discoideggs arranged uniseriately. Males are unknown.Hyponeoids have only been collected on several occasions (Heegaard, 1962; Markevitchand Titar, 1978; Ho, 1987) and have been positively recorded from only two hosts; abarracudina (Notolepis rissoi (Bonaparte, 1841): Paralepididae: Iniomi) and the fangtooth(Anoploaster comuta (Valenciennes, 1833): Anoplogasteridae: Berycomorphi).Hyponeoids seem to be a deep-sea group parasitic on the gill filaments of teleost hosts (Ho,1987). Nothing is known of their larval development.Lemanthropidae BiologyLemanthropidae contains seven genera: Lernanthropus de Blainville, 1822 with 123 species,Aethon Krøyer, 1837 with four species, Norion von Nordmann, 1864 with two species,SaumWilson, 1913 with seven species, Lernanthropodes Bere, 1936 with three species,Lemanthropinus Do, 1985 with eight species, and monotypic Lernanthropsis Do, 1985. Thehighly modified bilobate fourth legs of lernanthropids are a synapomorphy unifying thefamily (see Ho and Do, 1985). The adult female cephalothorax incorporates the firstpedigerous segment and typically folds ventrally along its lateral margins forming a trench15through which one host gill filament passes (Figs 7 and 8). In some species (e.g.Lernanthrouus chrvsophrvs Shishido, 1898) the cephalothorax exhibits lateral processes.Behind the cephalothorax the large indistinctly segmented trunk may display lateral (e.g.L.emanthropinus), dorsal (e.g. Lemanthropus, Aethon, Sagum, Norion), or ventral (e.g.Lernanthropodes) plates which may be partially or entirely formed from the third pair of legs(see Ho and Do, 1985). The abdomen usually is small and obscurely one- or two-segmented.First antennae are uniramous, often indistinctly segmented, and sometimes display aparabasal flagellum (e.g. Lernanthropus). Second antennae and maxiffipeds are powerfullysubchelate. Second maxilae are brachiform with well-developed distal armament. First legsare small, biramous, and unimerous. Second legs are usually similar to the first, or with ramifused to the sympod (e.g. Aethon), or absent (e.g. Norion). Third and fourth legs are highlymodified. The third legs are notable in that they sometimes are large ventrally directedstructures together forming a trench in line with that of the cephalothorax through which onehost gill filament passes (Fig. 7). Egg sacs are straight or coiled with discoid eggs arrangeduniseriately. Male lernanthropids mainly differ from females in being smaller because oftheir relatively smaller genital complexes. Lernanthropid males also differ from females inthat their cephalothoraxes are not as contoured to conform to the host’s gill filaments, and inthat the highly modified third legs are typically lobate or biobate structures which projectlaterally from the body.Although only one complete life cycle is known, developmental data for Lernaeopodidaeare significant. Development in Lernanthropus kroyeri van Beneden, 1851 involves twonauplius, one infective copepodid, four parasitic copepodid, two preadult, and one adultstages (Cabral, 1983; Cabral L. 1984). The life cycle is particularly important because itrepresents the first complete life cycle for a siphonostome parasitic on vertebrates whichdoes not include a chalimus stage (i.e. a copepodid tethered to its host by a frontal filamentissued from a frontal organ on the cephalothorax).16Lernanthropids have worldwide distribution on marine teleosts, and display relatively highlevels of host specificity (see Yamaguti, 1963; Kabata, 1979; Ho and Do, 1985). They areexclusive gill parasites whose adult female habitus is uniquely modified to allow thesesizable parasites to efficiently attach about the afferent and efferent arterioles of the gillfilaments of their hosts (see Davey, 1980).In a phylogenetic analysis of Lernanthropidae, Ho and Do (1985) presented a hypothesis ofintrafamilial evolution which reduced hydrodynamic drag and increased security of therelatively large and sessile adult female. Ho and Do (1985) proposed a euryhaline origin onteleost fishes for Lernanthropidae sometime about the Cretaceous. This conjecture wasbased on two points: the presumed relationship between Lernanthropidae and Dichelesthiidaeand the discovery of the dichelesthiid fossil Kabatarina Cressey and Boxshall, 1989 on aeuryhaline teleost from lower Cretaceous deposits, and the euryhaline host relationship ofone of the two most primitive extant lernanthropids (Ho and Do, 1985). However, theassumption that Kabatarina is more closely related to Lernanthropidae than it is to any othermarine siphonostome is now open to serious question because recent data suggest thatHyponeoidae appears much like Lemanthropidae (see Ho and Do, 1985; Ho, 1987). Becauseof this it is possible that Lernanthropidae originated on marine teleosts prior to theCretaceous.Dichelesthiidae BiologyDichelesthiidae contains three monotypic genera: extant Dichelesthium Hermann, 1804 andAnthosoma Leach, 1816, and extinct Kabatarina. A groove on the second maxilla delimitingthe distal portion of the brachium from the calamus is the only unique feature unifying17Dichelesthiidae (Cressey and Boxshall, 1989). The adult female dichelesthiid cephalothoraxincorporates the first pedigerous segment and is followed by three or four often indistinctthoracic segments, a genital complex, and a one- to three-segmented abdomen. Elytra can bepresent laterally on the second and third pedigerous segments (Dichelesthium), or dorsally onthe second (Anthosoma) or third and fourth (Kabatarina) segments. First antennae areuniramous, composed of six (Dichelesthium and Anthosoma) or at least 20 (Kabatarina)segments. Second antennae are subchelate and retractile in Dichelesthium and Anthosoma,and very robust and nonretractile in Kabatarina. Second maxillae are brachiform withprehensile tips. Maxillipeds are subchelate, with an undivided shaft and robust corpus inDichelesthium and Anthosoma, or a three-segmented shaft and relatively more slendercorpus in Kabatarina. Kabatarina displays four pairs of biramous, multimerous thoracic legs.In Dichelesthium legs one and two are biramous and unimerous, and leg three is anunsegmented lappet. In Anthosoma legs one-three are subcircular aliform plates. Egg sacsare straight in Dichelesthium, loosely coiled in Anthosoma, and unknown in Kabatarina.Eggs are discoid and arranged uniseriately. Sexual dimorphism is minimal inDichelesthiidae. Typically males are smaller than females because of a relatively smallergenital complex (Fig. 1). Males also lack well-developed lateral or dorsal elytra, andsometimes (e.g. Anthosoma) exhibit thoracic legs in a somewhat less modified conditionthan females. Little is known of the larval development of dichelesthiids. Kabata andKhodorevski (1977) have reported on a copepodid of Dichelesthium.Anthosoma crassum (Abildgaard, 1794) is distributed throughout the world’s oceansmainly on large pelagic sharks where it usually, but not always, attaches in the mouthbetween the teeth and in the branchial chamber along the gill arches (e.g. Wilson, 1932;Shiino, 1955; Lewis, l966a). Dichelesthium oblongum (Abildgaard, 1794) is distributed inthe North Atlantic, Mediterranean, and Adriatic and Black Seas, where it is a gill parasite ofsturgeons (Acipenseridae). Although it has been found in fresh water on migrating sturgeons18it is considered a marine species (see Kabata, 1979). Fossil Kabatarina pattersoni Cresseyand Boxshall, 1989 was discovered in northern Brazil in lower Cretaceous deposits(approximately 110 myo). These fossils were extracted from within the branchiocranium ofthe salmonoid fish Cladocvclus gardneri Agassiz, where they were presumably gill or buccalcavity parasites not unlike Dichelesthium and Anthosoma. Based on stratigraphy, Cresseyand Boxshall (1989) speculate that these fossils were deposited in an estuarine environment.It is notable that during this period of earth’s history Brazil was closer to Africa than it isnow (Windley, 1984) and the contemporary range of Dichelesthium oblonum (see Kabata,1979, 1988a) would have appeared smaller. This possibly indicates that continental drift isresponsible for the present distribution of this species.Penneffidae BiologyPennellidae contains 20 genera (see Kabata, 1979; Castro and Baeza, 1985; Boxshall, 1986),and is unique within Siphonostomatoida because some of its members exhibit two host lifecycles (Kabata, 1979).Pennellid development begins according to a typical or slightly modified siphonostomeplan. Developing eggs hatch, releasing either nauplii (e.g. see Sproston, 1942; Schram,1979) or infective copepodids (e.g. see Perkins, 1983). The latter pathway shortens the free-living portion of the life cycle in that nauplius development occurs while the embryo is stillwithin the shelter of the egg. Free swimming copepodids seek their intermediate hosts (oronly host for monoxenous species), on which they pass through a series of three or fourchalimus stages (Kabata, 1981; Perkins, 1983) tethered to the host by a frontal filament.During copepodid-chalimus development pennellids acquire their characteristic mouth tubes(Sproston, 1942; Rose and Hamon, 1953; Kabata, 1963; Ho, 1966a; Schram, 1979; Perkins,191983). The penneffid mouth tube is notable because its labrum and labium becomeintricately fused to form a proboscis-like oral cone which is capable of telescoping extension(Boxshall, 1990; Castro and Baeza, 1991). Chalimus development results in the productionof free swimming (i.e. not tethered by a frontal filament) adult males and untransformedadult females. At this point, copulation often takes place and in effect ends the male’susefulness. However, before death males may remain on the intermediate host, become freeswimming in the water column, or occasionally swim to the definitive host withoutsubsequent development (Kabata, 1958; Anstensrud, 1992). Adult males and untransformedadult females are relatively unspecialized. The first antennae typically display reducedsegmentation or an otherwise reduced appearance relative to most members ofEudactylinidae, Kroyeriidae, Hatschekiidae, Pseudocycnidae, Hyponeoidae,Lemanthropidae, and Dichelesthiidae. The second antennae are robust and chelate, andhaving been present in this form since the copepodid stage they have been the primaryattachment organs during postnauplius periods lacking the frontal filament. Up to four pairsof setose swimming legs each connected by an interpodal bar may be present, their locationssimilar to those of adult kroyeriids. The untransformed adult female’s cephalothorax isunusual because it lacks maxihipeds (Kabata, 1979). Untransformed females may alsodisplay mandibles with seemingly underdeveloped dentition (Kabata, 1967a; Schram, 1979;Castro and Baeza, 1986).After attaching to the definitive host, female pennellids undergo a metamorphosis. Thischange is apparently prompted by insemination (Anstenstrud, 1990a) and results in an oftenmonstrous fully transformed adult female that frequently has confused naturalists. In fact,pennellids were among the first recorded fish parasites, with such noted scholars as Aristotleand Pliny misinterpreting their taxonomic status and treating them as worms (Wilson, 1917).20The untransformed adult female attaches to the defmitive host using its powerful chelatesecond antennae. Then in an unknown manner the tiny female burrows into its host usually,but not always, toward a specific target. Often the lumen of some organ or region is sought:the ventral aorta (e.g. see Kabata, 1967b, 1970, 1979; Grabda, 1991), the heart (e.g. seeKabata, 1967b, 1970; Grabda, 1991; Perkins, 1983), the eye (e.g. see Kabata, 1969a;Schram., 1979; Grabda, 1991; Anstensrud and Schram, 1988), or the visceral cavity (e.g. seeShiino, 1958; Ho, 1966b; Kabata, 1979; Grabda, 1991). Prior to or upon reaching its finaldestination, the female begins to metamorphose (i.e. continuous growth not involving amolt). Various body regions (e.g. cephalic, thoracic, genital, and abdominal) begin toallometrically enlarge (see Kabata, 1969a, 1979; Schram, 1979, 1980; Grabda, 1991;Perkins, 1983; Castro and Baeza, 1985, 1986). The true appendages do not enlarge duringthis growth phase and are soon dwarfed by the surrounding regions’ often grotesqueexpansions. This process results in an almost unrecognizable adult female with acephalothorax deeply buried within the host, and genital and abdominal regions trailing freefrom the host into the surrounding water (Fig. 9). Egg sacs (which may be straight or coiled,with discoid eggs arranged uniseriately) extend from the female’s posteriorly located oviductopenings into the water. Depending upon the trajectory of penetration, the adult female maybe straight or highly twisted. The cephalothorax of some genera develops lateral processeswhich assist in anchoring these often enormous parasites (Kabata, 1979). Many pennellidsexhibit a relatively high degree of intraspecific phenotypic variation as a result of theirallometric growth phase interacting with various hosts and attachment locations (e.g. Kabataand Wilkes, 1977; Kabata, 1979; Hogans, 1986, 1987a, 1987b, 1988; Castro and Baeza,1988; Benz and Hogans, in press).Ophiolernaea Shiino, 1958 is a particulary unusual pennellid genus. Overall, most of thegrowth centers of Ophiolernaea are conservative in their metamorphic expansion. However,the oral region undergoes an enormous growth phase producing a long proboscis-like21extension. As a result, the buccal orifice is far removed from the rest of the cephalothorax.The vermiform proboscis of adult female Ophiolemaea tortuously works its way throughoutthe viscera of its host (Grabda, 1991). ODhiolemaea’s need for such an extremely long oralregion is unknown. However, it may be linked to the fact that the visceral cavity of fishes isa mass of relatively shifting tissues and is quite different from the relatively more solid andstable regions where other pennellids often live. Thus Ophiolernaea may periodically find itsmouth in a void. Possession of a growing mouth tube would seem to ensure contact withhost tissues in such an unstable environment and might be considered an adaptation tomesoparasitism of the visceral cavity. Incipient development of luxuriant oral regions can beseen in Metapeniculus antofaastensis Castro and Baeza, 1985 and some Peniculus vonNordmann, 1832 species (e.g. . elonatus Boxshafl, 1986).Pennellids share several morphological features which appear important to theirmesoparasitic lifestyle. For example, the diagnostic lack of maxillipeds by female pennellidsseems compensated for in males, untransformed females, and superficially attachedtranformed females by the powerful second antennae. During parasitic larval stages,possession of both chelate second antennae and a frontal filament reduces need formaxillipeds to secure the host. In deeply embedded species the transformed female’s generalhabitus itself provides additional attachment support. Maxillipeds are retained by malepennellids and are used during copulation (see Sproston, 1942; Schram, 1979; Perkins,1983). The mouth tube of pennellids also seems to lend itself well to mesoparasitism. Onceembedded in its definitive host, the female often may be so firmly surrounded by host tissuethat elevating or depressing the mouth tube in typical siphonostome fashion might beimpossible (see Kabata, 1974a, 1979; Boxshall, 1990). For pennellids, a telescoping mouthcone perhaps solves this problem. The allometric growth phase which results inmesoparasitic females is also notable because it reshapes the habitus so that the copepod’sbody is not only firmly anchored, but also so that it extends from the internal source of22nutrition to the external environment into which the offspring are shed. The ability totraverse this expanse precludes the free swimming larvae from having to negotiate aseemingly impossible journey. The allometric growth phase is considered (Kabata, 1979;Boxshall, 1986) to be an addition to the pennellid ancestral life cycle.Boxshall (1986) presented a cladogram of Pennellidae genera summarizing knowledge oftransformed adult females. Although only partially resolved, this phylogeny faithfullyreproduced earlier ideas of Kabata (1979) concerning major pennellid lineages. To updateBoxshall’s (1986) cladogram, Metapeniculus Castro and Baeza, 1985 can be assigned to thePeniculus-group. When ecological life history traits are mapped onto the cladogram theysuggest that mesoparasitism may have arisen from an ectoparasitic lifestyle withinPennellidae (Fig. 10). As set forth by Kabata (1982) and graphically depicted by Boxshall’s(1986) cladogram, attachment of pennellids on the body and fins of fishes represents theancestral condition while attachment to the gills and into the lumen of internal organsrepresents more derived lifestyles. Even relatively ectoparasitic penneffids (e.g. Peniculusand Peniculisa Wilson, 1917 species) burrow somewhat into their hosts using their secondantennae as major attachment organs. This invasion initiates the proliferation of host tissuessurrounding the parasite which eventually assists in strengthening parasite attachment(Kabata, 1979; Radhakrishnan and Nair, 1981). Although information concerning the larvaeof most pennellids is lacking, the use of two hosts may be another life history characteristicthat arose within the family (Fig. 10).Pennellidae is successful in infecting the most phylogenetically diverse host array of allsiphonostome lineages, with hosts including mollusks, teleosts, and mammals. Whetherfishes or invertebrates represent the more derived condition regarding the use of anintermediate host cannot be established based on current knowledge (see Fig. 10).Evolutionarily, however, it seems ecologically significant that pennellids often infect tightly23schooling organisms (see Yamaguti, 1963; Kabata, 1979). This preference may havepredisposed the lineage to sometimes use the same host species as both an intermediate anddefinitive host (e.g. see Anstensrud and Schram, 1988). Two host life cycles may havefurther been facilitated by the loose attachment and powerful swimming ability of larvae andyoung adults. It also seems significant that for many pennellids using different species as theintermediate and definitive hosts the intermediate host is often a schooling organism thatserves as prey for the definitive host (e.g. Pennella filosa (L, 1758) and L instructa Wilson,1917 use squid as intermediate hosts and very often tunas and biifishes as definitive hosts;see Rose and Hamon, 1953; Kabata, 1979; Hogans nj., 1985; Hogans, 1986). Such apredator-prey association between the definitive and schooling intermediate hosts wouldseem to assure close host juxtaposition for parasite transmission.Sphyriidae BiologySphyriidae contains eight genera: Sphyrion Cuvier, 1830 with two species, LophouraKöffiker, 1853 with 12 species, Tripaphvlus Richiardi, 1878 with two species, monotypicOpimia Wilson, 1908, Paeon Wilson, 1919 with five species, monotypic Periplexis Wilson,1919, monotypic Paeonocanthus Kabata, 1965, and monotypic Norkus Dojiri and Deets,1988. Sphyriids are easily identified by a combination of characters (see Dojiri and Deets,1988), however, a synapomorphy defining this family is unknown. Adult female sphyriidsare all mesoparasites and display a loss of external segmentation (Fig. 1). The femalehabitus can be divided into three general regions. The anterior region may be a simpleexpansion (e.g. Opimia, Periplexis, Paeonocanthus, Lophoura) or a more complex structurewith various protuberances (e.g. Norkus, Paeon, Tripaphylus, Sphvrion). The anterior regionis followed by a narrower cylindrical neck which may (e.g. Norkus, Periplexis,Paeonocanthus, Lophoura) or may not (e.g. Paeon, Tripaphvlus, Opimia, Sphvrion) display24some type of expansion presumably serving as a holdfast. The posterior region may eitherform a gradual expansion from the neck (e.g. Paeon, Tripaphvlus, Opimia), a discoid shape(e.g. Norkus) or an ovoid shape (e.g. Periplexis, Paeonocanthus, Lophoura, Sphvrion). Apair of posterior processes representing modified caudal rami is attached to the trailingportion of the posterior region and may be cylindrical (e.g. Norkus, Paeon, Tripaphvlus,Opimia, Paeonocanthus), transversely constricted (e.g. Periplexis), multiply cylindrical (e.g.Lophoura), or branching (e.g. Sphvrion). jtu, the cephalothorax and at least two freethoracic segments are embedded in the host with one thoracic segment and thegenitoabdomen trailing free from the host.Appendages of transformed sphyriid females are generally small. First and secondantennae are primitively uniramous and biramous respectively and sometimes onlyrepresented by cuticular swellings (e.g. Periplexis, Paeonocanthus, Lophoura, Sphvrion).The mandibles of most genera are unknown, however, those of Norkus display both primaryand secondary teeth (Dojiri and Deets, 1988) and appear very similar to the mandibles oflernaeopodids (e.g. see Kabata, 1979). When present, the second maxillae may be long andindistinctly segmented (e.g. Norkus) or mere cuticular sweffings (e.g. Lophoura, Sphvrion).Maxillipeds, when present, are subchelate (e.g. Norkus, Tripaphvlus, Opimia, Sphvrion).Thoracic legs, represented as vestigial structures (e.g. Opimia), are rarely present. Sphyriidegg sacs contain spherical eggs arranged multiseriately.Sphyriid males have a grub-like form (Fig. 1), and are similar to males found in thefamilies L.ernaeopodidae and Naobranchiidae. Developmental observations of Sphyriidaeare few and detail only early and late life history stages. In Paeon and Sphvrion, naupliusstages are passed inside the egg, resulting in a copepodid being the first free-swimminglarval stage (Wilson 1920, 1932; Jones and Matthews, 1968). It is noteworthy that twoimportant features can be seen in the first copepodid stage of Paeon (see Wilson, 1932) and25Sphvrion (see Jones and Matthews, 1968): the coiled frontal filament, and the biramoussecond antennae. Based on observations of lernaeopodid development (see below) it isgenerally accepted that the highly modified adult female results from the metamorphosis ofan untransformed larval or young adult stage. Observations of Sphvrion metamorphosisreveal a process of polyphasic growth of various body regions (this process was detailed byKabata (1979) concerning Penneffidae).Based on the phylogenetic analysis of Dojiri and Deets (1988), Sphyriidae consists of twoclades. The Tripaphvlus-clade (i.e. Norkus, Paeon, Tripaphylus, Opinlia) infectsElasmobranchii while the Sphvrion-clade (i.e. Periplexis, Paeonocanthus, Lophoura,Sphvrion) infects Teleostei. The sphyriid phylogeny of Dojiri and Deets (1988) isinteresting because it is almost entirely congruent with an independent phylogeny of theseparasites’ hosts. Dojiri and Deets (1988) mapped environmental life history traits ofsphyriids onto their sphyriid phylogeny and noted two dade specific lifestyles. Whenrecords of this author (Benz, 1986) are added to the analysis of Dojiri and Deets (1988),members of the Elasmobranchii infecting Tripaphvlus-clade are all seen as parasites of theolfactory and branchial chambers while species composing the Teleostei infecting Sphvriondade all penetrate the body musculature.Lernaeopodidae BiologyLemaeopodidae contains many genera and about 260 species. Lernaeopodids are foundthroughout the world’s oceans on teleosts and chondrichthyans. As a group they may infectall external surfaces of the host’s body, including the gills, spiracles, and olfactory sacs. Thesalmincolaforms are notable lernaeopodids because they are the most successfulsiphonostome, yet only lernaeopodid, taxon which has invaded fresh water. Each lineage26within Lernaeopodidae exhibits a fair degree of host specificity (see Yamaguti, 1963;Kabata, 1979, 1981).The habitus of postmetamorphosis lernaeopodid females consists of a cephalothorax andtrunk (Fig. 1). The cephalothorax may range from long (e.g. Clavella Oken, 1816, ClavellisaWilson, 1915) to almost nonexistent (e.g. Nectobrachia Fraser, 1920). Caudal rami andposterior fimbrate processes may be attached to the trunk (see Kabata, 1979). Egg sacs areusually allantoic in shape and contain round eggs multiseriately arranged. Crvptova Kabata,1992 is unusual within the family in possessing a brood chamber formed by a modificationof its posterior processes (Kabata, 1992). First antennae are uniramous. Second antennaeare biramous and usually have a large one-segmented exopod. Mandibles are typically shortand robust, and may exhibit both primary and secondary teeth. Second maxillae are theprincipal attachment appendages, and are usually elongated, fused at their tips, and insertedinto a structure known as the bulla. The bulla is implanted into the host, and along with thesecond maxillae serves an anchoring role. This scheme is modified a number of waysthroughout Lernaeopodidae (see Kabata, 1979), and a bulla does not always provide theultimate attachment. For example, in Dendrapta Kabata, 1964, Brianella Wilson, 1915, andSchistobrachia Kabata, 1964 the bulla is present in a vestigial condition. In these taxa, thebulla is only used during the initial attachment to the host. Afterwards, the buried tips of thesecond maxillae sprout luxuriant branches which permanently anchor the parasite (seeKabata and Cousens, 1972). Lernaeopodid maxillipeds are subchelate, and thoracic legs arevestigial or absent.The general habitus of lernaeopodid males is grub-like (Fig. 1). Overall, males are bestenvisaged as equivalent to their respective females prior to female metamorphosis (Fig. 1),and hence they are considered to represent a relatively primitive level of development. Inconsidering Lernaeopodidae, Kabata (1979) divided males into three groups. In the first27group males exhibit a cephalothorax and genitoabdomen, the lengths of which may or maynot be similar. In the second group males have highly reduced trunks which give them abulbous appearance. In the third group males are somewhat polytypic and relative to theother two groups they appear to be intermediate forms. The appendages of all three types ofmale are relatively homogeneous. First antennae are uniramous. Second antennae arebiramous. Mandibles, when known, are typically short and may exhibit both primary andsecondary teeth. Second maxillae and maxillipeds are subchelate. Thoracic legs arevestigial or absent.Life cycles are known for several species of Lemaeopodidae (e.g. see Zandt, 1935; Dedie,1940; Wilkes, 1966; Shotter, 1971; Kabata and Cousens, 1973; Kawatowj., 1980;Piasecki, 1989). In reviewing developmental programs of parasitic copepods, Kabata (1981)considered Lernaeopodidae to exhibit two types of life cycles. The first, exemplified bySalmincola californiensis Dana, 1852, possesses one nauplius stage that is passed through inthe egg, followed by an infective copepodid stage, four chalimus stages, an adult male, andan untransformed adult female which metamorphoses into a fully transformed adult (seeKabata and Cousens, 1973). In this scheme, molts only exist between nauplius, copepodid,chalimus, and adult stages. The transition between the untransformed adult female and thedefinitive adult female proceeds as a gradual metamorphosis. The second type oflernaeopodid life cycle proposed by Kabata (1981) is exemplified by the Clavella-branch ofLernaeopodidae, wherein (see Shotter, 1971) the free-swimming nauplius molts into aninfective copepodid which subsequently molts into a “pupa” (sensu Heegaard, 1947). Thefemale pupa (herein regarded as an untransformed adult) gradually metamorphoses into afully transfonned adult without molting, while the male pupa requires little noticeabledevelopment to be considered fully mature.28Recently, Piasecki (1989) has challenged Kabata’s (1981) view of two life cycles withinLemaeopodidae using two lines of reasoning. First, Piasecki (1989) considers Kabata (1981)to be in conflict with some reports of free-living nauplii in some Salmincola-typelernaeopodids. In particular, Piasecki (1989) cites Zandt’s (1935) report of two naupliusstages in . coregonorum (Kessler, 1868), stating that his own observations of this speciescorroborate Zandt’s. Kabata (1976) suggested that some observations of free-swimmingnauplii in Salmincola-type life cycles may have been made on larvae obtained underunnatural conditions. Piasecki (1989) reports his own observations of a very short-livednauplius stage which may rupture and release the copepodid stage simultaneously withrupture of the egg sac. Piasecki (1989) contends that perhaps the proportion of hatchingnauplii to “hatching” copepodids is variable, and that this proportion may shift dependingupon environmental factors. Secondly, as evidence of a transition between Kabata’s (1981)Salmincola- and Clavella-type life cycles, Piasecki (1989) cites a study by Kawatow .t i.(1980) which reports only three tethered chalimus stages in Alella macrotrachelus (Brian,1906), a member of a lernaeopodid lineage which according to Kabata (1981) should beexpected to exhibit four chalimus stages. Complete life cycles of other lernaeopodids areneeded to settle this issue, however, as discussed by Piasecki (1989), both Kabata’s (1981)and Piasecki’s (1989) ideas on lemaeopodids illustrate two apparent developmental trends.One is the abbreviation of the free-swimming nauplius stage, and the other is a shift fromecdysial growth (i.e. growth mainly achieved via the molting process) to interecdysialgrowth (i.e. growth mainly achieved without molting; sensu Piasecki, 1989). Both trendsseem to have some adaptive significance concerning the efficiency with which copepods caninfect active hosts such as fishes.The bulla which lernaeopodids implant in the host is formed during later chalimusdevelopment from the frontal organ which had formerly provided the frontal filament (seeKabata and Cousens, 1973; Piasecki, 1989). Throughout parasitic larval development and29into adulthood, the second maxillae join to the anchoring organ, thus tethering parasite to itshost. This system, therefore, is best regarded as the modification and incorporation of alarval characteristic into the adult life history. Direct attachment of the muscular andcontractile second maxillae to the bulla enables lernaeopodoids with short cephalocollums(i.e. the portion of the cephalothorax from the first antennae up to but not including thesecond maxilae; sensu Piasecki, 1989) to pull their mouth tubes to the host substrate. This isnot possible for the larval chalimus which often sways seemingly helpless at the end of along (see Benz, 1991) frontal filament. As noted by Kabata (1979), some lernaeopodidsincrease their feeding range via possession of an elongated cephalocollum (e.g. Clavella).The punctuated crawling style lernaeopodids use to move about during nontetheredchalimus existence, as well as during untransformed female and adult male periods differsfrom the swimming style of many other copepods. As discussed by Kabata and Cousens(1973) locomotion is accomplished by an inchworm-like motion which can be divided intothree phases. In phase I the cephalocollum stretches forward and is held to the host substrateby the hooks of the second antennae. In phase II the trunk loops forward, its caudal ramipinning it in place behind the maxillipeds. In phase ifi the cephalocollum contracts andmaxillipeds are released. This results in a forward shift of the second maxillae andmaxillipeds. When the second maxiflae reach a position close behind the buccal region, theirgrasp along with that of the maxillipeds is reapplied. Next the second antennae disengageand the copepod has now cycled back to its original stance. This method of movementprovides a strong stationary stance, secured to the host by both powerful second maxillae andmaxillipeds. The security this stance provides is important for the male during copulationand for the female when implanting the bulla. Crawling provides these copepods fairwandering ability which plays an important role in both mate location by the male andpermanent attachment location by the female (e.g. see Kabata and Cousens, 1973), and itpossibly has facilitated the radiation of lemaeopodids into new niches on their hosts.30Naobranchiidae BiologyNaobranchiidae contains one genus, Naobranchia Hesse, 1863 with 34 species. The generalhabitus and appendages of Naobranchia females are similar to those of lernaeopodids.Naobranchiids are unique, however, because they secure themselves to their hosts byencircling a gill filament with their enlongated, ribbon-like second maxillae (Fig. 8). Malenaobranchiids display the grub-like form characteristic of lernaeopodid males. Kabata(1992) has recently reported that males may occur in one of three basic forms differing in theplacement and orientation of the genitoabdomen on the trunk.Naobranchia has a cosmopolitan distribution and is found on a wide variety of teleosts(Yamaguti, 1963). Almost nothing is known about development in Naobranchiidae. Ovoideggs may be carried in multiseriate egg sacs or in brood sacs. A report by Wilson (1915) ofan incompletely metamorphosed Naobranchia iiz (Krøyer, 1863) ifiustrates the manner inwhich the band-like second maxillae develop. Apparently each second maxilla elongates andupon encircling a host gill filament the tips fuse with the trunk independent of one another tocomplete the unique belt-like holdfast.Tanypleuridae BiologyTanypleuridae contains one monotypic genus, Tanvpleurus Steenstrup and Lütken, 1861.Tanvpleurus attaches to its host using its short fused second maxillae which are highlybranched at their tips to form a holdfast. The cephalothorax is represented by a smalltubercle on the trunk. The trunk is wide, and wraps ventrally from each side to form thebulk of an unusual habitus. The first antennae are small uniramous appendages which bearsome general likeness to the first antennae of lernaopodids. The second antennae are31uniramous and seemingly highly modified. The first maxiliae appear reduced into smalluniramous structures armed with two apical setae that are constricted along their lengthsmuch like those seen within Lemaeopodidae. Maxillipeds are absent, as are all traces ofthoracic legs.Attached Tanvpleurus have only been reported from the gills of Eumicrotremus spinosus(Muller, 1777) (yclopteridae), Lvcodes reticulatus Reinhardt, 1838, and L. lavalaeiVladykov and Tremblay, 1936 (both Zoarcidae) in the North Atlantic (Kabata, 1969b,1988a). Kabata (1969b) references a report of two specimens taken from the stomach of aGreenland shark (Somniosus microceDhalus (Bloch and Schneider, 1801)), which hadprobably been swallowed along with their host. Although developmental data are unknownfor Tanypleuridae, the seemingly modified habitus of the ovigerous female suggests that ametamorphosis exists between an untransformed larval or young adult stage and the knownadult female form. Egg arrangement is multiseriate with egg sacs curling in a dorsaldirection and containing spherical eggs. Male tanypleurids have not been discovered.Dissonidae BiologyDissonidae contains one genus Dissonus Wilson, 1906 with 11 species (see Deets and Dojiri,1990). The dissonid cephalothorax incorporates the first pedigerous segment and is modifiedin the form of a dorsoventrally flattened shield. Along the anterior border of this shield are apair of flap-like frontal plates. Areas of the cephalothorax and frontal plates which contactthe host often have a thin marginal membrane which appears to assist in sealing thecephalothorax to the host substrate. Dissonids have the usual complement of siphonostomeappendages. The first antennae lie in close contact with the host. The claw-like secondantennae and subchelate maxillipeds are the primary attachment appendages. Legs one-four32are biramous and trimerous. The fifth and sixth legs are vestigial and are located on thegenital complex. Egg sacs are long and discoid eggs are uniseriately arranged. Disregardingthe genital complex, dissonid males appear very similar to females. Males, usually havelonger setae on their swimming legs and caudal rami than females, and these setae oftenappear to have denser arrays of setules.Dissonus species are parasitic on elasmobranchs and teleosts. Almost nothing is knownabout the ecology of Dissonidae. Some species have been reported from the gills of theirhosts, while others have been collected from the general body surface. In either case theexact location of infection has seldom been noted. Dissonus adults appear capable ofswimming, based on the well-developed setae of their natatory legs.Little is known about development in Dissonidae. According to Anderson and Rossiter(1969), Dissonus nudiventris Kabata, 1965 hatches as a relatively immobile nauplius whichremains attached to the ruptured egg sac by its elongated balancers. Dissonus nudiventrispossesses only one nauplius stage. This nauplius is unusual because it has unsegmented andunarmed first and second antennae, and mandibles. Anderson and Rossiter (1969) alsoreported no evidence of a frontal organ in what appears to have been the infective copepodidof ]2 nudiventris. It is notable that the present author has observed a frontal organ in adultfemale j.. spinifer Wilson, 1906 which perhaps indicates the former presence of a frontalfilament (see Anstensrud, 1990b; Piasecki and MacKinnon, 1993).Pandaridae BiologyPandaridae consists of 13 genera and 42 species. The only known synapomorphy for thefamily is the possession of distinctive maxillipeds with a squat corpus maxillipedis and a33distally displaced myxal region (Kabata, 1979). Except for the maxillipeds, the generalmorphology of pandarids is similar to that of dissonids and cecropids. Pandarids incorporatethe first pedigerous segment into the cephalothorax, with pedigerous segments two-foursequentially separate. Although some genera possess conspicuous corrugated adhesion padsand adhesion surfaces (Fig. 11) these structures are found outside of Pandaridae as well (e.g.see Kabata, 1966a; Benz and Deets, 1987, 1988; Benz, 1989; Deets and Benz, 1988; Deetsand Dojiri, 1989). A high degree of variation in both leg segmentation and leg armamentexists within the family. Seemingly primitive genera (e.g. Paging Cressey, 1964) tend tohave biramous, multimerous legs with long densely pinnate setae. More derived genera (e.g.Pandarus Leach, 1816) generally display fusion of ramus segments and spiniform setae.Variations in body form and leg structure among pandarids have prompted considerationthat perhaps Pandaridae is composed of two clades (Cressey, 1967; Kabata, 1979; Dojiri,1983). The Dinemoura-group (sensu Kabata, 1979) consists of species which have beenreported to exhibit a relatively narrow second free thoracic segment without dorsal or lateralplates, second maxillae with a crista (i.e. a patch of setules or denticles distally on thebrachium of the second maxilla), and relatively unmodified legs (see Cressey, 1967; Kabata,1979; Dojiri, 1983). The Pandarus-group (sensu Kabata, 1979) consists of species whichhave been reported to exhibit a more solid looking habitus with a wider second free thoracicsegment with lateral or dorsal plates, second maxillae with a distal clavus (i.e. a spine-likeprojection located distally on the brachium between the calamus and canna), and modifiedlamelliform legs (see Cressey, 1967; Kabata, 1979; Dojiri, 1983). Having examined 12 of13 pandarid genera this author does not support that Pandaridae is composed of two clades.First, the decision to characterize legs as unmodified versus lamelliform is a rather arbitraryone. For example, Cressey (1967) characterized the legs of Echthrogaleus Steenstrup andLütken, 1861 and Dinemoura Latreffle, 1829 as lamelliform even though they are membersof a group defined as possessing unmodified legs (see Cressey, 1967; Kabata, 1979; Dojiri,341983). Furthermore, some legs of Nessious Heller, 1868 are very similar to those ofPseudopandarus Kirtisinghe, 1950 even though these two genera reside in different groups(see Cressey, 1967; Kabata, 1979; Dojiri, 1983). The presence of a crista versus a clavusalso seems misleading. For one, this author has found pandarids with both crista and clavus(Fig. 12). Secondly, the clavus of some species appears to be composed of a twisted groupof cuticular fibers which could represent tightly whirled setules of a crista (Fig. 12). Theonly character which legitimately separates the Dinemoura and Pandarus groups is the formof the second free thoracic segment. Cressey (1967) noted that when interpretingmorphological features of pandarids, this family’s wide range of lifestyles has to beconsidered. This author concurs, and suggests that the morphological variation seen amongpandarid genera is graded and is functionally associated with a transition from more mobileto more sessile forms.Adult female pandarids are incapable of efficient swimming, and as noted by Wilson(1907b) they move in an uncoordinated fashion apparently seeking a holdfast when removedfrom their hosts and placed in aquaria. However, the males of many pandarid species areexcellent swimmers, and rival any caligid the present author has had opportunity to observe.Pandarids are considered exclusive parasites of elasmobranchs, although a few records ofindividuals taken from teleosts exist (e.g. see Kabata, 1979). Pandarids are relatively hostand infection site specific (see Benz, 1981, 1986; Rokicki and Bychawska, 1991), and aresometimes found in large clusters on their hosts (e.g. see Benz, 1981). The corrugatedsurfaces which these copepods often possess seem to allow them to match the fluted surfacesof the placoid scales of elasmobranchs, thus helping to secure them against the ceaselesswater flow encountered as parasites of such active hosts. The cephalothorax of at least somepandarids is rimmed with a row of ventrally directed spines (Fig. 13) which along with themarginal membrane must assist in attachment. Some species which inhabit relatively rough35regions of the host studded with prominent scales possess only the ventrally directed spines(Fig. 13).Pandarid second antennae are typically used as grapnels, and those of some species arecapable of becoming deeply embedded in the host (Fig. 14). Likewise, the chelatemaxillipeds can sometimes play a primary role in attachment, and in particular those ofPandarus species seem specifically designed to grasp the placoid scales of elasmobranchs(Fig. 15; see also Benz, 1992). Some pandarid species are capable of passive pernianentattachment not requiring energy to maintain a grip. For example, adult female Perissopusoblonatus (Wilson, 1908) embed their toothed second antennae (Fig. 16) between theplacoid scales and into the flesh of their shark hosts. Typically assuming a “handstand”position, it is difficult to understand how these copepods apply their mouth tubes to the hostsubstrate. Interestingly, adult females of the closely related E. dentatus Steenstrup andLütken, 1861 use their maxillipeds rather than second antennae as the primary organs ofattachment by permanently cementing the expansive planar surface of the myxal pad to hostplacoid scales (Fig. 17). Given that the second antennae and maxillipeds of oblongatusand E. dentatus are so similar (Cressey, 1967), it is unknown why these apparent sisterspecies have such dissimilar methods of attachment.Developmental records of pandarids are incomplete. Wilson (l907b) briefly discussed andfigured newly hatched nauplii of Pandarus and Nesippus apparently obtained from aquarium-held ovigerous females. Wilson (1907b) also described a Nesippus copepodid that had beenattached by its second antennae to a gill filament of an Atlantic sharpnose shark(Rhizoprionodon terraenovae (Richardson, 1836)), and further discussed and figured threechalimus stages of Perissopus dentatus collected from smooth dogfish (Mustelus canis(Mitchill, 1815)). Not only are these last reports noteworthy as the first authenticatedobservations of pandarid chalimus stages, but they also are important because they noted the36structure of the pandarid frontal filament. Wilson (1907b) detailed the frontal filament astwo broad flat parallel bands emanating from a quadripartite frontal organ. Wilson (1907b)further noted that each band was very short, and their attachment required the cephalothoraxof the chalimus to lie in close host contact. Since Wilson’s observations, some observershave reported pandarid frontal filaments (e.g. Shiino, 1963) while others have not (e.g.Lewis, 1964; Cressey, 1967, 1968). Most recently Benz and Last (in review) reported ashort, thin, double stranded frontal filament in Echthroaleus torpedinis Wilson, 1907. Thiscorroborated Wilson’s (1907b) observations of a multi-stranded tether in at least somepandarids, and it now seems likely that the short, thin pandarid frontal filament may be easilybroken or overlooked by researchers. The general inability to identify pandarid chalimusstages probably has hindered identification of preadults. However, it is possible that severaljuvenile pandarids reported by Shiino (1954) and Hewitt (1967) may have represented thesestages.Lewis (1964) made an interesting discovery of what appeared to be copepodid stages ofNesippus costatus Wilson, 1924 encysted in the fins of several teleost species. Normally,Nesippus adults are ectoparasitic on sharks, and as noted above, Wilson (1907b) reported aNesippus copepodid collected from a shark. The many observations of Lewis (1964),however, suggest that encysted costatus larvae did not represent unusual occurrences.The cysts surrounding these larvae were produced by the hosts and each had a small openingat one end through which the copepod’s caudal rami protruded. Lewis (1964) hypothesizedthat such a position would allow the encysted larvae to respire anally. Lewis (1964) foundevidence that molting occurred while larvae were encysted, but did not have enough studymaterial to be confident in assigning specific stages to the four larval morphs he examined.No frontal filament was seen in these larvae, however, a quadripartite frontal organ wasobserved. Further study of the life cycle of costatus seems desirable as it possibly37represents a two host life cycle known elsewhere among the siphonostomes parasitic onvertebrates only in Penneffidae.Cecropidae BiologyCecropidae consists of five genera: Luetkenia Claus, 1864 with two species, and monotypicCecrops Leach, 1816, Orthaoriscicola Poche, 1902, Phiorthaoriscus Horst, 1897, andEntepherus Bere, 1936. A synapomorphy for Cecropidae is unknown. Although the secondand third thoracic segments are fused in some cecropid species, this character is also seen insome pandarids (e.g. Echthroaleus). Like Dissonidae and Pandaridae only the first thoracicsegment is incorporated into the cephalothorax in Cecropidae. Except for the maxillipeds,cecropid appendages generally resemble those seen among pandarids. Adult femalececropids are massive copepods that can reach at least 3 cm in total length. Their large sizeand reduced leg setae suggest poor swimming ability, and according to Wilson (1907b) theyare relatively sessile on their hosts and somewhat uncoordinated when removed and placedin aquaria. The crypting and proliferation of host tissues often associated with cecropidinfections (e.g. see Scott, 1892; Wilson 1907b; Grabda, 1973; Benz and Deets, 1988)supports Wilson’s (1907b) remarks, as such pathologies require the presence of stationaryparasites. Male cecropids are also relatively heavyset in comparison to other siphonostomemales with dorsal shields (Fig. 1).Cecropids are parasitic on batoids and teleosts. The ocean sunfish (Mola mola (L., 1758))can harbor three cecropid genera which form a monophyletic group (see Benz and Deets,1988). Cosmopolitan j, mola and its cecropid parasites, therefore, become an interestingspecies pattern which could have formed by either parapatric or sympatric speciationprocesses. The confused records describing the exact location of these copepods on the38ocean sunfish, however, do not allow either speciation process to be favored (e.g. cf. Wilson,1907b and Wilson, 1932 concerning the distributions of Orthaoriscicola muricata (Krøyer,1837) and Phiorthaoriscus serratus (Krøyer,1863)). Benz and Deets (1988) noted that allcecropid hosts are epipelagic fishes, and it is possible that Cecropidae represents a taxon thatconstantly tests and periodically colonizes highly mobile oceanic hosts. Although nocomplete life cycle is known for Cecropidae, nauplius and chalimus stages have beenobserved (Wilson, 1907b; Grabda, 1973). The frontal filament of the chalimus is composedof two parallel bands (Wilson, 1907b; Grabda, 1973). Grabda (1973) observed that thechalimus of Cecrops latreilii Leach, 1816 uses its second antennae and maxillipeds inaddition to its frontal filament to secure its host.Trebiidae BiologyTrebiidae contains two genera: Trebius Krøyer, 1838 with 14 species, and monotypicKabataia Kazachenko, Korotaeva and Kurochkin, 1972. Trebiids are superficially similar toother siphonostomes with cephalothoracic shields, however, their overall body plan uniquelyconsists of a cephalothorax incorporating the first two pedigerous segments, followed by twofree pedigerous segments, a genital complex, and an abdomen. Trebiids, euryphorids, andcaligids share distinctive first maxillae whose rami are separated from one another. Theendopod forms a robust projection and the exopod is a small cuticular bump with one-threesetae. Kabataia differs from Trebius in possessing lateral plates on the first free pedigeroussegment and in lacking a sternal furca.Monotypic Kabataia is parasitic on teleosts while all 14 species of Trebius infectelasmobranchs (Kabata, 1979; Deets and Dojiri, 1989). Phylogenetic relationships withinTrebiidae have not been established, however, Deets and Dojiri (1989) recently grouped39some Trebius species using various morphological characters. Few developmental data existfor Trebiidae. A chalimus stage of I. caudatus Krøyer, 1838 and what possibly were thefirst and second preadult stages of I. exilis Wilson, 1906a have been reported by Wilson(1907a).Euryphoridae BiologyEuryphoridae contains five genera: Eurvphorus Edwards, 1840 with two species, GloiopotesSteenstrup and Lütken, 1861 with 5 species, Alebion Krøyer, 1863 with 8 species,Paralebion Wilson, 1911 with two species, and Tuxophorus Wilson, 1908 with six species.Euryphorids are generally similar to other siphonostomes that possess cephalothoracicshields. They share with trebiids and caligids a two piece first maxilla. Euryphorids haveonly one free thoracic segment between the cephalothorax and genital complex, with the firstthree pedigerous segments and their legs incorporated into the cephalothorax.A synapomorphy for Euryphoridae is unknown (see Dojiri, 1983). Kabata (1979)proposed the possession of paired dorsal aliform plates on the fourth leg-bearing segment offemale euryphorids as a familial marker. However, Dojiri (1983) speculated that the dorsalplates of euryphorids perhaps were adaptations which hydrodynamically streamline or assistthese copepods in attachment, and that their presence might be indicative of anenvironmental lifestyle rather than phylogeny. Dojiri (1983) further argued for the inclusionof euryphorid species within Caligidae based on the presence of aliform plates on the genitalcomplexes and abdomens of some Caligidae members, stating that the presence of aliformstructures should not carry any more taxonomic weight in one family versus another. Dojiri(1983) noted that the euryphorid Paralebion elongatus Wilson, 1911 does not exhibit welldefined dorsal aliform plates on its fourth pedigerous segment but rather slightly inflated40joints where the fourth legs meet the body. Therefore, Euryphoridae and Caligidae sharevariable character mixes and are difficult to delimit.The design of the cephalothorax and third pair of legs makes adult euryphorids capableswimmers and allows them to seal themselves to their hosts using suction (see discussionbelow). Euryphoridae has representatives infecting both sharks and teleosts, withEurvphorus seemingly preferring large scombrids, Gloiopotes seeking bilifishes, Alebion andParalebion infecting carcharhiniform sharks, and Tuxophorus parasitizing various nearshoreand oceanic teleosts (see Yamaguti, 1963; Kabata, 1979). Euryphorids are usually found onthe general body surface of their hosts. Some species parasitic on sharks exhibit very narrowniches as adults (Fig. 18).Developmental data are incomplete for Euryphoridae. Wilson (1907a) stated thateuryphorid nauplii are different from those of Caligidae regarding shape of the balancers (i.e.tapering in euryphorids and spatulate in caligids). However, Benz 1 J,. (1992) noted that thebalancers of the euryphorid Paralebion elongatus are spatulate in the first nauplius andtapering in the second nauplius. More importantly, Wilson (1907a) noted that a frontalfilament was lacking from attached copepodids of Alebion glaber Wilson, 1905. Instead,these larvae attached to their shark hosts using their powerful second antennae. Benz (1989)has corroborated Wilson’s (1907a) observations by finding no evidence of a frontal filamentin attached copepodids of lobatus Cressey, 1970 (see Fig. 19).Caligidae BiologyConsisting of at least two dozen genera and well over 300 species, Caligidae contains morespecies than any other siphonostome family. Like euryphorids, caligids have only one free41thoracic segment between the cephalothoracic shield and genital complex, with the first threethoracic segments and their legs incorporated into the cephalothorax. As discussed above, nosynapomorphy exists to separate caligids from euryphorids. The general habitus ofCaligidae, however, seems adequate for familial pigeonholing even though its membershipexhibits a diverse range of morphologies (see Kabata, 1979).The thoracic legs are relatively uniform throughout Caligidae (Kabata, 1979, 1988b).Although some adult female caligids seem to prefer a relatively sessile existence (Fig. 20),many observers have commented on this group’s swimming abilities. Kabata and Hewitt(1971) detailed the role of various appendages associated with caligid locomotion. The firstand second legs work together in antagonistic fashion to produce a propulsive thrust of waterwhich is expelled from under the cephalothorax through the posterior sinuses. Water isrecruited for locomotion from below the frontal plates in the anterior region of thecephalothorax. Dorsoventral flexion of the trailing portions of the body (genital complex,abdomen, and caudal rami) apparently are responsible for initiating dorsoventral movements.Kabata and Hewitt (1971) also described settling movements of caligids. Settlingmovements are important to copepods attempting to maximize attachment efficiency bylocating and securing an optimal resting site. The third pair of legs and their interpodal plateplay an important role in the process of settling and attachment because together they allowthe cephalothorax to be sealed to the host substrate. The second maxillae assist in crawlingand lateral body movements.Tines associated with the second antennae, postantennary processes, sternal furca, andswimming legs likely assist in anchoring caligids in the face of the forward-aft water flowassociated with a swimming host. In addition to these structures, some caligids possess apair of suctorial lunules which appear to be an elaboration of the marginal membrane42associated with the frontal plates (see Kabata, 1979). The lunules seem to provide theanterior portion of the cephalothorax a means of attachment which might assist the copepodwhen it releases suction from beneath its cephalothorax and actively skitters over its host.Caligids use a structure known as the strigil to rasp free bits of host tissue to be conveyeddeeper into the mouth tube by the mandibles (Kabata, 1974a). To date the strigil has onlybeen identified from Caligidae and some members of Euryphoridae (see Kabata, 1979;Dojiri, 1983; Benz nj., 1992).Although caligids have some representatives infecting elasmobranchs (see Yamaguti,1963) and invertebrates (see Ho, 1980; Ruangpan and Kabata, 1984), they are predominantlyparasites of teleosts, and like most siphonostomes they exhibit a fair degree of hostspecificity (see Yamaguti, 1963; Kabata, 1979). Caligids can be found virtually anywhereover the general body surface of potential hosts (olfactory, buccal, and branchial cavitiesincluded), and upon close study particular species are often seen to be relatively specificconcerning infection site of the adult female (Fig. 20; see also Anstensrud, 1990c, 1990a).Because caligids cause disease on schooling fishes of considerable commercial importance(see Wootten n.j., 1982; Roth nj., 1993) it is not surprising that their life cycles are betterunderstood than those of other siphonostomes possessing dorsal shields. Within Caligidae,four species of Lepeophtheirus von Nordmann, 1832 (see Lewis, 1963; Voth, 1972;Boxshafl, 1974b; Johnson and Aibright, 1991a) and seven species of Ca1ius MUller, 1785(see Gurney, 1934; Heegaard, 1947; Hwa, 1965; Izawa, 1969; Kabata, 1972; Caillet, 1979;Ben Hassine, 1983) have had all or most of their developmental stages identified. Thesestudies, along with numerous others less completely detailing development, depict a standardlife cycle for Caligidae consisting of ten stages: free swimming nauplius 1 and 2, infectivecopepodid, chalimus 1-4, preadult 1 and 2, and adult.43Like all chalimus stages, those of Caligidae are tethered to their hosts by a frontal filamentextruded from a frontal organ. Several reports of caligid preadult stages attached by a frontalfilament have conflicted with a majority of others depicting preadult and adult stages as freeranging (e.g. see Lewis, 1963; Kabata, 1972, 1981; Anstensrud, 1990b; Johnson andAibright, 1991a). Recently, however, Anstensrud (1990b) observed that just prior tomolting, the preadult produced a frontal filament which tethered it throughout the process ofecdysis. Soon after molting, once the new cuticle had hardened, the frontal filament wasbroken and prehension was facilitated by typical adult mechanisms (Anstensrud, 1990b).Anstensrud (1990b) observed that in Lepeophtheirus pectoralis (Muller, 1777) the preadultfrontal filament was composed of two very thin twisted strands. These strands arose from afrontal organ formerly considered to have a chemosensory function (Kabata, 1981), orpossibly no function at all (Oldewage and Van As, 1989). Anstensrud (1990b) stated thatgiven the brief existence and fragile nature of these frontal filaments it is understandable whythey have not often been observed. Perhaps the presence of the rugose frontal organ can beused to predict the former or future presence of frontal filaments.SIPHONOSTOME RELATIONSHIPSAnalysis of the 18 siphonostome families parasitic on vertebrates resulted in one mostparsimonious cladogram supported by 30 characters (Fig. 21 and Table 1). This phylogenywas based on the concept that the siphonostome families parasitic on vertebrates form anatural (i.e. monophyletic) group. Important (but not essential) to this concept are the ideasthat Siphonostomatoida is monophyletic, and that the siphonostomes parasitic on vertebrates44were derived from the siphonostomes of invertebrates. These topics will be discussed brieflybefore the phylogeny for the siphonostomes parasitic on vertebrates is detailed.Monophyletic SiphonostomatoidaThorell (1859) proposed a classification for copepods that grouped taxa independent ofecological characteristics (i.e. free-living versus parasitic). This classification was importantto the study of Copepoda, for without pretension founded upon ecological pigeonholing,subsequent phylogenetic analyses based on morphological and anatomical characters suggesta multiple origin of parasitism as a copepod lifestyle (see Bocquet and Stock, 1963; Kabata,1979; Ho, 1990; Huys and Boxshall, 1991; Stock, 1991).Recently none have seriously challenged the monophyly of Siphonostomatoida (seeKabata, 1979; Huys and Boxshall, 1991; Stock, 1991). Marcotte (1982) argued, albeit verytentatively, for at least a diphyletic Siphonostomatoida based on general differences in theoral cone between siphonostomes associated with invertebrates and those parasitic onvertebrates, as well as on body segmentation and several appendage characteristics.However, these differences were not explicitly explained, and no consideration was given tothe possibility that evolution within the order had produced the taxonomic diversity observedtoday. Such shortcomings render Marcotte’s (1982) di- or polyphyletic Siphonostomatoidahighly speculative and founded solely on the vast and often confusing variation among thesecopepods. In fact, as set forth by Thorell (1859), membership within the order is bestdemonstrated by the possession of a tubular mouth (oral cone) composed of anterior andposterior lips (respectively the labrum and labium) and containing styliform mandibles (Fig.22).45Monophyly of Siphonostomes Parasitic on VertebratesInterfamilial relationships among siphonostomes are ill-defined (see Huys and Boxshail,1991). Progress in defining these relationships has been hindered by a relative lack ofknowledge about the siphonostomes associated with invertebrates, and by the difficult tointerpret diversity of the siphonostomes parasitic on vertebrates. However, becausesiphonostome families are almost always exclusively associated with either invertebrate orvertebrate hosts it has generally been assumed that siphonostomes parasitic on vertebratesmight form a derived and monophyletic group (see Huys and Boxshall, 1991). Huys andBoxshall (1991) characterized this lineage by a number of features, none of which are bothexclusive to and universally possessed throughout the group.The lack of any clear synapomorphy unifying siphonostome families parasitic onvertebrates has periodically prompted discussions of polyphyly (Kabata, 1979; Cressey andBoxshall, 1989). Kabata (1979), for example, briefly considered the ectoparasiticsiphonostomes of fishes to perhaps have been derived from siphonostome associates ofinvertebrates exhibiting depressed cephalothoraxes and podoplean design (i.e. forms inwhich the main body articulation exists between the fourth and fifth pedigerous somites).However, Kabata (1979) did not mention the possible origins of fish-parasitic families suchas Eudactylinidae, Kroyeriidae, Hatschekiidae, Pseudocycnidae, Dichelesthiidae,Hyponeoidae, and Lernanthropidae, all of which are not markedly depressed dorsoventrallyand yet which seem in many respects to be relatively primitive among the siphonostomesparasitic on vertebrates. Kabata (1979) suggested that Pennellidae might have arisen fromMegapontiidae-lilce ancestors based on the presence in these families of a peculiar mouthcone. However, recent comparative studies of the siphonostome oral cone (Boxshall, 1990)46reveal the mouth tube of Megapontildae to differ fundamentally from that of Penneffidae,although one possibly could speculate on the evolution of the latter from the former.The idea that siphonostomes parasitic on vertebrates form a monophyletic group isendorsed in this thesis based on four characters. The first character (character 1 of Table 1and Fig. 21) unifying the siphonostomes parasitic on vertebrates is the presence of aprominent row of teeth along one side of the mandible (e.g. see Fig. 22). The mandibles ofsiphonostomes associated with invertebrates often have very small teeth and/or teeth whichappear in a short row at the mandible’s apex. This characteristic is not clear-cut. Somesiphonostomes parasitic on vertebrates belonging to highly modified families possessmandibles with seemingly reduced dentition (e.g. some Pennellidae), or may even lackmandibles (e.g. some Sphyrlidae). Antithetically, some siphonostomes associated withinvertebrates possess relatively Stout mandibles with somewhat larger teeth that appearconcentrated on one side of the apex (e.g. Dirivultidae).The second character unifying the siphonostomes parasitic on vertebrates is the presence ofsecond antennae lacking exopods (character 2 of Table 1 and Fig. 21). This character also isnot clear-cut. The one-segmented exopod characteristic of the siphonostomes associatedwith invertebrates may be small or virtually absent (as in Dirivultidae and Dinopontiidaerespectively), or sometimes completely absent (e.g. Nanaspididae, Nicothoidae andMicropontiidae). To the contrary, the closely allied families Sphyriidae, Lemaeopodidae,and Naobranchlidae (all parasitic on fishes) possess second antennae with well-developedone-segmented exopods. These second antennae, however, appear to function in bothimportant sensory and attachment roles associated with the highly modified larval and adultlifestyle characteristic of these copepods (Kabata, 1979). This functional reliance on thesecond antennae might be responsible for the maintenance or evolution of this character.47The third character unifying the siphonostomes parasitic on vertebrates is the possession ofrelatively long uniseriate egg sacs (character 3 of Table 1 and Fig. 21). This characteristic isalso not clear-cut, with Jushevus (Eudactylinidae), Sphyrildae, Lernaeopodidae,Naobranchiidae, and Tanypleuridae displaying multiseriate or otherwise modified eggs sacs.As discussed below, the multiseriate egg sacs seen among the siphonostome associates ofinvertebrates and the above mentioned taxa are probably nonhomologous.The last character unifying the siphonostomes parasitic on vertebrates is the absence of themandibular palp (character 4 of Table 1 and Fig. 21). This absence is considerd a loss and,therefore, implies that the siphonostomes parasitic on vertebrates were derived fromsiphonostomes associated with invertebrates. Huys and Boxshall (1991) considered theabsence of a mandibular palp to be the most robust character separating the siphonostomesparasitic on vertebrates from those associated with invertebrates. However, this character ishardly clear-cut and actually appears to be the weakest of the four characters presentedherein separating the two groups. Although the absence of a mandibular paip is acharacteristic shared by all siphonostome families parasitic on vertebrates, it is also absent onmany siphonostome families associated with invertebrates (e.g. Brychiopontiidae,Calverocheridae, Cancerillidae, Dinopontiidae, Dirivultidae, Dyspontiidae, Ecbathyriontidae,Entomolepidae, Megapontiidae, Myzopontildae, Nanaspididae, Nicothoidae, Saccopsidae,Spongiocnizontidae, and Stellicomitidae). It is not known whether this commonalityrepresents convergence or homology among these taxa and the siphonostomes parasitic onvertebrates.48Interfaniilial Relationships Among Siphonostomes Parasitic on VertebratesAlthough cladistic analysis of the 18 families of siphonostomes parasitic on vertebrates didnot fully resolve the phylogenetic relationships among these taxa, several well-defmedlineages were identifed (Fig. 21) along with a general trend indicating the evolution ofmorphological characteristics which seem to increase the efficiency of attachment and insome cases open new niches.Eudactylinidae has generally been considered the most primitive siphonostome familyparasitic on vertebrates (Kabata, 1981; Huys and Boxshall, 1991). In this thesisEudactylinidae’s primitive status is based on its members possessing fifth thoracic legs whichare free from the genital somite (see characterS of Table 1 and Fig. 21). Because thischaracteristic is shared with many siphonostome associates of invertebrates it is asympleisiomorphy rather than a synapomorphy considering the cladogram. Althoughvirtually all published considerations of the evolutionary position of Eudactylinidae mentionthe importance of a free fifth thoracic segment as a primitive characteristic (e.g. see Kabata,1979; Deets and Ho, 1988; Huys and Boxshall, 1991), it should be noted that the formationof a genital complex may have independently occurred more than once among thesiphonostomes infecting vertebrates and that endorsement of such a parallelism could placeEudactylinidae in an unresolved relationship with other relatively underived taxa (see Fig.21).Although some members of Eudactylinidae exhibit other seemingly primitivecharacteristics such as geniculate condition of the male first antennae (see Huys andBoxshall, 1991), these characteristics are possessed by only a few species within the familyand, therefore, they were not chosen for inclusion in this dissertation’s phylogenetic analysis.The multiseriate egg sacs of Jushevus are considered a reversal within Eudactylinidae from49the uniseriate condition used to help delimit the siphonostomes parasitic on vertebrates(character 3 of Table 1 and Fig. 21).Progressing up the cladogram, Kroyeriidae is set apart from surrounding taxa by its chelatesecond antennae (character 6 of Table 1 and Fig. 21), a homoplastic character shared withPenneffidae and Pseudohatschekia. Kroyeriidae is further separated from Eudactylinidaebased on its fifth legs being incorporated into a genital complex (character 5 of Table 1 andFig. 21). Kroyeriidae is delimited from families Hatschekiidae, Pseudocycnidae,Hyponeoidae, Lemanthropidae, and Dichelesthiidae based on its unmodified fourth legswhich are connected by well-developed interpodal bars and which are located on welldefmed free thoracic segments (see character 7 of Table 1 and Fig. 21). Kroyeriidae isdelimited from taxa further up the cladogram by its lack of a frontal organ associated with alarval frontal filament (see charater 12 of Table 1 and Fig.21) and by its relatively highlysegmented first antennae (see character 13 of Table 1 and Fig. 21). It should be noted thatvirtually nothing is known about the development of kroyeriids and that the absence of afrontal organ is based on examinations of adults rather than larvae.Together, families Hatschekiidae, Pseudocycnidae, Hyponeoidae, Lernanthropidae, andDichelesthiidae form the dichelesthiiform assemblage (see Fig. 21). These five families aregrouped together based on their possessing fourth thoracic legs which are highly modified orcompletely lost (character 7 of Table 1 and Fig. 21). A superficially similar characteristic isseen within the highly derived lemaeopodiform lineage (i.e. Sphyriidae, Lernaeopodidae,Naobranchiidae, and Tanypleuridae) in that all thoracic legs of lernaeopdiforms are vestigial(see character 16 of Table 1). Because dichelesthiiforms and lernaeopodiformsmorphologically appear so distinct and because reduction in leg segmentation is aphenomenon seen within a number of siphonostome lineages, this similarity is notconsidered a homoplasy, but rather two distinct characters. It should be noted that the fossil50dichelesthiid Kabatarina possesses four pairs of possibly unmodified biramous legs (seeCressey and Boxshall, 1989), and that its inclusion in the cladogram as a dichelesthild mightrequire some to consider character 7 more exclusive, resulting in Dichelesthiidae droppinginto a more immediate association with Kroyeriidae. This convention has not been followedfor two reasons. First, the relationship of Kabatarina to other dichelesthiids is questionablybased on only one fine characteristic (a groove on the second maxilla delimiting the distalportion of the brachium from the calamus; see Cressey and Boxshall, 1989). Of course thetransfer of Kabatarina into some other family would only serve to alter which family wouldfall into closer relationship with Kroyeriidae. More importantly, the leg segmentation ofKabatarina is somewhat uncertain (see Cressey and Boxshall, 1989) and it seems verypossible that it may represent a reduction from the biramous, trimerous condition seen inKroyeriidae. This author would like to make notice of the four pairs of swimming legspossessed by all kroyeriids as being primitive and notably different from the conditions seenamong families Hatschekiidae, Pseudocycnidae, Hyponeoidae, Lernanthropidae, andDichelesthiidae, and yet similar to that seen among untransformed pennellids and caligiforms(i.e. Dissonidae, Pandaridae, Cecropidae, Trebiidae, Euryphoridae, and Caligidae). Thisprimitive condition is also shared with underived eudactylinid genera such as Protodactylinaand Bariaka (see Deets and Ho, 1988) and is considered a sympleisiomorphy in this analysis.It certainly is possible, however, that a trend defined as the reduction of the first four pairs oflegs from a biramous, trimerous, setose state with left and right pairs connected by well-developed interpodal bars may have occurred more than once among these families. If thiswere so concerning the entire dichelesthiiform assemblage then character 7 would have to beabandoned and the polytomy that it supported would then additionally include Kroyeriidae(see Fig. 21).Dichelesthiiforms are also separated from Pennellidae and other taxa further up thecladogram (i.e. caligiforms and lernaeopodiforms) by lacking a frontal organ associated with51the larval frontal filament (see character 12 of Table 1 and Fig. 21) and by generally havingfirst antennae with a relatively high number of segments (see character 13 of Table 1 andFig. 21). This last character is not clear cut, as among some seemingly modifieddichelesthilforms the segmentation of the first antennae may be indistinct (see Kabata, 1979).It should also be remembered that developmental information is almost completely lackingfor dichelesthiiforms, with only one complete life cycle being known (Cabral, 1983). Thediscovery of a dichelesthiiform frontal organ or frontal filament would require re-evaluationof the phyletic position of its owner’s family.Within the dichelesthiiform assemblage parallelism and convergence are thought to becommon, especially as they concern trends in body tagmosis in which thoracic segments areincorporated into the genital complex, and the reduction of the thoracic legs (see Kabata,1979). Among dichelesthilforms, shared primitive characteristics are also thought to becommon, mainly involving the general shape of the body (subcircular in cross section), andthe structure of the cephalothoracic appendages (see Kabata, 1979; Ho, 1987; Cressey andBoxshall, 1989). Certainly the comparison of the fossil Kabatarina to other dichelesthiiformsstrengthens these ideas (see Cressey and Boxshall, 1989). However, as the only fossilcopepod, j pattersoni unfortunately is somewhat of a red herring regarding its ability tohelp define interfamilial relationships. Because of the above and the fact that a strongsynapomorphy defining the entire assemblage is unknown, Kabata (1979) independentlyconsidered these families.Based on the superficial morphology of some dichelesthiiform species (i.e. general habitusand structure of thoracic legs), Hatschekiidae and Pseudocycnidae might be interpreted asprimitive and closely allied. In fact, the general habitus of some hatschekiids andpseudocycnids is quite similar to that of kroyeriids, and characteristics such as the cuticularflaps and spines on the legs of some hatschekiids seem to further suggest some loose52affiliation with eudactylinids. Using similar criteria, a more derived alliance betweenHyponeoidae, Lernanthropidae, and Dichelesthiidae, might be considered. Suchobservations would structure the dichelestiiform assemblage so that Hatschekildae andPseudocycnidae appear primitive while Hyponeoidae, Lernanthropidae, and Dichelesthiidaewould seem relatively derived. Ecologically this pattern would suggest a shift fromrelatively more mobile to more sessile forms. However, this scheme cannot be consideredrobust because its promotion requires the use of many ad hoc conventions.Pennellidae is separated from taxa further below on the cladogram and united withcaligiforms and lernaeopodiforms based on the two previously mentioned characters 12 and13 (Table 1 and Fig. 21). It should be noted that character 12 (possession of a frontal organand use of a frontal filament during larval development) is a complex character. Althoughthis character has not been weighted on the cladogram, further examination would probablysubstantiate its division into several distinct yet related characters.The general similarity of the overall body segmentation of adult male and untransformedadult female pennellids with adults of both Dissonidae and especially Kroyeriidae are notablesympleisiomorphies. Even more striking is the similarity between the overall habitus of themesoparasitic kroyeriid Kroyeria caseyi (see Benz and Deets, 1986) and partiallytransformed pennellid females (e.g. see Kabata, 1979: Figs 1342 and 1416). Theconvergence of these forms seems based on both a combination of plesiomorphic traits andsuperficial similarities associated with a mesoparasitic lifestyle. As mentioned above,pennellids also share with kroyeriids chelate second antennae (character 6 of Table 1 andFig. 21). This character is considered homoplasious, a determination that is furthersupported if character 12 was reconsidered as discussed above. Lastly, pennellid females,hatschekild males and females, and tanypleurids lack maxilhipeds. This absence is53considered a loss of this appendage and is shared between these taxa through homoplasy(character 9 of Table 1 and Fig. 21).Concerning the relationship of Penneffidae to the caligiform and lernaeopodiform lineages,the pennellid chalimus appears much like that of caligiforms. However, this form appearsrelatively underived based on the general segmentation of its body and appendages and,therefore, must be considered plesiomorphic and incapable of resolving affmities.The lemaeopodiform lineage is united by four characters (see Fig. 21). The first is thepossession of second antennae with prominent exopods. As discussed above, thischaracteristic appears to be a reversal, and is similarly shared with some siphonostomesassociated with invertebrates (see character 2 of Table 1 and Fig. 21).The second character uniting lernaeopodiforms is the possession of multiseriate eggarrangement (character 15 of Table 1 and Fig. 21). This trait is shared with thesiphonostome associates of invertebrates and most likely represents a distinct character statefrom an evolutionary perspective. This conclusion is based on the observations that withinEudactylinidae, Jushevus has seemingly reverted to a multiseriate egg arrangement, and thatwithin Lernaeopodidae, Clavellistes lampri (Scott and Scott, 1913) apparently represents aswitch from a multiseriate to a uniseriate egg arrangement (see Kabata, 1979; Deets andBenz, 1987; Deets and Ho, 1988).The third character uniting lemaeopodiforms is that all thoracic legs are modified intovestigial structures or are completely lost (character 16 of Table 1 and Fig. 21). Thehomoplastic relationship of this character to the reduction of the highly modified fourth legsof dichelesthiiform members has been discussed above.54The most notable character unifying the lernaeopodiform lineage is the possession of ahighly modified grub-like male and untransformed adult female (character 17 of Table 1 andFig. 21). This character is a powerful synapomorphy which has not been weighted on thecladogram, but which could be divided into several distinct yet related characters.Families Lemaeopodidae, Naobranchiidae, and Tanypleuridae are united and separatedfrom Sphyriidae based on the second maxillae being highly modified and serving as theprimary attachment appendages of the fully transformed adult female (character 18 of Table1 and Fig. 21). Although transformed female sphyriids are mesoparasitic, it is interesting tonote the long second maxillae of Norkus (see Dojiri and Deets, 1988) which give theimpression that lemaeopodiforms may have been ancestrally united by expansive femalesecond maxillae or the genetic ability to develop them.Relationships among L.ernaeopodidae, Naobranchiidae, and Tanypleuridae appearunresolved (see Fig. 21). Based on the work of Kabata (1966b, 1979, 1981; Kabata andCousens, 1972), phylogenetic relationships within Lernaeopodidae depict this large family tobe composed of five lineages (salmincolaforms, lernaeopodaforms, brachiellaforms,charopiniforms, and clavellaforms). The morphological diversity of transformed femalelernaeopodids along with the lack of thorough descriptions of the systematically importantadult males renders lernaeopodid phylogeny a difficult hypothesis to construct (e.g. seeKabata, 1979, 1990; Ho and Do, 1984). The inclusion of Naobranchiidae and Tanypleuridaeinto this conundrum further complicates matters.Kabata (1979) reviewed the history of Naobranchia from its inclusion by Wilson (1915) inL.emaeopodidae (subfamily Claveffinae) to its transfer by Yamaguti (1939) as sole memberof Naobranchiidae. Given current theory of Lernaeopodidae phylogeny, Naobranchia doesnot appear to exhibit any derived characteristics warranting independent familial status (Fig.5521). As recently noted by Kabata (1992) Naobranchia displays three basic types of males.Two types seem quite similar to lernaeopodid males, and possibly indicate parallel evolutionbetween the males of these two families. The typical adult female Naobranchia firstantennae seem easily acceptable as reduced lernaeopodiform antennae. The longNaobranchia cephalocollum is clavellaform. The distinctive band-like Naobranchia secondmaxillae which fuse with the thorax without hint of a bulla (character 20 of Table 1 and Fig.21), appear too easily derived from within Lernaeopodidae to endorse distinct familial status.Lastly, the unusual brood sacs of some naobranchilds seem easily derived from somelernaeopodid ancestor. To support this, the brachiellaform lemaeopodid Crvptova Kabata,1992 is noted as possessing brood chambers (see Kabata, 1992). Therefore, it appears thatNaobranchia can be accommodated in Lernaeopodidae as a close relative of clavellaforms orbrachiellaforms, and future studies should consider more thoroughly the suppression ofNaobranchiidae.Tanypleuridae, erected by Kabata (1969b) to hold Tanvpleurus alcicornis Steenstrup andLUtken, 1861, likewise, seems closely related to Lemaeopodidae. Steenstrup and LUtken(1861) recognized similarity between Tanvpleurus, Lernaeopoda Blainville, 1822, andAnchorella Cuvier, 1830 (=Clavella) in that these genera all use the second maxillae asprincipal attachment organs. Although Wilson (1920) also noted possible affinities betweenTanvpleurus and Lernaeopodidae, through misfortune Tanvpleurus eventually came to residewithin the poediostomatoid family Chondracanthidae (see Kabata, 1969b). In redescribingTanvpleurus, Kabata (1969b) reaffirmed siphonostome status for the genus and noted itsaffinity with Lernaeopodidae and Naobranchiidae. In particular, Kabata (1969b) comparedthe dendritic holdfast of Dendrapta (Lernaeopodidae) with that of Tanvpleurus. However,based on the structure of both the second antennae and first maxillae, and on the lack ofmaxillipeds, Kabata (1969b) erected Tanypleuridae to accommodate the species.56Considering this matter the present author notices that as illustrated by Kabata (1969b) theuniramous second antenna of Tanypleurus possibly represents the endopod remnant of atypical Lernaeopodidae structure. To support this possibility, Clavella stellata (Krøyer,1838) is noted as having an almost uniramous second antenna composed mainly of endopod(see Kabata, 1979). Kabata (1969b) stated that the first maxilla of Tanvpleurus resembledthat of Lernaeoceridae more than that of Lernaeopodidae. The present author, however,contends that the Tanvpleurus first maxila as illustrated by Kabata (1969b) represents theendopod remnants of a lernaeopodid structure. To legitimize this claim it can be noted thatterminal setae present on the endopods of the first maxillae of Lernaeopodidae typically arenaked cylindrical papihiform setae which taper abruptly at some point along their lengths(see Kabata, 1979). Setae of the Tanvpleurus first maxilla illustrated and described byKabata (1969b) exhibit this form, however, those of Pennellidae (=Lernaeoceridae) do not(see Kabata, 1979). Further supporting this argument, there appears to be a tendency withinLemaeopodidae for reduction of the first maxilla into a uniramous condition displayingmainly an endopod with two lernaeopodid-type setae (e.g. see Kabata, 1979). Kabata’s(1969b) mention of Tanvpleurus lacking maxillipeds certainly denotes a regressive condition(shared with hatschekiids and pennellid females) and does not warrant independent familialstatus. In fact, within Lernaeopodidae at least one genus, Tracheliastes Nordmann, 1832,exhibits vestigial maxillipeds. In light of the above and giving special consideration tosimilarity between the holdfasts of Tanvpleurus and Dendrapta as noted by Kabata (1969b),the present author feels that it will take the discovery of a truly atypical lernaeopodid malefor Tanvpleurus to maintain familial status outside of Lernaeopodidae.As discussed above, caligiforms share with pennellids and lemaeopodiforms a frontalorgan which produces a frontal filament used during development (character 12 of Table 1and Fig. 21), and a marked reduction in the segmentation of the first antennae (character 13of Table 1 and Fig. 21). Although a frontal filament has not yet been observed in three57caligiform families, either it or a frontal organ has been seen in all six families (e.g.Caligidae (see Kabata, 1974b, 1981; Cressey and Cressey, 1979), Euryphoridae (see Benz 1]., 1992), Trebiidae (Benz, unpublished observations), Cecropidae, (see Grabda, 1973),Pandaridae (Fig. 23; also see Benz and Last, in review), and Dissonidae (Benz, unpublishedobservations). The caligiform lineage, therefore, is tentatively considered to primitivelypossess a frontal ifiament based on the existence of a frontal organ as evidence of itspresence (see Anstensrud, 1990b; Piasecki and MacKinnon, 1993). While the frontalfilament of some caligiforms is hard to detect and may easily be overlooked, it is possiblethat different ecological constraints may have altered its form or presence within this lineage.Caligiforms are united by three characters which all represent modifications of thecephalothorax. The first of these is the possession of a relatively large cephalothorax(minimally containing the first pair of thoracic legs) which is dorsoventrally flattened andwhose ventral surface is concave (character 21 of Table 1 and Fig. 21). This distinctivecephalothorax, known as the dorsal or cephalothoracic shield, is primitively divided intoanterior and lateral regions by cuticular thickenings not necessarily associated with thedemarcation of true body segments (Parker nj., 1968; Boxshall, 1974a; Kabata, 1979).Although this shield is well-developed in caligiforms, some siphonostome associates ofinvertebrates possess cephalothoraxes that appear somewhat similarly flattened, although lesspronounced and lacking well-defined lateral regions (e.g. Dirivultus Humes and Dojiri,1980).The second character unifying the caligiform lineage is the possession of two thin cuticularflaps, known as frontal plates, attached one on each side of the midline along the anterioraspect of the dorsal shield (character 22 of Table 1 and Fig. 21). Frontal plates are not seenon siphonostomes other than caligiforms.58The third character unifying caligiforms is the possession of a unique type of first maxifiawhich primitively is biramous, with a relatively large dentiform endopod and a small exopodapically bearing three small spiniform setae (character 23 of Table 1 and Fig. 21).Four structures (sternal projections, postantennary processes, postoral processes, andelytra) which are widely but not universally found among caligiforms were not included inthe phylogeny because their exact relationships to one another are ill-defined. Nonetheless, abrief discussion of each will serve to summarize current understanding of these potentiallysynapomorphic features.Various types of sternal projections are possessed by caligiforms. The most familiar ofthese is the sternal furca of some trebiids, euryphoriids, and caligids (see Kabata, 1979). Thesternal furca is a posteroventrally aimed medial projection between the maxillipeds and firstthoracic legs which may be flexible or immovable (Fig. 24. As noted by Kabata (1981), thenecessity of this furca is open to debate, as it is not universally possessed among caligiforms,and species lacking it are not noticeably affected by its absence. Several authors havesuggested that application of the furca to the host substrate may provide a brake against thetypical forward-aft water flow continually pressuring many caligiforms (Wilson, 1905;Gnanamuthu, 1948; Lewis, 1966b; Kabata and Hewitt, 1971).Lewis (1966b) argued that the sternal furca possibly represents either a remnant of styletbearing interpodal bars (as seen in Kroveria: Kroyeriidae) or stylet issuing interpedigerousplates (as in seen male Nesippus borealis (Steenstrup and Lütken, 1861): Pandaridae). Ineither instance the furca furnishing plate appears to have been associated with themaxillipeds. Systematic rearrangement since Lewis’s (1966b) report makes the idea thatKroyeria possesses a possible precursor of this furca even more interesting. Also interestingis Lewis’s (1966b) observation that male Paeon (Sphyriidae) possess second maxillae and59maxillipeds which are paired along the midline in an unclear manner relative to the form ofsternal projections. As further noted by Lewis (1966b) the medial sternal stylet of thepandarid Demoleus heDtapus (Otto, 1821) bears striking resemblance to the sternal furcae oftrebiids, euryphorids, and caligids (Fig. 24). Kabata (1965, 1966a) has provided descriptionof both a sternal furca and sternal stylet in Dissonus. These observations leave onlyCecropidae, seemingly well-embedded within the caligiform lineage, lacking at least onerepresentative with some form of sternal projection.The postantennary processes are paired cuticular projections shared by many caligiformswhich are also of unresolved origin (see Lewis, 1969; Kabata, 1979, 1981). Theseprojections are found ventrally on the cephalothorax posterolateral to the second antennae ofsome pandarids, trebiids, euryphorids, and caligids. These processes may exist as corrugatedadhesion pads (e.g. Pandarus and Alebion) or as tine-like structures (e.g. Trebius,Gloiopotes, and Caligus). Three groups of setules are associated with the postantennaryprocesses, and the presence of these setules is known from other caligiforms not displayingthe cuticular postantennary processes (e.g. Dissonus).The postoral processes are paired cuticular projections located posterolateral to the mouthtube which are shared by many caligiforms. Like the postantennary processes, the posturalprocesses exist as corrugated pads (e.g. Pandarus and Alebion) or as tine-like structures (e.g.Gloiopotes). The postoral processes represent a modified element of the first maxilla(Lewis, 1969; Kabata, 1979). Along with the postantennary processes, they serve to prop theventral aspect of the cephalothorax against the host substrate. Generally, species whichreside on the placoid scales of elasmobranchs have a greater tendency to possess processeswith corrugated surfaces while species residing on teleosts exhibit tine-like projections.60Many caligiforms also possess dorsal, ventral, and/or lateral elytra (often referred to asplates). While some pandarids possess plate-like structures associated with the abdomen,most caligiform elytra are associated with the thoracic segments. These outgrowths exhibitbilateral symmetry and are sometimes fused along the midline to form a single shield (e.g.plates associated with the third and fourth pedigerous segments of Pandarus species). Kabata(1979) considered the caligid dorsal shield to be partially formed by the fusion of severalsuch plates. Comparison of the dorsal shield of dissonids, pandarids, cecropids, trebiids,euryphorids, and caligids (e.g. cf. Kabata, 1966a; Benz and Deets, 1987, 1988; Benz, 1989;Deets and Benz, 1988; and Deets and Dojiri, 1989) supports Kabata’s (1979) premise, as itappears that the posterior sinus of trebiids, euryphorids, and caligids is laterally bound by therenmant of a lateral plate associated with the second pedigerous segment, whereas indissonids, pandarids, and cecropids the posterior sinus is not as well-delimited and islaterally bound by pre-second pedigerous segment components. Although lateral platesassociated with the posterior sinus are known to assist in attachment by sealing the dorsalshield, the functions of other cuticular alae are generally unknown. Kabata (1979) noted thatfemale Anthosoma crassum (Dichelesthiidae) possess elytra which seem to offer protectionfrom encroaching host tissues. However, unlike Anthosoma, caligifonns seldom are deeplyembedded in their hosts. The ventral surface of some lateral plates of pandarids possess acorrugated surface which may (e.g. Pandarus species) or may not (e.g. Nesippus species) beexpanded into an adhesion pad. Corrugated surfaces would seem to assist in attachment byfunctioning as friction plates. Elytra are added throughout development from copepodid toadult, and other than those seemingly associated with locomotion and attachment, the alae ofmale caligiforms are typically fewer and/or smaller than those of their correspondingfemales.Kabata (1979) proposed that the caligiform lineage was composed of two groups, the firstlacking dorsal and lateral plates (considered represented by Dissonidae, Trebiidae, and61Caligidae), and the second possessing such plates (considered represented by Pandaridae,Cecropidae, and Euryphoridae). Within each group Kabata (1979) hypothesized anevolutionary trend involving a step-wise process of cephalization incorporating the natatorythoracic segments into the cephalothorax. Although this process is quite evident amongcaligiforms, Kabata’s (1979) two group proposal must be questioned because as noted byDojiri (1983) the presence or absence of dorsal and lateral plates does not so convenientlycleave caligiforms into two groups.Dojiri’s (1983) consideration of interfaniilial relationships among caligiforms regarded thegroup to be composed of two clades. One consisted of Pandaridae and Cecropidae, and theother of Dissonidae, Trebiidae, and Caligidae (into which Dojiri placed Euryphoridae). Tothis author, the characters used by Dojiri (1983) to support two caligiform clades seemunconvincing and/or ill-defined. For example, the long and slender mouth tube that Dojiri(1983) assigned to the pandarid-cecropid dade seems to be a very graded characteristicwhich appears related to the functional constraint of having to feed between the raisedplacoid scales of elasmobranch hosts (see Fig. 22). The dentiform process whichdistinguishes Dojiri’s (1983) dissonid-trebiid-caligid dade is only slightly modified amongpandarids and cecropids. The possession of biramous legs one-four that distinguishesDojiri’s (1983) pandarid-cecropid dade is a characteristic shared with dissonids. Lastly, thetrend toward reduction of the segmentation of legs one-four in Dojiri’s (1983) pandaridcecropid dade is a character which probably represents a homoplasy, having happened onseveral occasions within the caligiform lineage. Support for this argument comes from asimilar general trend within Dojiri’s (1983) dissonid-trebiid-caligid dade.Based on the present analysis there appears no justification to split the caligiform lineageinto two clades (see Table 1 and Fig. 21), and yet the herein proposed phylogeny depicts theevolution of cephalization among caligiforms as generally proposed by Kabata (1979) and62Dojiri (1983). Although this author feels inclined that Dissonidae represents the mostprimitive caligiform family (a premise more boldly advanced by both Kabata, 1981 andDojiri, 1983), strong character evidence supporting this remains unfound. The idea thatdissonids are most primitive appears to be linked to the overall appearance of their habitus, aform that appears unspecialized and in which sexual dimorphism is unpronounced. Whilethis form contrasts sharply with cecropids and modified pandarids, it does not conflictgreatly with unmodified pandarids such as Paina and Demoleus Heller, 1865. Thisphylogenetic analysis, therefore, considers Dissonidae to be the sister group to a dadeconsisting of Pandaridae and Cecropidae (see Fig. 21). The pandarid-cecropid dade ismarginally set apart by possessing first maxillae with relatively small rami and endopods notdistinctly dentiform (character 24 of Table 1 and Fig. 21).While Pandaridae and Cecropidae appear closely allied, their separation has historicallybeen problematic. Kabata (1979) proposed that the shape of the female corpus maxillipedis(squat with myxal region displaced distally in Pandaridae, slender in Cecropidae) can beused to distinguish these two closely related families (see character 25 of Table 1 and Fig.21). A recent redescription (Benz and Deets, 1988) of the cecropid Entepherus laminipesBere, 1936 has strengthened Kabata’s (1979) criterion. In addition to the maxilliped ofEntepherus fitting the cecropid form, the report of Benz and Deets (1988) is importantbecause it offers evidence that the dissimilarity displayed between the maxillipeds ofpandarids and cecropids is not due to functional constraints. This conclusion is madebecause Entepherus is the only cecropid which is parasitic on elasmobranchs, and prior to adetailed description of its maxillipeds one might have considered that differences in hostsubstrates (i.e. surfaces with placoid scales versus surfaces without them) rather thancommon ancestry may have determined the different maxihipeds of pandarids and cecropids.Adding further evidence that this difference between pandarids and cecropids is free fromfunctional bias, it should be noted that among pandarids (all of which are parasitic on63elasmobranchs) squat maxiffipeds with their myxal regions displaced distally are found onboth species which attach to surfaces with and without placoid scales (cf. Figs 15 and 25).Comparisons among the maxillipeds of dissonids, pandarids, and cecropids suggest the formshared by pandarids to be derived.Continuing up the caligiform dade, Trebiidae is separated from Dissonidae and thepandarid-cecropid dade by possessing a cephalothorax into which the first and secondthoracic legs have been incorporated (character 26 of Table 1 and Fig. 21). Trebiidae alsoshares with Euryphoridae and Caligidae first maxillae which are distinctively composed oftwo parts (character 27 of Table 1 and Fig. 21).Finally, in Euryphoridae and Caligidae the first three pairs of thoracic legs becomeincorporated into the cephalothorax (character 28 of Table 1 and Fig. 21), with the third pairand their interpodal bar forming a posterior seal for the cephalothorax (character 29 of Table1 and Fig. 21). All euryphorids and caligids except Eurvphorus (Euryphoridae) also sharethe apomorphy of possessing uniramous fourth thoracic legs (character 30 of Table 1 andFig. 21). This author must concur with Dojiri (1983) that Euryphoridae and Caligidaecurrently seem impossible to differentiate from one another.EVOLUTIONARY BIOLOGY OF SIPHONOSTOMES PARASITIC ON VERTEBRATESHistorical considerations can provide rich insight. For biologists, Darwin legitimized thisendeavor by viewing biological process in an evolutionary context. Since Darwin, the who,what, where, and when questions become answered through the reclamation of historicalpattern, and the curious why questions associated with historical process are most rightfullyplaced in tow. Evolutionary studies of free-living organisms are difficult enough, and64similar considerations of parasitic taxa are inescapably hindered by the need for yet furtherlayers of information.Although many phenomena are open to evolutionary inspection, larval development, adultnatural history, and host associations are of particular interest to parasitologists. In thisthesis it seems appropriate to add to this list the invasion of fresh waters, as thesiphonostomes infecting vertebrates have several veterans of this significant ecologicaltransition. It also is appropriate to consider the temporal origin of the siphonostomesparasitic on vertebrates, mainly because fossils virtually do not exist for these animals andtracing origins is fascinating, but also because studies of the possible coevolution of parasitesand their hosts require the assumption of equally ancient hosts and parasites.Trends in Larval DevelopmentAlthough our knowledge of the ontogeny of the siphonostomes parasitic on vertebrates isincomplete, data suggest that several developmental incidents and trends have punctuated theevolution of these copepods (Figs 26 and 27). A life cycle with ten stages (two nauplius, oneinfective copepodid, four parasitic copepodid, two preadult, and one parasitic adult stages)appears to be a primitive characteristic among the siphonostomes parasitic on vertebrates(Figs 26 and 27).The free-living and typically motile nauplius stages disperse copepods throughout hostpopulations. For parasitic species which must secure hosts, a tradeoff logically existsbetween larval dispersal and larval security. Nauplius stages are suppressed in several ordersof Copepoda infecting vertebrates (Kabata, 1981; Raibaut, 1985). Among the siphonostomesparasitic on vertebrates, a reduction in the planktonic nauplius stages that presumably65reduces dispersion is seen in several taxa (Fig. 26). For example, observations of Dissonusnudiventris suggest that the balancers of its nauplius may be crudely used to snag its mother’sruptured egg sacs. Such entanglement would seem to ensure the subsequent copepodidstage’s close proximity to a suitable host (Anderson and Rossiter, 1969). Sphyrlids and somelernaeopodids and pennellids complete precopepodid development within the egg so thathatching liberates an infective copepodid (Fig. 26). This process could be viewed as acombination of delayed hatching and precocious development.Enormous somatic development produces a copepodid from a nauplius. The firstsiphonostome copepodid typically exhibits a cephalothorax with five pairs of cephalothoracicappendages, a number of biramous swimming legs individually issued from thecephalothorax and free thoracic segments, and an abdomen bearing a pair of caudal rami.Among siphonostomes, the first copepodid is maintained as the primary infective stage (Fig.26). This is a life history characteristic that is shared with Poecilostomatoida (Kabata, 1981;Raibaut, 1985). Upon securing its host the infective copepodid undergoes one to six moltswhich ultimately transform it into a preadult or adult (Fig. 26).The term chalimus is often used for copepodids that tether themselves to their hosts via afrontal filament. The frontal filament is produced by the frontal organ during the infectivecopepodid stage, and can often be seen in its coiled and untriggered condition within theanterior portion of the cephalothorax of some copepodids. Upon securing its host, theinfective copepodid extrudes the frontal filament and securely anchors it. Once fastened, thecopepodid molts into what is generally considered the first parasitic stage, the first chalimus.The frontal filament is absent in Lernanthropidac (Fig. 26) and based on similarities ingeneral lifestyles (Fig. 27) possibly also in Eudactylinidae, Kroyeriidae, Hatschekiidae,Pseudocycnidae, Hyponeoidae, and Dichelesthiidae. The presence of the frontal filament66seems associated with an ecological shift from the branchial chamber and olfactory capsulesto the general body surface (Fig. 27), as well as with the appearance of derived modes ofadult attachment (see below).The frontal filament fastens the chalimus during the molting process and providesunyielding security for young copepods that have not yet developed adult holdfastmechanisms. But, as seen in Lemanthropidae, this tether is not required by allsiphonostomes parasitic on vertebrates. How these copepods stay attached to their hostsduring molting is not well known, however, copepodids that tightly attach to their hostseither by burrowing or through deep penetration of the host with attachment appendageswould seem capable of emerging from still anchored exuviae and re-attaching nearby.Although this has not been observed, it seems possible that some lineages never needed thefrontal filament, and that other taxa may have modified or reduced their reliance on it. Forexample, the short thin frontal filament of Echthroaleus torpedinis described by Benz andLast (in review) appears too feeble to support a larva throughout its entire development. It ispossible that as some copepods molt and develop adult mechanisms of attachment the needfor the frontal filament becomes solely associated with the molting process. For Caligidae itmight be advantageous for early larvae to be permanently tethered to the host. Swinging onthe end of their frontal filaments, these superficial grazers could forage over a relatively wideregion. However, for some caligiforms which infect elasmobranchs and who insert theirrelatively long mouth tubes between the placoid scales of their hosts, a less waveringattachment mode might be required to allow the oral cone to remain stationary. Such anattachment mode might be facilitated by the placoid scales themselves or methods involvingthe invasive application of attachment appendages.Virtually nothing is known of the energy requirements of developing siphonostome larvae,and therefore the real value of the frontal filament is unknown. However, beyond mooring67the chalimus throughout the molting process, the frontal filament presumably provides astrong passive form of attachment requiring little maintenance energy. Unknown also iswhat life at the end of the frontal filament is like. For example, many caligiforms andpenneffids exhibit relatively short frontal ifiaments which ensure that the mouth tube couldcontact the host and allow feeding. Contrarily, many lemaeopodids possess extremely longfrontal filaments (e.g. see Benz, 1991) which would offer them a larger feeding area, butwhich seemingly would unpredictably dangle them about unless the second antennae and/ormaxillipeds were used to grasp the host.While developmental observations are needed to settle the issue concerning whichsiphonostome taxa parasitic on vertebrates possess a frontal filament, comparative studies offrontal filaments are also needed. This is because preliminary observations (albeit sketchy)indicate possible structural differences among the frontal filaments of siphonostomes thatmay denote homologous relationships or analogous representations of obvious evolutionarysignificance. Careful comparisons are also needed with nicothoiid frontal filaments (seebelow) to fully understand the phylogenetic implications of this ecologically useful structure.Just prior to adulthood up to two preadult stages may exist (Fig. 26). Kabata (1981) statedthat the preadult stages represent that period when the copepod either settles definitely on itshost and undergoes metamorphosis, or otherwise attains its final level of organizationwithout aid of the semi-permanent protective larval attachment. In discussing the preadultstage in Ergasilidae (Poecilostomatoida), Kabata (1981) further stated that the differencebetween the copepodid and preadult could be more semantic than substantial. Kabata’s(1981) remarks are valid because in some instances no solid characteristic delineates so-called preadult stages from the earlier larval series while in the rest of all instances nothingdelimits them from actual adults. It is not surprising, therefore, that some authors have not68used the term preadult, instead opting to classify these stages as copepodid, chalimus or adult(e.g. see Lewis, 1963).A general shortening of the later larval series is exhibited by Penneffidae andLernaeopodidae (Fig. 26), and based on the similarities among lernaeopodiforms a similartrend is probably also present in Sphyriidae, Naobranchiidae, and Tanypleuridae. InPennellidae and Lernaeopodidae a discrete preadult stage does not occur. After the lastchalimus stage the untransformed adult female metamorphoses without molt into her finalhabitus. Males, likewise, become functional adults after the last chalimus. The greatestreduction of the larval series is seen in some lernaeopodids (Fig. 26) that display only threelife history stages (i.e. one nauplius, one copepodid, and the pupa-adult). The highly motileCaligidae have retained all ten life history stages (Fig. 26). This fact raises the question ofwhether or not the relatively complex organization of these copepods dictates maintainingthe entire developmental series. It is also notable (Fig. 26) that the greatest tendency towarda reduction of larval stages among the siphonostomes parasitic on vertebrates appears sharedby lineages such as Pennellidae and Lemaeopodidae (and presumably otherlernaeopodiforms as well) that possess the most highly transformed adult females. Certainly,however, the forms of the retained chalimus stages of Pennellidae and Lernaeopodidae arequite different. Pennellids maintain a rather primitive, highly motile, and streamlinedappearance while lernaeopodids appear as grub-like pupae. The two host life histories ofpenneffids possibly place selective pressure on the untransformed adults (mainly the females)to retain a form capable of swimming, because it is this stage which must actively seek thedefinitive host.69Trends in Adult Natural HistorySiphonostomes infecting vertebrates display a general trend in adult sexual dimorphismmanifested as a relatively smaller adult male (Fig. 1) often with better developed sensory andlocomotory setae than its mate (see above). These male characteristics are generallyconsidered primitive traits (Kabata, 1979), and prompt appraisal of the often regressiveappearance of the adult female as a derived product of evolution. The male accrues its adultcharacteristics sequentially throughout ontogeny and upon reaching adulthood continues toundergo only slight changes in appearance associated with general somatic growth. At thestage of young adulthood the sensory and locomotory armature of the female is less well-developed than those of the male, though the general habitus might not be extremelydissimilar. However, soon after firmly attaching to her host, and often subsequent tocopulation, the female proceeds to grow without molt into a form that can range from mildlyenlarged and retaining the general male configuration to forms so bizarre that the process isbest envisaged as a metamorphosis (Fig. 26; also see above).Species within Eudactylinidae, Kroyeriidae, Hatschekiidae, Pseudocycnidae, Hyponeoidae,Lernanthropidae, and Dichelesthiidae exhibit sexual dimorphism that usually is not verypronounced (e.g. see Fig. lA-C). Among these copepods, males and females of any onespecies usually have similar ecological traits (i.e. sessile, semi-sessile, or errant). Kroveriacasevi is a striking exception to this generality in that it possess typical males andmesoparasitic adult females. Although its males are undiscovered, Carnifossorius siamensisDeets and Ho, 1988 is probably similarly sexually dimorphic. It is notable that the samemechanisms used to secure males to their hosts are also used to grasp females duringcopulation in the above mentioned families (e.g. see Benz and Adamson, 1990). While thisillustrates the versatility of the holdfast appendages, it also indicates that there is at least70some minimal similarity in shape between the host substrate and portions of the femalewhich males seek to grasp.Members of Pennellidae routinely develop extremes of adult sexual dimorphism (Fig. 1D).The adult male and untransformed adult female are only mildly dissimilar, and each exhibitsan active ectoparasitic lifestyle. However, after copulation and upon attaching to thedefinitive host the female assumes a mesoparasitic lifestyle accompanied by a sizablemetamorphosis.Caligiforms exhibit three general types of sexual dimorphism. The first is exemplified byDissonidae, Trebiidae, and many members of Euryphoridae and Caligidae and consists ofhighly mobile adults of both sexes. Males differ mainly in being smaller and retainingslightly more elaborate sensory and locomotory setae as well as in modifications of themaxillipeds and second antennae (Fig. 1E). The second antennae are used during copulationin Caligidae (Anstensrud, 1990b), and their modification in highly active males may havebeen facilitated by the ability of the cephalothorax to provide suctoral attachment in morederived caligiform taxa (e.g. Trebiidae, Euryphoridae, and Caligidae). The second type ofcaligiform sexual dimorphism is exemplified by many members of Pandaridae and somemembers of Euryphoridae and Caligidae and consists of the above described adult malepaired with a relatively sessile adult female (Fig. if). Certainly this is the most dissimilarcaligiform pairing, as the ovigerous female typically is heavyset and sometimes possesses acephalothorax that lacks the marginal membrane. The third type of sexual dimorphismamong caligiforms is exemplified by many Cecropidae members and consists of relativelysessile adult males and females (Fig. 1G). Typically, these males retain a smaller size andmore elaborate sensory and locomotory setae than their respective mates, however, relativeto other caligiform males they are quite large and are capable only of limited crawlingmovements.71Lernaeopodiforms show two types of sexual dimorphism. The first is seen in Sphyriidaeand consists of pupaform adult males and young adult females, and relatively large,transformed mesoparasitic females (Fig. 1H). The second type is displayed by members ofLernaeopodidae and Naobranchiidae (and presumably Tanypleuridae also) and consists ofpupaform adult males and young adult females, and relatively large, permanently attached,transformed ectoparasitic females (Fig. 11).When adult ecological characters of the siphonostomes parasitic on vertebrates are mappedonto the phylogeny of familial relationships it appears that mesoparasitism has independentlyevolved several times (Fig. 27). Studies of Eudactylinidae (Fig. 2; also Deets and Ho, 1988),Kroyeriidae (see Benz and Deets, 1986; Deets, 1987), and Pennellidae (Fig. 10; alsoBoxshall, 1986) indicate that once mesoparasitism is firmly established within a lineage areturn to ectoparasitism is unlikely. Given the modifications exhibited by mesoparasiticfemales, explanations of this phenomenon involving natural selection seem obvious.However, there appears no logical reason why a lineage could not return to an ectoparasiticlifestyle via either the modification of the adult metamorphic program or via the processes ofneoteny or progenesis. However, generally we must consider that mesoparasiticsiphonostome lineages appear directed toward deeper associations with their hosts, and thatthe presence of a nauplius and/or copepodid stage which must be shed into the environmentmay represent the barrier precluding true endoparasitism. Of course this indicates anectoparasitic origin for siphonostomes parasitizing vertebrates, a conclusion also supportedby data from studies of the relatively primitive families Eudactylinidae and Kroyeriidae (seeBenz and Deets, 1986; Deets, 1987; Deets and Ho, 1988). Kabata (1982) commented thatthe burrowing habits of many siphonostome larvae may have ultimately been responsible foror facilitated the evolution of mesoparasitic lineages. However, no matter what its origin,mesoparasitism appears to have been one method allowing siphonostomes to affix72themselves about the general body surface of active fishes. It is notable that this firmestmethod of attachment has produced adult females that are dramatically larger than theirectoparasitic relatives and conspecific mates. It is further important that this increase in sizehas been realized through a number of developmental schemes involving different somaticregions. For example, in Carnifossorius the bulk of the embedded body represents the firstpedigerous segment, while in pennellids, sphyriids, and Kroveria casevi this portionrepresents the thoracic segments and some of the genital complex.Caligiforms are evolutionarily interesting because they represent a very successful lineagewhich often is associated with the general body surface of their hosts. Unlike pennellids andlernaeopodiforms, caligiforms have not evolved widespread provision for permanent passiveattachment. Instead they have evolved two basic lifestyles. Pandaridae and Cecropidaeseem to have followed a trend toward increasing the sessile nature of the adult female.Dissonidae, Trebiidae, Euryphoridae, and Caligidae appear to have maintained and/orexploited a more mobile existence. As if dictated by necessity, the swimming legs seenwithin these more active families appear more conservative than those possessed by moresessile pandarids and cecropids. While the evolution of these differences is hard to explain,the placoid scales which typically cover elasmobranchs appear to offer a very stable substrateon which to permanently attach (see Benz, 1992), and which might somewhat release thethoracic legs from functional use. On the other hand, the relatively smooth and seeminglyhard to grasp body surface of teleosts should encourage the evolution of mechanismsenhancing the ability to rapidly attach. Such mechanisms naturally would involve bothpowerful swimming and efficient settling abilities as seen in most caligids. However, thecommon existence of fast swimming pandarid males of considerable size on many species ofelasmobranchs indicates that a sessile lifestyle need not be a prerequisite for caligiformsinfecting elasmobranchs, and as mentioned above some caligid females are relatively sessileas adults (see Fig. 20).73Routine attachment at particular locations on the host is a parasitic phenomenon oftenexhibited by siphonostomes that infect vertebrates, and generally speaking, these parasiteshave quite successfully invaded the external surfaces of fishes (Table 2). The relativelyrandom initial distributions of larvae (e.g. see Kabata and Cousens, 1977; Anstensrud andSchram, 1988; Benz, 1989) reveal that site selectivity often intensifies throughout life, andfurther suggests that the phenomenon of site specificity may be related to maturation andreproduction. The relatively random distribution of larvae and nonrandom distribution ofadult females also suggests that highly efficient mechanisms of autoinfection (i.e. the hostbeing infected by the progeny of parasites residing on it) are not well-developed because ifthey were one would expect the distribution of infective larvae to better resemble thedistribution of ovigerous females. Males representing several different familial lineageshave been noted to exhibit wider distributions than females (Benz, 1980; Benz, 1986; Benzand Dupre, 1987; Anstensrud, 1990c). Benz and Dupre (1987) proposed that water flowabout the gills of blue sharks was responsible for the initial distributions of Kroveriacarchariaeglauci, and that males ranged over a wider area in search of mates throughout theranks of gill filaments. Other distributions are more difficult to explain. For example, manyadult female caligiforms are found in dense clusters attached at very restricted andpredictable locations on their hosts (Figs 18 and 20; also see Benz, 1980; Anstensrud,1990c). A convincing explanation for these disthbutions is lacking. Benz (1980) noted thatPandarus satvrus Dana, 1852 individuals which appeared to assume more posterior positionsin clusters seemed to be younger adult females and that males tended to associate most withthese peripheral females. Anstensrud (1990c), however, noted in observing Lepeophtheiruspectoralis that most copulatory activity took place away from clusters and that males seldomfrequented them.74Several siphonostome lineages infect both the branchial chambers and olfactory capsulesof their vertebrate hosts (Fig. 27). The branchial chambers of fishes offer small parasites anorderly yet heterogeneous environment best envisaged as consisting of many niches (Figs 6and 8). Within the branchial chambers, most members of Eudactylinidae, Kroyeriidae,Hatschekiidae, Pseudocycnidae, Hyponeoidae, Lernanthropidae, and Dichelesthiidae tend tobe intimately associated with the gill filaments of their hosts (Wilson, 1932; Kabata, 1979;Benz, 1980; Davey, 1980; Benz and Dupre, 1987; Benz and Adamson, 1990). Although afew caligiforms attach directly to the gill filaments, most residing in the branchial chamberare associated with the interbranchial septa of elasmobranchs or the gill arches. Pennellidsand sphyriids infecting the branchial chambers are likewise distributed, although the cryptingthese relatively large sessile copepods cause on the gills can affect large regions of therespiratory surface (see Grabda, 1991). As discussed above, naobranchiids are confined toregions of the gills where they can encircle a gill filament with their second maxillae.Lernaeopodids and tanypleurids require an attachment substrate which will support thefemale anchoring system, and within the branchial chambers the interbranchial septa andtissues capping the efferent arterioles of elasmobranchs, the tissues capping the afferent andefferent arterioles of teleosts, the gill arches, and the branchial chamber walls best providethis requisite.The gills and olfactory capsules of elasmobranchs show many similarities (Fig. 28), andsiphonostomes infecting olfactory capsules tend to occupy niches similar to their closerelatives residing within the branchial chambers (Fig. 28). In presenting an ecologicalsummary of Kroyeriidae, Deets (1987) noted the probable habitat shift of some protokroyeriid from the branchial chamber to the olfactory capsule of chondrichthyans. In light ofthe similar construction of the olfactory capsules and gills of these primitive fishes (Benz,1984, in preparation), such a habitat shift raises an interesting question. Have somesiphonostomes invaded the olfactory capsules of fishes from the branchial chambers because75these habitats represent analogous and ecologically conservative environments, or are theolfactory capsules modified branchial chambers which through their derivation from the gillsprovided a powerful vicariant event that promoted the isolation and subsequent speciation ofparasite inhabitants?Several authors have speculated on the possibility that the olfactory capsules were derivedfrom premandibular gill pouches (see Dohrn, 1875; Marshall, 1881) or gill arches (seeBjerring, 1972, 1973; Bertmar, 1972). Unfortunately, the developmental programs thatresult in forming the olfactory capsules of extant fishes appear so derived that compellingevidence linking the origin of the olfactory sacs to the gills may no longer exist (see Jollie,1977). While the present author would not challenge that original innovations can ariseindependently within the framework of evolution, he would also argue that in consideringthe origin of the olfactory capsules, parsimony would seem to favor derivation of these rathercomplicated structures from the similarly organized gills (see Fig. 28). Such pathway seemseven more likely given the serial nature of the gills and the universally accepted theory that asimilar process involving the modification of gill arches led to the formation of true chordatejaws. If evolution of the olfactory capsules was immediately instrumental in isolatingsiphonostome lineages such as Kroeverina, it would mark the presence of vertebrateinfecting siphonostomes at least as far back as the Ordovician (441-504 mya) and wouldextend the association between siphonostomes and chordates to include some (if not all) ofthe earliest vertebrates (Stahl, 1985; Chaline 1990).The ecological shift from the branchial chambers and olfactory capsules to the generalbody surface was apparently coincident with the appearance of the frontal filament (Fig. 27)and might have been further facilitated by three different modes of extending this attachmentsecurity throughout adulthood. As discussed above, adult pennellids and sphyriids evolvedmesoparasitic females capable of securing the host. Penneffidae retained a small swimming76male while Sphyriidae shares with Lernaeopodidae and Naobranchiidae (and presumablyalso Tanypleuridae) a crawling grub-like male. Adult female lemaeopodids, tanypleuridsand some caligiforms permanently attach to their hosts via superficially invasive methods.Other caligiforms use a suctoral attachment mode which provides firm grasp yet can bevented to free these able swimmers to move about their hosts. Although shifts from thebranchial chambers and olfactory capsules seem to coincide with morphological changes inboth sexes, the form of the adult female appears to have been altered more radically, andthese alterations are often reflected in a larger overall female size which is generally thoughtto be associated with increasing reproductive potential (Kabata, 1979).Trends in Host AssociationsMany siphonostomes appear particularly well-adapted and consequently appear restricted toparticular hosts. For example, the unique holdfast of Naobranchiidae which must encircle agill filament appears to confme this family to the gills of teleosts (Fig. 8). Similarly, thenoninvasive method of attachment and long vermiform bodies of most Kroveria speciesseem tailored to living in the water channels formed by the gill filaments and interbranchialsepta of chondrichthyans (Fig. 4; also see Benz and Dupre, 1987). Further still, the lock andkey mode of attachment exhibited by Pandarus species certainly appears to restrict theseparasites to the placoid scales of elasmobranchs (Fig. 15; also see Benz, 1992). However,even these best examples of morphologically founded host restriction seem incomplete, asrespectively among teleosts, chondrichthyans, and elasmobranchs, Naobranchiidae, Kroveria,and Pandarus are relatively host specific.The radical ecological transitions exhibited within some otherwise conservativesiphonostome lineages make the host specificity generally displayed by siphonostomes even77more difficult to understand. This is because these transitions suggest that as a group theseparasites may be at least periodically capable of speciation involving major lifestylealterations (e.g. see discussions above of Kroveria casevi and Carnifossorius). Therefore,facile rationalizations of siphonostome-host associations based solely on morphologicaladaptation are usually inadequate to explain why these parasites have not additionallyinvaded seemingly available hosts and niches.Nonetheless, as discussed above, one cannot help but notice that siphonostome infectionshave permeated Pisces and more remarkably have invaded Cetacea, and that somesiphonostome characteristics may have preadapted or have come to adapt certain copepodspecies to certain hosts. For example, the relatively long mouth tubes of many Pandarusspecies allows them to feed beyond the hard nutritionally unsuitable placoid scales that coverthe general body surface of many elasmobranch hosts. Similarly, the mesoparasitic lifestyleof Pennella balaenoptera Koren and Danielssen, 1877 seems conducive to infecting large andrelatively smooth skinned cetaceans.The ability of siphonostomes to develop efficient attachment mechanisms capable ofsecuring highly active hosts must have been instrumental during the early colonization offishes. As the two most successful families of siphonostomes parasitic on vertebrates,Caligidae and Lemaeopodidae have each evolved a distinct mechanism to accomplish this.For caligids, the high mobility and ability to rapidly attach to a host perhaps was one factorresponsible for speciation success because it facilitated the invasion of new host taxa byhighly mobile copepodids, preadults, and adults. For lemaeopodids, the evolution of apermanent method of attaching to the host along with some shortening of the life cycleseems significant.78Since at least von Ihering (1891), parasitologists have postulated that parasites may evolvealong with their hosts and that congruent patterns of phylogeny between hosts and theirparasites may reflect this process. For the parasitologist, often denied a meaningful share ofthe fossil record, such reasoning has become an imaginative time machine fueled by thephylogenetic relationships of hosts and potential former hosts.Copepodologists have recently begun to use phylogenetic techniques such as cladisticanalysis and host mapping to try and better understand the historical relationships betweenparasitic copepods and their hosts. To date, these types of studies of various siphonostometaxa have revealed varying degrees of phylogenetic congruence with host taxa (e.g. see Ho,1983, 1989; Deets, 1987; Benz and Deets, 1988; Deets and Ho, 1988; Dojiri and Deets,1988; Ho, 1992). Instances of incongruence between parasite and host phylogenies arethought to denote colonization episodes mediated more by ecology than phylogeny.Surprisingly, however, cases of strict agreement between host and parasite lineages are moredifficult to assess. This is because congruent regions of host and parasite phylogenies oftenexhibit an enormous disparity between the phylogenetic breadth of the represented parasitesand the phylogenetic breadth of the represented hosts. This disparity usually is caused by thephylogenetic scope of the host taxa present (as determined by parasite records) far exceedingthat of the parasites analyzed (i.e. many host species which are members of the host groupsdelimited by the studied parasites have no known parasites associated with them). Withoutadditional data, it is impossible to explain this common phenomenon. Certainly theundersampling of parasites cannot be entirely responsible for these differences.Furthermore, although explanations involving the extinction of parasites theoretically couldaccount for such differences, such hypotheses need sound biological data to be properlyadvanced, and these data are seldom available.79No matter how these instances of host-parasite congruence are explained, it is interestingthat to date no study examining phylogenetic congruence between siphonostomes and theirhosts has determined a strict stepwise association of host and parasite species (see Deets,1987; Benz and Deets, 1988; Deets and Ho, 1988; Dojiri and Deets, 1988; Ho, 1992). If weaccept that siphonostome copepods are approximately the same evolutionary age as theirhosts (and this assumption is an axiom of phylogenetic studies of the coevolution betweenparasites and hosts) then we must accept that generally they have exhibited a lowerspeciation rate or higher extinction rate than their hosts. Parasitic taxa in general exhibit thisphenomenon, together suggesting that the lifestyle of parasitism is often linked to lowerspeciation rates than those of associated hosts. Of course some parasite taxa have apparentlyspeciated as fast as or faster than their hosts. An example of this from among thesiphonostomes parasitic on vertebrates is the cecropid dade consisting of Phiorthagoriscus,Orthagoriscicola, and Cecrops, all which are virtually exclusive parasites of the oceansunfish (Benz and Deets, 1988).The importance of host phylogeny and history cannot be overstated when considering theevolution of parasitic lineages. Certainly the fossil record indicates that various host andpotential host lineages have originated, gone extinct, or otherwise increased and decreasedover time. It seems logical to assume that this biotic flux has played a major role in theevolution of parasitic lineages in a manner analogous to and layered upon the geological,geographical, and climatic changes commonly accepted as influencing the evolution of free-living lineages, and upon the more controversial catastrophic events that may havepunctuated the biological record (see Raup, 1991).80Invasion of Fresh WaterSiphonostomatoida exhibits a modicum of success in fresh water, having moved into thisenvironment at least twice (Fig. 27). One caligiform can complete its entire life cycle infresh water. CaIius lacustris Steenstrup and Lütken, 1861 (Caligidae) occurs in the Baltic,Black, Azov, Caspian, and Aral Seas, and adjacent brackish waters (Grabda, 1991).Although adults are good swimmers and are sometimes found among the plankton and uponmany species of fish, cyprimd fishes (Cyprinidae) seem to be preferred hosts (Yamaguti,1963; Grabda, 1991). Adult lacusths are found on the gills and general body surface oftheir hosts (Markewitch, 1976), while chalimus larvae are commonly found attached to thefins (Grabda, 1991). It is very likely that . lacustris evolved into a freshwater species frommarine caligid ancestors, and recently Gusev and Kabata (1991) have determined that amongover 200 congeners, £. lacustris appears most closely related to four species (, curtusMUller, 1785, minimus Otto, 1821, . mugilis Brian, 1935, and dicentrarchi Cabral andRaibaut, 1987) whose ranges overlap to varying degrees.About 30 salmincolaform lernaeopodid species grouped in seven genera (Achtheres vonNordmann, 1832; Basanistes von Nordmann, 1832; Tracheliastes von Nordmann, 1832;Cauloxenus Cope, 1871; Salmincola Wilson, 1915; Coregonicola Markevich, 1936;Pseudotracheliastes Markevich, 1956) can only complete their life cycles in fresh water.These genera are restricted to the northern hemisphere, with a fair number of their speciesdisplaying circumpolar, Palaearctic or Nearctic distributions (Kabata, 1969c; 1979; 1988a).Host affiliations of freshwater lernaeopodids are fairly restricted, with many anadromoussalmonids (Salmonidae) and sturgeons (Acipenseridae) serving as hosts. Adult females ofsome genera (e.g. Salmincola) are sometimes found in oceanic waters on anadromous fishes,however, these individuals are unable to reproduce in marine environments (Kabata, 1979).81Kabata (1979, 1981) considered salmincolaforms to have invaded fresh water on someprimitive salmonid during an interglacial portion of the Pleistocene (1.6-0.0 1 mya). Kabata(198 1) also noted that because salmincolaforms are considered among the most primitivelernaeopodids such a scenario tends to compress lernaeopodid evolution into what appears arecent burst of speciation. However, Kabata (1981) reported that the study of Kabata and Ho(1981) indicated that Neobrachiella insidiosa (Heller, 1865) must have existed more than 50mya (i.e. Tertiary) to be able to colonize its present distribution range. Important here is thatinsidiosa is a brachiellaform, a lineage of Lernaeopodidae considered far derived fromancestors of salmincolaforms (see Kabata, 1979; 1981). From these data Kabata (1981)postulated that early salmincolaforms must have existed in the marine environment longbefore they invaded fresh water. It is important to add to Kabata’s (1981) explanation thatone salmincolaform genus (Pseudotracheliastes) is composed of species that are exclusiveparasites of sturgeons (Acipenseriformes). Sturgeons are an ancient group and could haveopened fresh waters to salmincolaforms long before the arrival of salmonids, possibly as farback as 310 mya during the Pennsylvanian (see Nelson, 1976). Although no detailedphylogeny of the salmincolaform branch of Lemaeopodidae exists, Kabata (1979) noted thatin some respects Pseudotracheliastes is more derived than Salmincola. However,Pseudoiracheliastes could have evolved throughout a long relatively independent existence.Surely, a detailed phylogenetic analysis of all salmincolaform species would provide aninteresting starting point for a proper discussion of how this successful lineage ofSiphonostomatoida entered fresh water.It seems logical that siphonostomes moved into fresh water under the power of their moremobile hosts rather than through self dispersal. Using this method, copepods would beferried into freshwater environments by diadromous fishes (i.e. truly migratory fishes thatmove between sea water and fresh water). Although freshwater invasion could have beenmediated by nondiadromous species, the relatively unpredictable nature of this mode of82access makes it seem that the rhythmic life history associated with diadromy would optimizeinvasion opportunity. In turn, although anadromous (i.e. diadromous fishes that migratefrom sea water to fresh water to breed), catadromous (i.e. diadromous fishes that migratefrom fresh water to sea water to breed), or amphidromous (i.e. diadromous fishes whosemigrations between sea water and fresh water or vice versa occur regularly but not associatedwith breeding) fishes might serve as transport, anadromous and marine amphidromousspecies (i.e. amphidromous species that are born in fresh water, grow in sea water, and returnto and grow and reproduce in fresh water) theoretically appear best suited for this task. Thisis because such species tend to be more numerous in comparison to catadromous andfreshwater amphidromous species (i.e. amphidromous species that are born in sea water,grow in freshwater, and return to and grow and reproduce in sea water), and because theyenter fresh water at relatively older ages and larger sizes (see McDowall, 1988) and thuswould have had additional time to acquire maximum marine parasite loads. Anadromousfishes seem further desirable as agents in this process in that they often form large, denseschools as they run into fresh water to spawn (see McDowall, 1988).Contemporary life histories of most anadromous fishes depict an existence whereinattached biota would be relatively rapidly conveyed into brackish and then fresh water. Suchrapid transition into fresh water might prove too much osmotically for some externalparasites. However, a more gradual transition is possible. Via this scenario copepods couldreside within nearshore brackish waters on nonanadromous fishes, and upon the yearlypassing of large schools of anadromous species, infective stages could attach to them. Forfirmly attached adult copepods (e.g. Lernaeopodidae) this would have required copepodidsto be available. For motile species (e.g. Caligidae) both adults and larvae could have beeninvolved in this host shift. In fact, today similar host shifts of sea lice (Lepeophtheirussalmonis Krøyer, 1837 and Caligus elongatus Edwards, 1840) are known to take place(Bruno and Stone, 1990).83Having reached the homestream and spawned, anadromous fishes either perish or return tothe sea. Therefore, to continue thriving in fresh water, copepods (or their progeny) mustlocate new hosts. For motile copepod species (e.g. Caligidae) or those capable of producinginfective larvae tolerant of fresh water this might be instantaneously accomplished bytransferring to different host species living in the freshwater environment. On a moreevolutionary thnescale, persistence in fresh water may have been accomplished bymaintaining association with the host as it evolved into a true freshwater species (this ofcourse presumes a marine origin for the host species). It is interesting to consider here thatnatural selection could have a strong effect on parasite populations entering fresh water oniteroparous host species (i.e. species whose individuals have repetitive reproductive cycles).During the spawning migration, individual copepods which could not endure a freshwaterexcursion would be eliminated from the population. As postspawning fishes return to thesea, copepod veterans genetically capable of surviving the freshwater migration couldproduce a future generation of freshwater tolerant adults. No doubt, yearly repetition of suchculling episodes would eventually result in viable populations of copepods more tolerant offresh water. Through such a mechanism, adult copepods which permanently attach to theirhosts (i.e. Lernaeopodidae, Sphyrildae, Pennellidae) might have an advantage over moremotile species (e.g. Caligidae). As many know that have attempted to use osmotic imbalanceto eradicate copepod infections from fishes, loosely attached individuals often dislodgethemselves when they begin to become stressed. Once dislodged, these copepods areeventually doomed unless they can find another host. It might be that the survivorship inpermanently attached species is a more direct reflection of osmotic tolerance in that unable todislodge when stressed, these copepods are committed to completing the freshwater journey.The ramifications of such a selection mechanism might also immediately extend into the nextgeneration if females were ovigerous upon entering fresh water.84A more subtle scenario accounting for freshwater siphonostomes involves an ecologicalinheritance mechanism. Via this method, creation of freshwater habitats from former marineenvironments caused by periodic changes in world sea level could have slowly allowed theevolution of freshwater copepods in ifli. In reality, a similar inheritance mechanism mightbe linked to the evolution of diadromy in fishes and, therefore, it is difficult to consider suchan inheritance scenario as being completely separate from the formerly presented invasionmechanism.Although ovigerous females of a few parasitic copepods (e.g. Erasilus li.z Krøyer, 1863;Poecilostomatoida) have been recorded from both marine and fresh waters (see Bere, 1936;Causey, 1953; Kelly and Allison, 1962), osmotic difficulties probably represent the greatestbarrier preventing marine siphonostomes from thriving in fresh water. In studying thesurvival of the marine species Lepeophtheirus salmonis held at reduced salinities, Johnsonand Aibright (1991b) found a direct relationship between survival rate and salinity. Theyproposed that these results indicated a higher energy requirement for the maintenance of ahyperosmotic state when these marine copepods are subjected to lower salinityenvironments.Some disagreement exists concerning the role of osmotic pressure in the hatching ofparasitic copepods (see Heegaard, 1947; Lewis, 1963; Davis, 1968). In placing ovigerousfemales of many marine copepod species into fresh water or unbuffered fixative, however,the present author has often been rewarded with thousands of hatched nauplil. In general,copepod larvae seem to have greater difficulty than adults with osmotic shifts (e.g. seeShields and Sperber, 1974; Johannessen, 1978; Wootten nj., 1982; Schram andAnstensrud, 1985; Johnson and Aibright, 1991b). In a report to the contrary, Berger (1970;as reported in Kabata, 1981) noted nauplii of the marine caligid Lepeophtheirus salmonis tobe more tolerant of fresh water than corresponding adults. In discussing these results Kabata85(1981) mentioned that adult L salmonis have frequently been found on Oncorhvnchus nerka(Walbaum, 1792) in British Columbia rivers far upstream in pure fresh water, butadditionally stated that possibility exists that various geographic stocks of Leveophtheirussalmonis may exhibit differences in salinity tolerance. It is notable that recentlyHahnenkamp and Fyhn (1985) and Johnson and Aibright (1991b) have shown Kabata’ssupposition to be correct in that L salmonis from the eastern Pacific seem much moretolerant of low salinity than the same species from the eastern Atlantic.Concerning interactions between host and parasite, Panikkar and Sproston (1941)concluded in studying the marine species L.ernaeocera branchialis (L., 1758) (Pennellidae)on cod (Gadus morhua L., 1758) that mesoparasitic copepods were hyperosmotic to hostblood but hypoosmotic to sea water, and that upon excision from the host copepods rapidlybecame isosmotic with sea water. Contrary to these findings, Sundnes (1970; as reported inKabata, 1981) found the intestinal contents of L.ernaeocera branchialis to be almost isosmoticwith sea water. In studying the freshwater mesoparasitic poecilostome Lernaea cvprinaceaL., 1758 on Fundulus heteroclitus (L., 1766), Shields and Sperber (1974) noted that assalinity was raised adult but not senile copepods were generally able to maintain theirosmotic balance. In light of the above, Kabata (1981) seemed correct when stating that thehost’s role in maintaining the osmotic balance of parasitic copepods probably depends on thespecific instance of host-parasite relationship and the impact of the environment on it.At present Lernaeopodidae has no peer rival in fresh water. Current host associationssuggest that lernaeopodids may have utilized large schooling iteroparous hosts to facilitatethe sea to freshwater transition, and that the permanent attachment mechanism of adultfemale lernaeopodids may have increased the value of anadromous iteroparous fishes to theirtransition into true freshwater parasites through the above outlined natural selectionmechanism. Additionally, the shortened life cycle of lernaeopodids, exhibiting at most one86very short nauplius stage and for some species an egg sac which directly yields infectivecopepodids (Fig. 26), surely seems favorable in lotic environments where pelagic dispersalof larvae becomes a risky proposition. Beyond this, the role of the bulla in mediatingenvironmental perturbations via host-parasite exchange has not been thoroughly examined,although some studies indicate the bulla to serve some exchange purpose (Kabata andCousens, 1972; Kabata, 1979).By comparison, Caligidae seems to have entered fresh water via perseverance. Likelernaeopodids, caligids are well-represented on schooling iteroparous anadromous fishes,however, their life cycles typically contain at least one nauplius and two preadult stages notseen in lernaeopodids (Fig. 26). As adults caligids are also much less permanently fixed ontheir hosts. It is likely that the notable swimming ability of caligids during all phases ofdevelopment not tethered by the frontal filament has facilitated their transfer to new hostsand environments.It is interesting to consider why Sphyriidae and Pennellidae, whose adult females arepermanently fixed to their hosts, haven’t established themselves in fresh water. Sphyriids, inparticular seem preadapted for this transition in that as members of the lernaeopodiformlineage they possess life cycles in which the egg sac hatches directly into an infectivecopepodid. However, sphyriids are a small group, half of which infect elasmobranchs, agroup of fishes which has shown little evolutionary inclination to invade fresh water. Theremaining half infect demersal and often deep-sea teleosts (see Yamaguti, 1963; Kabata,1979). Pennellidae on the other hand does infect some densely schooling anadromousteleosts (see Yamaguti, 1963). However, many pennellids exploit two host life cycles,requiring the close juxtaposition of large numbers of intermediate and definitive hosts. Thistwo host life cycle may represent a barrier to successful exploitation of freshwater habitats.87Temporal Origin of Siphonostomes Parasitic on VertebratesMost copepodologists would agree that if the siphonostomes parasitic on vertebrates dorepresent a monophyletic lineage, this lineage probably arose from siphonostomes associatedwith invertebrates. Unfortunately, relatively little is known about the interfamilialrelationships and general life histories of the siphonostome associates of invertebrates thatlends itself directly to resolving relationships with taxa parasitic on vertebrates (see Gotto,1979). Also, it seems likely that within many siphonostome lineages evolution has followeda common parasitic pathway resulting in a reduction and loss of appendages, and thispathway ultimately muddles the issues of homology and character transformation (Kabata,1979; Huys and Boxshall, 1991). Finally, virtually no fossil record exists forSiphonostomatoida. This makes the discussion of ancestral forms highly speculative andnecessarily based on chimera-like constructions pieced together from “primitive” bitsscrounged from extant taxa. Thus any consideration of the origin of the siphonostomesparasitic on vertebrates must be considered highly speculative.Huys and Boxshall (1991) provided a detailed character set depicting an ancestralsiphonostomatoid. This diagnosis is interesting in that it was primarily based onplesiomorphic characteristics displayed by siphonostomes associated with both invertebratesand vertebrates. As such it acknowledges the relatively derived state of many invertebrateassociates, as well as, the seemingly very primitive characteristics of several taxa infectingvertebrates. For example, Eudactylinidae is commonly considered to represent a primitivedesign among siphonostomes of vertebrates (Kabata, 1976, 1981; Deets and Ho 1988; Huysand Boxshall, 1991). Some of these primitive features include highly segmented firstantennae (e.g. Bariaka, Protodactvlina, male Eudactvlinella ]j) and a genital segmentseparate from the first abdominal segment (e.g. Protodactvlina). Highly segmented andseemingly plesiomorphic first antennae are also exhibited by many siphonostome associates88of invertebrates, as well as the fossil parasite of fishes Kabatarina. Notable also is thatamong all siphonostomes, only Protodactvlina and Jushevus (both members ofEudactylinidae) exhibit a truly separate genital somite. Certaiiily this must be considered aprimitive characteristic for Siphonostomatoida, and its existence in otherwise primitiveappearing eudactylinids parasitic on fishes leads one to consider these parasites as ancientand in some respects relictual siphonostomes. Synapomorphies that separate thesiphonostomes of vertebrates from those of invertebrates notwithstanding (Table 1 and Fig.21), the fact that Eudactylinidae and the siphonostome associates of invertebrates are setapart from other siphonostomes by having the fifth leg bearing segment free from the genitalsomite further attests that Eudactylinidae possibly bridges the siphonostomes of invertebratesand vertebrates (Fig. 21).Several biogeography studies of fishes and their siphonostome parasites stake sometemporal markers denoting the existence (but not origin) of various siphonostome families,for example: Lernaeopodidae 50 mya (see Kabata and Ho, 1981; Ho 1989), Lernanthropidae110 mya (see Ho and Do, 1985), Eudactylinidae 35 mya (see Deets and Ho, 1988), andSphyriidae over 3 mya (see Ho, 1992). The study of Eudactylinidae by Deets and Ho (1988)is particularly notable because of the generally accepted antiquity of this family (Fig. 21;also see discussion above). Deets and Ho (1988) proposed that rajiform-parasitizingeudactylinids form a monophyletic group that originated 35 mya in the Tethys Sea. Thisrajiform-parasitizing lineage of Eudactylinidae, however, is depicted (Deets and Ho, 1988)as a derived eudactylinid group and, therefore, its presence some 35 mya detracts nothingfrom the probably much more ancient origin of the family.The only fossil parasitic copepod, Kabatarina pattersoni, provides more evidence of anancient origin for the siphonostomes parasitic on fishes. According to Cressey and Boxshall(1989) L pattersoni holds membership in Dichelesthiidae based on one unequivocal89character. Although its familial membership in Dichelesthiidae seems tenuous, pattersonishares a number of characteristics with other closely allied families such as Eudactylinidae,Kroyeriidae, Hatschekiidae, Pseudocycnidae, Hyponeoidae, and Lernanthropidae, includingthe general design of its second antennae, first maxillae, and second maxillae (see Cresseyand Boxshall, 1989). Kabatarina also exhibits some very primitive characteristics. Mostnotably, its first antennae are composed of at least 20 segments (Cressey and Boxshall,1989), and its maxillipeds display a distinct praecoxa and coxa (a condition unknown insiphonostomes of fishes but shared with many siphonostome associates of invertebrates (seeBoxshall, 1985; Cressey and Boxshall, 1989)). In all, K. pattersoni’s mixture of primitiveand derived features suggests the probable early acquisition of fishes as hosts bySiphonostomatoida, and further attests that this transition did not necessitate the wholesaleabandonment of some tried and true morphological characteristics.Therefore, it seems that associations between siphonostomes and vertebrates must beconsiderably older than 110 my. But how much older? If Siphonostomatoida ismonophyletic, and if its families parasitizing vertebrates likewise are monophyletic anddescended from ancestors associated with invertebrates, could the first siphonostomescolonizing vertebrates have emerged with the origin of fishes during the Ordovician over 441mya? Although highly speculative, data suggesting the evolution of the vertebrate olfactorysacs from branchial components along with some siphonostome distributions suggesting apossible shift from the gills into the nose encourage further consideration of such a history(see discussion above).Because the phylogenetic relationships of the siphonostomes associated with invertebratesare so poorly understood (see Gotto, 1979; Huys and Boxshall, 1991) it is difficult tonominate particular invertebrate associating taxa as having particularly close affiliation withtaxa parasitic on vertebrates. Conjecture forwarded by Kabata (1979) and Huys and90Boxshall (1991), however, accurately depicts Asterocheridae, Dirivultidae, andMegapontiidae as primitive taxa associated with invertebrates that possibly are closelyrelated to taxa infecting fishes. Nicothoidae, an associate on other Crustacea, is also notablein that it possesses a little-studied attachment organ much like the frontal filament seen inpenneffids, caligiforms, and lernaeopodiforms. Nicothoids are also interesting because theyare highly modified copepods bearing a loose overall resemblance to untransformedlernaeopodids and naobranchiids (and presumably other lemaeopodiforms), although theappendages of these groups reveals this similarity to appear superficial (e.g. cf. nicothoid andlernaeopodid morphologies presented in Kabata (1979), Boxshall and Lincoln (1983), andBoxshall and Harrison (1988)). In light of the above, it is apparent that detailed studies ofthe interfamilial relationships of the siphonostomes associated with invertebrates are neededto better resolve affinities among siphonostome families parasitic on vertebrates, and thatmolecular studies of siphonostomes may assist in unraveling relationships possibly obscuredby many morphological episodes of parallel evolution. Furthermore, the monophyletic statusof the siphonostome parasites of vertebrates cannot be fully accepted until a phylogeneticanalysis of all siphonostome families is completed. Here it is interesting to note a recentphylogenetic analysis of Poecilostomatoida (Ho, 1991) that indicated that the ten vertebrateinfecting poediostome families originated independently from three different clades ofinvertebrate infecting families.SUMMARY AND CONCLUSIONSIn this thesis, a phylogeny for the 18 siphonostome families parasitic on vertebrates has beenpresented which considers these taxa monophyletic. Although a spectacular set of fossils hasfirmly established these copepods’ presence during the Cretaceous (110 mya), host andhabitat distributions are consistent with a possible origin along with the earliest fishes during91the Ordovician (over 441 mya), and that these copepods evolved from ancestors associatedwith invertebrates.Siphonostomes that infect vertebrates typically are found attached at specific locations ontheir hosts. Most copepod distributions remain inexplicably confined, although morphologycan sometimes be used to explain realized niches. Contemporary distributions suggest thatthe branchial chambers and olfactory capsules were the first regions of the vertebrate bodycolonized. Parasite distribution and host morphology data also suggest that the olfactorycapsules of vertebrates may have been derived from some premandibular branchialcomponent and their evolution in turn caused an evolutionary split in some portions of theparasite fauna infecting the branchial chambers of noseless and jawless fishes. The generalbody surfaces of vertebrates were probably colonized by taxa formerly infecting the gills andolfactory capsules. This invasion may have been facilitated by the development of a newstructure of larval attachment, the frontal filament, which securely tethered larvae to theiractive hosts. In addition to the frontal filament, adults of these larvae appear to havedeveloped two modes of extending this progress in attachment security throughoutadulthood. One mode is seen as the derived cephalothorax of many caligiforms, and endowsthese copepods with the ability to swim powerfully in addition to providing a strong methodof suctoral attachment that can be used on the relatively slick external body surfaces of manyswift swimming fishes. The second mode is seen in the form of permanently attached adultfemale copepods, and is realized in two general ways. The first consists of permanentattachment either by encircling a host gill filament with the second maxillae(Naobranchiidae), or by actually anchoring the second maxillae to the host (Lernaeopodidaeand Tanypleuridae). The second form involves an ecological shift from ectoparasitism tomesoparasitism (Penneffidae and Sphyriidae).92The primitive life cycle of the siphonostomes infecting vertebrates consists of ten stages.A reduction in the number of molts required to reach adulthood is exhibited by a number oflineages and seems to have been realized through amalgamation of free-living nauplius,and/or parasitic copepodid, chalimus or preadult stages. The first copepodid is maintainedthroughout all lineages as the initial colonizing stage. Sexual dimorphism ranges from subtleto pronounced, with male modifications seemingly associated with the location and graspingof females, whereas female modifications appear to be directed towards requirementsimposed by parasitism and reproduction.Although most siphonostomes have one host life cycles, at least some pennellids haveevolved two host lifestyles. The evolution of these two host cycles seems to have beenfacilitated by both use of a highly mobile untransformed adult female to infect the definitivehost, as well as, by the close ecological proximity of the intermediate and definitive hostspecies either through the use of the same densely schooling species for both portions of thelife cycle, or through a predator-prey linked association of two dissimilar species.Among siphonostome taxa infecting vertebrates, mesoparasitism has apparently evolvedseveral times from ectoparasitic taxa. Phylogenetic data illustrate that once a lineage hasbeen initiated into mesoparasitism, reversal to ectoparasitism is unlikely. Possiblerequirements of shedding larvae into an open environment may represent the only constraintprecluding these mesoparasitic lineages from an endoparasitic lifestyle.Two siphonostome lineages have successfully invaded fresh water. This significantecological shift appears to have been facilitated, although not absolutely determined, by anumber of morphological, developmental, and ecological traits.93Preliminary studies suggest that siphonostomes have sometimes coevolved with theirvertebrate hosts while at other times they have colonized phylogenetically distant yetecologically similar hosts. Although rich in species, overall numbers suggest that thespeciation rate of these copepods seems to have lagged behind that of potential host taxa. Nodoubt the ever changing array of host species available for infection has and continues tochallenge this most successful crustacean taxon of vertebrate parasites.Evolutionarily, parasitism represents one logical culmination of the intimate associationbetween two species, and considering absolute numbers of species, parasitism may be themost successful heterotrophic lifestyle. As such, parasitism is an ecological rather than aphylogenetic phenomenon. 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Anat. 60,289-344.108TABLESTable1ApomorphylistsupportingFigure21aCharacterDescription1Eachmandiblebearingaprominentrowofteethalongoneside2Secondantennaelackingprominentexopods3Longuniseriateeggsacs4Mandibularpaipabsent5Fifththoraciclegsincorporatedintogenital doublesomitetoformgenitalcomplex6Chelatesecondantennae7Fourththoraciclegshighlymodifiedorcompletelylost8Secondmaxillaewithbifidclaws9Maxillipedsabsent10Highlymodifiedbiobatefourthlegs11Grooveonsecondmaxilladelimitingdistalportionofbrachiumfromcalamus12Frontalorganpresent,frontalfilament usedtotethersomelarvalstagestohost13Markedreductioninsegmentationoffirstantennae14Labrumandlabiwnfusedtoformadistinctivemouthtube15Eggarrangementmultiseriate16Allthoraciclegsabsentorvestigial17Highlymodifiedgrub-likemalesanduntransformedfemales18Secondmaxillaeusedasprimaryorgansofattachment19Secondmaxillaeattachedtobullatoanchoradultfemale20Secondmaxillaelong,ribbon-like,usedtoencirclehosttissues,tipsattachedtotrunk21Cephalothoraxinformofdorsalshield22Frontalplatesoncephalothorax23Firstmaxillawithlargedentiformendopodandsmallexopodwiththreespiniformsetae24Firstmaxillawithreduceddigitiformendopod25Corpusmaxillipedissquatwithmodifiedmyxa,subchelaataboutarightangletolongaxisofcorpuswhenclosed26Secondpedigeroussegmentincorporatedintothecephalothorax27Firstmaxillaedistinctivelycomposedoftwoparts28Thirdpedigeroussegmentincorporatedintothecephalothorax29Thirdthoraciclegsandinterpodalplatemodifiedandfusedtofonuasealforthecephalothorax30FourththoraciclegsuniramousaCharactersrefertoconditionseenintheadultfemaleunlessotherwisenoted.CharacternumberscorrespondtothoseinFigs21and27.Atuapomorphiccharactersareonlyidentifiedtoresolvepolychotomiesortonotecharacteristicsofsignificancetodiscussion.Fordiscussionofcharactersconsulttext.GeneralGillsandSharkbodybranchialOlfactoryBuccalTotalspeciesaNsurfacechamberssacschamberbodyBigeyethresher831-4Threshershark711--2Whiteshark743-18Shortfinmalco12124-27Nightshark153-1-4Bignoseshark1152--7Tigershark94-4-6Blueshark78441-9Scallopedhammerhead35521-8AllSharksb2914242219100(33spp.)Table2NumbersofcopepodspeciesinfectingvariousbodyregionsofsomesharksinthewesternNorthAtlantic(Benz,unpublisheddata)I I CaCommonnamesofsharksaccordingtoRobinsetat.(1991).bCopepodspeciesfromeachregionreportedaspercentoftotalbodyvalue.SaTflOHITT112FIG. 1 Examples of sexual dimorphism in the adult general habitus of some siphonostomesinfecting vertebrates. A, Eudactylinidae; B, Kroyeriidae; C, Dichelesthiidae; D, Pennellidae;E, Trebiidae; F, Phvllothvreus (Edwards, 1840); G, Cecropidae; H, Sphyriidae; I,Lernaeopodidae. Identification labels separate sexes (female always on left); D and I eachdepict (left to right) untransformed adult female, transformed adult female, and adult male.For explanation see text. Figures modified from Kabata and Cousens (1973) and Kabata(1979). Scale bars represent: 0.5 mm on A, B, D (untransformed female and male), and I;2.0 mm on C, D (transformed female), E, F, 0, and H.113114FIG. 2 Ecological summary cladogram of Eudactylinidae genera, considering from top tobottom: host group, lifestyle, and general attachment location. Phylogenetic relationships ofcopepods as proposed by Deets and Ho (1988), ecological data from numerous primarysources. Bladders on cladogram denote synapomorphic support from cladogram of Deetsand Ho (1988).ElasmobranchsITeleoststctoparasitic—GillsElasmobranchs—MesoparasiticIEctoparasiticOlfactoryOralandSacsandBrancliialGillsGillsChambersU,116FIG. 3 Two Nemesis species infecting different regions of the gill ifiaments of lamnidsharks. Top, Nemesis lamna Risso, 1826 infecting gill filaments of the shortfin mako (Isurusoxvrinchus Rafmesque, 1810). Nemesis lamna usually attaches at the dorsal (this instance)and ventral aspects of a gill arch some distance in from the tip of a gill filament; Bottom,Nemesis robusta (van Beneden, 1851) infecting gill filaments of the thresher shark (Alopiasvulpinus (Bonnaterre, 1758)). Note how Nemesis robusta aggregate about the gill arch andattach about the efferent tips of the gill filaments. Top from Benz (1980), Bottom from Benzand Adamson, 1990).118FIG. 4 Kroveria carchariaeglauci Hesse, 1879 females parasitic on gills of a blue shark(Prionace 1auca (L., 1758)). Top, individual residing in water channel between two gillfilaments. Note chelate second antennae grasping the host substrate and the dorsal styletprojecting upwards toward the secondary lamellae; Bottom, a dorsal stylet propped against asecondary lamella of a gill filament. Top and Bottom from sectioned material.119— s.q•I.4120FIG. 5 Kroveria casevi Benz and Deets, 1986 females embedded in the interbranchialseptum of a night shark (Carcharhinus signatus (Poey, 1868). Note the collar of host tissuesurrounding the parasites where they penetrate the host (from Benz and Deets, 1986).t%j122FIG. 6 Sectioned elasmobranch gill (diagrammatic) illustrating niches typically inhabited bysome siphonostomes (clockwise from top left): Pandarus cranchii Leach, 1819 on gill arch;Eudactvlinodes uncinata (Wilson, 1909) and Bariaka alopiae Cressey, 1966 on secondarylamellae; Nemesis lamna Scott, 1929 and Lernaeopodina longimana (Olsson, 1869) oncapping tissue surrounding efferent arteriole; Phvllothvreus cornutus (Edwards, 1840)superfically on interbranchial septum; Paeon vaissieri Delamare Deboutteville and NunesRuivo, 1954 and Kroveria casevi Benz and Deets, 1986 partially embedded in interbranchialseptum; Gangliopus pvriformis Gerstaecker, 1854 on secondary lamellae; Kioveria lineatavan Beneden, 1853 in water channel and on secondary lamellae; Lernaeopodina longimanaand Anthosoma crassum (Abildagaard, 1794) on gill arch. Distribution records of parasitesfrom the author’s personal observations. Abbreviations: GA, gill arch; GF, gill ifiament; IS,interbranchial septum.124FIG. 7 Lernanthropus pomatomi Rathbun, 1887 female from gill filaments of a bluefish(Pomatomus saltatrix L., 1758). Note how edges of cephalothorax curl ventrally to form atunnel-like pathway through which one host gill filament can pass. The claw-like secondantennae and chelate maxillipeds can be seen positioned along this pathway, where theysecure the filament in their grasps. Note also the highly modified third pair of thoracic legswhich form a more posterior passageway which assists in attachment and in maintaining theparasite in line with the gill filament in the face of respiratory water flow.cJ,126FIG. 8 Sectioned teleost gill (diagrammatic) illustrating niches typically inhabited by somesiphonostomes (clockwise from top left): Clavella adunca (Strøm, 1762) and Caligusproductus Dana, 1852 on gill arch and gill rakers; Lernanthropus species on capping tissue ofsurrounding efferent arteriole; Naobranchia species encircling gill filament; Lemanthropusspecies on tissue surrounding afferent arteriole; Clavella adunca on capping tissuesurrounding efferent arteriole; Hatschekia species on secondary lamellae; Haemobaphesspecies and Lernaeocera species cephalothorax and portion of trunk penetrating afferentartery and often coursing to heart. Distribution records of parasites from the author’spersonal observations. Abbreviations: GA, gill arch; GF, gill filament.‘GF128FIG. 9 Pennella instructa Wilson, 1917; mesoparasitic females embedded in swordfish(Xiphias gladius L., 1758). Top, posterior body portions of two females trailing free fromhost (arrow marks point of parasite entry); Bottom, close-up of two different femalesshowing abdominal plumes which give the external portion of these parasites an arrow’s shaftappearance. Length of white ruler approximately 15 cm.129-..130FIG. 10 Ecological summary cladogram of Penneffidae genera, considering from top tobottom: definitive host group, intermediate host group, and lifestyle. Phylogeneticrelationships of copepods as proposed by Boxshall (1986). Ecological data from numerousprimary sources. Bladders on cladogram denote synapomorphic support from cladogram ofBoxshall (1986).Teleosts-iTeleostsandCetaceansTeleosts1TeleostsCephalopodsGastropodsEctoparasiticI.\ii UMesoparasitic-iEctoparasitic1—Mesoparasitic—,2’1, II‘I Li132FIG. 11 Ventral view of female Pandarus bicolor Leach, 1816 showing major structures ofattachment. Abbreviations: a2, second antenna; api, adhesion pad associated with firstantenna; ap2, adhesion pad associated with second antenna; ap3, postoral adhesion pad; ap4,adhesion pad associated with first free thoracic segment mxp, maxilliped. Electronmicrograph.-DI-,’‘V.—rIc.- 1‘I134FIG. 12 Second maxillae of some pandarid species. Top left, Pandarus bicolor Leach, 1816,adult female; Top right, clavus of E. bicolor. adult female; Bottom left, Echthrogaleuscoleoptratus (Guerin-Meneville, 1837), adult female; Bottom right, Echthrogaleus sp.copepodid. See text for explanation. Abbreviations: ci, ciavus; cr, crista; ?, projectioncrowned with this spinules.136FIG. 13 Cephalothorax rim of two pandarid copepods. Top, inner edge of femaleEchthroaleus coleoptratus (Guerin-Meneville, 1837) cephalothorax. Note marginalmembrane and basal rank of spines; Bottom, inner edge of female Pandarus bicolor Leach,1816 cephalothorax. Note how border Consists only of membranous rays that becomeamalgamated into spines along the outer edge. Echthrogaleus coleoptratus typically resideson portions of a shark’s body where the placoid scales are very fine (see Benz, 1986) andwhere the combination of a marginal membrane and row of spines about its cephalothoraxwould seem highly useful in both sealing the cephalothorax to the host and in gripping thehost. Pandarus species are normally found attached to their shark hosts where the placoidscales are large (see Benz, 1981, 1992) and where a row of stout spines about thecephalothorax would serve to assist in gripping the host.‘IF%‘zr—:tT..V...—...e-4.;..•d.c$$••q,r.....:—--.••.--Iq.—•..—.—•——‘_•‘—_!I-—-—•qp.—II. I I II-Ipi138FIG. 14 Female Phvllothvreus cornutus (Edwards, 1840) attached to blue shark (Prionaceglauca (L., 1758)) interbranchial septum. Note claw-like second antennae deeply penetratinghost. From sectioned material.‘.0‘s.&r tA(1c•4ji4*’ N —t4140FIG. 15 Female Pandarus bicolor Leach, 1816 maxillipeds. Top, empty maxilliped;Bottom, maxilliped clasping a host placoid scale. Note how bifid tip of claw meets neck ofplacoid scale and how the grasping action of the maxilliped forces the scale’s crown againstthe myxal pad and lateral myxal projection. Top and Bottom electron micrographs.Abbreviations: ci, claw; lmp, lateral myxai projection; mp, myxal pad; ps, placoid scale.141impmp(cicII,. ciPSL iih-mp Irrjp•142FIG. 16 Second antenna of female Perissopus oblongatus (Wilson, 1908). The toothed apexis buried deep into host tissues to secure this species. Electron micrograph.144FIG. 17 Female Perissopus dentatus Steenstrup and Lütken, 1861. Top, lateral view ofcephalothorax showing maxilliped still attached to many host placoid scales; Bottom,maxilliped free of placoid scales showing scale impressions in the gluey substance whichcovers the myxal pad. Top and Bottom electron micrographs.C C 3I-aU,146FIG. 18 Cluster of ovigerous female Alebion crassus Wilson, 1932 below trailing edge ofthe first dorsal fin of a scalloped hammerhead (Sphvrna lewini (Griffith and Smith, 1834).L1T148FIG. 19 Alebion lobatus Cressey, 1970 copepodids infecting a sandbar shark (Carcharhinusplumbeus (Nardo, 1827)). Top, scatter of perforations caused by invading copepodids;Bottom, electron micrograph of copepodid nestled in a lesion surrounded by placoid scales.Top and Bottom from Benz (1989).61i1150FIG. 20 Large gathering of Ca1ius productus Dana, 1852 on the roof of the buccal cavity ofa yellowfin tuna (Thunnus albacares (Bonnaterre, 1788)).is-i:152FIG. 21 Hypotheses of phylogenetic relationships of siphonostome families parasitic onvertebrates. Numbers refer to character states listed in Table 1, asterisks denotehomoplasious characters, character reversals are indicated by solid circles (copepods redrawnfrom Kabata, 1966a, 1968, 1969b, 1979; Ho, 1987).154FIG. 22 Mouth tubes of two elasmobranch infecting pandarid siphonostomes. A, Pandarussatvrus Dana, 1852, female; B, Dinemoura latifolia (Steenstrup and Lütken, 1861), female.Note how the mouth tube of Dinemoura possesses a fringing skirt seemingly capable ofsealing the tip to the host, while in Pandarus the tip is pointed and possesses robust spineswhich appear able to anchor the mouth tube within host tissues. Note also that the invasivetip of Pandarus is considerably narrower than the sealing tip of Dinemoura. A and B drawnfrom electron micrographs. Abbreviations: ib, labium; fr, labrum; m, mandible.U,156FIG. 23 Frontal gland on ventral surface of the cephalothorax of two adult female pandarids.Top, Pandarus cranchii Leach, 1819; Bottom, Echthrogaleus coleontratus (Guerin-Meneville,1837). Top and Bottom electron micrographs.i-1_CjU,t158FIG. 24 Sternal elements of two caligiform copepods. Top, sternal furca of femaleParalebion elonatus Wilson, 1911; Bottom, sternal projection of female Demoleus heptapus(Otto, 1821). Note the corrugated tip of this projection and be aware that J2 heptapus infectsthe placoid scale studded surface of sharks where the application of such a rough tipprobably assists the copepod to maintain a stationary position in the face of passing water.Top and Bottom electron micrographs._14F160FIG. 25 Maxilliped of female Phvllothvreus comutus (Edwards, 1840) grasping epithelialtissue of the interbranchial septum of a blue shark (Prionace glauca (L., 1758)). Note thatthe myxal region of this pandarid appears distally displaced and that it is grasping a hostsurface devoid of placoid scales. From sectioned material.C’162FIG. 26 Life cycle summaries for siphonostomes parasitic on vertebrates. Vertical linesdenote molts, arrows denote considerable development without molting (i.e.metamorphosis). See text for further explanation and primary references. Figure entries asfollows: C, copepodid; CR, chalimus; ECH, ephemeral chalimus (preadult) using frontalifiament for molting and exhibiting an untethered condition for most of its existence; JE,nauplius development passed while in egg; inf, first or only colonizing stage; P, pupaformlarva; TF, transformed adult female; UT, untransformed adult male and female; UTM,untransformed adult male; X, stage present; ?C, copepodid stage possibly observed; -, stageconsidered absent.CD—.€-CDCD.z•CDCD-.CDCDCDCDC300CD)0I-..CDCDCD:0-0-CDCD—.0-CD“CD‘0.._..CD0-z0.-CDCDzCDCDCDCDCDCDCD><>><I><IIIIII>cII-.C)C)C)C)C)C)C)C),-C)C)C)C)C)C)(Th0 CDC)C)C)C)(_)0 0-.C)C)C)C)C)C)0-0-C)C)C)x-C)C)C)C)I0C)IjHHHHHHHHHHHITITjrjtj164FIG. 27 Ecological summary cladogram for siphonostome families parasitic on vertebrates(considering from top to bottom: environmental habitat, major host groups, lifestyle, andgeneral attachment location on host). Entries in parentheses denote relatively minorrepresentation. Ecological data from numerous primary records. Phylogenetic relationshipsof copepods as proposed in Fig. 21. Numbers on phylogeny correspond to supportingmorphological characters (see Table 1), homoplasious characters are denoted by asterisks,character reversals are indicated by solid circles.-I.-Cl)-4.10-EUDACTYLINIDAEKROYERITDAEHATSCHEKJJDAEPSEUDOCYCNIDAEHYPONEOIDAELERNANTHROPIDAEDICHELESTNIIDAEPENNELLIDAEDISSONTDAEPANDARJDAECECROPIDAETREBIIDAEEURYPHORIDAECALIGIDAESPHYRTIDAELERNAEOPODIDAENAOBRANCIIIIDAETANYPLEURIDAETh2C)1tj—c IzcIi..J0IJ7-OCl)0-Cl)Cl)10•‘1Cl)I1X-Cl)CMI•)—.—I0-,:—‘Sr4. ‘•23. -I0 I_1:zI lCl)I13IrX0Li Ir,I.iZ I-i_Jz10Cl) ,I.IIII-1C,1) Cl)II)II1I,JJJMIC.)MU’MI‘I-41-4CD.S91166FIG. 28 Comparison of the gills and olfactory sacs of elasmobranchs. Top, seriesillustrating (left to right) how a gill can be modified to form an olfactory sac. Arrows denotedirections of water flow; Bottom, gill (left) and olfactory sac (right). Note how both gillsand olfactory sacs possess orderly arrangements of serially repeating components (i.e.filaments and lamellae) radiating from a supporting rod (i.e. gill arch and rachis). Note alsohow kroyeriid and some pandarid copepods infect similar (homologous?) regions within eachenvironment. Abbreviations: GA, gill arch; GF, gill filament; GSL, gill secondary lamella;K, kroyeriid copepod; OF, olfactory filament; OSL, olfactory secondary lamella; P, pandaridcopepod; R, rachis; WC, water channel. Figure prepared with data from Benz (1984, inpreparation).GillOlfactorySac168APPENDIX169Appendix 1. List of species and collections examined during the phylogenetic analysis ofsiphonostomes parasitic on vertebrates. Abbreviations: ARCHML, AtlanticReference Centre Huntsman Marine Laboratory (St. Andrews, N.B.); BCPM, BritishColumbia Provincial Museum; BENZ, Personnal collection of the author; BMNII,British Musuem of Natural History; DEETS, Personnal collection of Gregory B.Deets (University of British Columbia); IZAWA, Personnal collection of KunihikoIzawa (Mie University); SAMA, South Australian Museum in Adelaide; SAMCT,South African Museum (Cape Town); SHUNO, Collection of Sueo Shiino (MieUniversity); USNM, United States National Museum.Eudactylinidae:Bariaka alopiae Cressey, 1966: BENZ Coil. Nos. A128, A131.Eudactvlina sp.: BENZ Coil. No. B6.Eudactvlinodes keratophagus Deets and Benz, 1986: USNM Coil. Nos. 231378 (Holotype),231379 (Paratypes).Jushevus shogunus Deets and Benz, 1987: USNM Coil. Nos. 231384 (Holotype), 231385(Ailotype).Nemesis lamna Scott, 1929: BENZ Coll. Nos. A59, A80, A 128, A131, A140, A180, A426,A454, A457, A458.Nemesis robusta (van Beneden, 1851): BENZ Coil. Nos. B80, B 122, B417, B478.Nemesis spinulosus Cressey, 1970: BENZ Coil. Nos. B 124, B 125, B 126.Kroyeriidae:Kroyeria carchariaeglauci Hesse, 1879: BENZ Coil. Nos. A86, A142, A219, A225, A226,A524, A525, A526.Kroveria casevi Benz and Deets, 1986: USNM Coil. No. 231376 (Holotype); BENZ Coil.Nos. BlO (Allotype), Bli (Paratypes).Kroyeria dispar Wilson, 1935: BENZ Coil. No. A2.Kroeverina elongata Wilson, 1932: BENZ Coil. Nos. B17, B70, B71, B72, B73, B424.Kroverina scottorum Cressey, 1972: BENZ Coil. Nos. B74, B75, B76, B422, B423.Pseudocycnidae:Pseudocycnus appendiculatus Heller, 1865: BENZ Coil. No. A379.170Dichelesthiidae:Anthosoma crassum (Abiidgaard, 1794): BENZ Coil. Nos. A590, B62, B64, D12.Kabatarina pattersoni Cressey and Boxshafl, 1989: BMNH Coil. Nos. 63466, 63467, 63468,63469, 63470, 63625, 63626, 63627.Lernanthropidae:L.emanthropinus nematistil Deets and Benz, 1988: BCPM Coil. Nos. 986-274-1 (Holotype),986-274-2 (Allotype).Lernanthropus brevoortiae Rathbun, 1887: BENZ Coil. Nos. A147, A148.Lernanthropus pomatomi Rathbun, 1887: BENZ Coil. No. B 101.Penneffidae:Haemobaphes intermedius Kabata, 1967: BENZ Coil. No. B470.Lernaeenicus longiventris Wilson, 1917: BENZ Coil. No. B301.Lernaeenicus radiatus Le Sueur, 1824: BENZ Coil. No. A148.Lernaeenicus sp.: BENZ Coil. No. B414.Penneila fliosa (L., 1758): BENZ Coil. Nos. B42, B43, B202; USNM Coil. Nos. 180162,180163.Pennella instructa Wilson, 1917: BENZ Coil. Nos. D7, D10.Prixocephalus sp.: BENZ Coil. No. A 164.Dissonidae:Dissonus spinifer Wilson, 1906: USNM Coli. No. 56592.Pandaridae:Demoleus heptapus (Otto, 1821): BMNH Coil. Nos. 1911.11.8.48111, 1911.11.8.48112;USNM Coil. No. 60465.Dinemoura discrepans Cressey, 1967: BENZ Coil. Nos. B19, A130.Dinemoura latifoiia (Steenstrup and Lütken, 1861): BENZ Coil. Nos. A98, A106, Alil,A265, A534, A535, A536.Dinemoura producta (Muller, 1785): BENZ Coil. Nos. B26, B28; BMNH Coil. No.1940.; SAMA Coil. Nos. TC2294, TC2295.171Echthrogaleus coleoptratus (Guerin-Meneville, 1837): BENZ Coil. Nos. A248, A262, A399,A401, A521.Echthrogaleus denticulatus Smith, 1874: BENZ Coil. Nos. A593, A594, A595, A596, A598.Echthrogaleus clisciarai Benz and Deets, 1987: USNM Coil. Nos. 231380 (Holotype),231381 (Ailotype), 231382 (Paratype), 231383 (Paratype).Echthrogaleus torpedinis Wilson, 1907: BENZ Coil. No. B24; USNM Coil. No. 11350(Syntypes).Gangliopus pvriformis Gerstaecker, 1854: BENZ Coil. Nos. A543, A544; USNM Coil. Nos.153570, 153572, 153574.Nesippus orientalis Heller, 1868: ARCHML Coil. No. 8750866; BENZ Coil. Nos. B67, B68.Nesippus tigris Cressey, 1967: BENZ Coil. No. A339.Paging tunica Cressey, 1964: BENZ Coil. Nos. A129, A153.Pandarus bicolor Leach, 1816: BMNH Coil. Nos. 197, 1975.679, 1975.689; USNMCoil. No. 305795.Pandarus cranchii Leach, 1819: BENZ Coil. Nos. A193, A200, A256, A539.Pandarus floridanus Cressey, 1967: BENZ Coil. Nos. A428, A434, A436.Pandarus satvrus Dana, 1852: BENZ Coil. Nos. A206, A212, A213, A220, A268.Pandarus sinuatus Say, 1817: BENZ Coil. Nos. A24, A303, A325.Pandarus smithii Rathbun, 1886: BENZ Coil. Nos. A239, A252, A255, A517.Pandarus zvgaenae Brady, 1883: BENZ Coil. Nos. A278, A298.Pannosus japonicus (Shiino, 1960): SHUNO Coil. No. 493 (Holotype).Paranesippus incisus Shiino, 1955: SHI1NO Coil. No. 94 (Holotype).Perissopus dentatus Steenstrup and Lütken, 1861: BENZ Coil. Nos. A51, A438; BMNHCoil. Nos. 1911.11.8.45203, 1969.3.14.2, 1984.132; USNM Coil. Nos.154171, 154210.Perissopus oblongatus (Wilson, 1908): BENZ Coil. No. B31; BMNH Coil. No. 1974.700.Phvflothvreus cornutus (Edwards, 1840): BENZ Coil. Nos. A346, A402, A540, A542;BMNH Coil. No. 84. 14.”Chailenger”.Pseudopandarus gracilis Kirtisinghe, 1950: BMN}I Coil. No. 1984.131; USNM Coil. No.753760.172Cecropidae:Cecrops latreiffi Leach, 1816: BENZ Coil. Nos. A414, A522, A523.Entepherus laminipes Bere, 1936: DEETS unaccessioned specimens.Orthagoriscicola muricatus (Krøyer, 1837): BENZ Coil. No. B214.Trebiidae:Trebius caudatus Krøyer, 1838: USNM Coil. No. 8033.Euryphoridae:Alebion carchariae Krøyer, 1863: BENZ Coil. Nos. A82, A83, A321, A322, A332.Alebion crassus Wilson, 1932: BENZ Coil. Nos. A253, A258, A277, A289, A290.Alebion glaber Wilson, 1905: SAMA Coil. Nos. TC2290, TC2293.Alebion lobatus Cressey, 1970: BENZ Coil. Nos. A272, A273, A295.Eurvphorus brachvnterus (Gerstaecker, 1853): BENZ Coil. Nos. B49, B 107.Gloiopotes hygomianus Steenstrup and LUtken, 1861: BENZ Coil. Nos. A381, A383.Gloiopotes watsoni Kirtisinghe, 1934: BENZ Coil. Nos. A63, A64.Paralebion elongatus Wilson, 1911: BENZ Coll. Nos. B261, B262, B263; USNM Coil. No.256546.Caligidae:Caligus chelifer Wilson, 1905: BENZ Coil. No. A53.Caligus corvphaenae Steenstrup and LUtken, 1861: BENZ Coil. Nos. A380, A382, A406,A412, A556, A580.Caligus curtus MUller, 1785: BENZ Coil. Nos. A89, A217.Caligus productus Dana, 1852: BENZ Coll.Nos. A398, A404, A405, A409, A410, A582,A583, A584, A585.Lepeophtheirus nordmanni (Edwards, 1840): BENZ Coil. No. A415.Lepeophtheirus salmonis (Krøyer, 1837): BENZ Coil. Nos. B442, B503, B504.173Sphyrlidae:Opimia sp.: BENZ Coil. No. A403.Periplexis lobodes Wilson, 1919: BENZ Coil. No. A132.Lernaeopodidae:Acbtheres pimelodi Krøyer, 1863: BENZ Coil. Nos. B88, B115, B390.Aibioneila etmopteri (Yamaguti, 1939): IZAWA Coil. Nos. K-424, K-455, K-500, K-582;SAMCT Coil. No. SM107.Aibioneila kabatai Benz and Izawa, 1990: USNM Coil. No. 254426 (Hoiotype).Albioneila oviformis (Shilno, 1956): SHIINO Coil. No. 480 (Holotype).Brachiella thvnni Cuvier, 1830: BENZ Coil. Nos. A354, A355.Claveila adunca (StrØm, 1762): BENZ Coil. Nos. A61, A62, A216.Lemaeopodina longimana (Olsson, 1869): BENZ Coil. Nos. B250, B291.Nectobrachia indivisa Fraser, 1920: BENZ Coil. Nos. B336, B337.Salmincola califomiensis (Dana, 1852): BENZ Coil. No. B310.NaobranchiidaeNaobranchia lizae (Krøyer, 1864): BENZ Coil. No. B 149.


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