PARASITE BIOGEOGRAPHY : A REVIEW OF THE ORIGINS AND IDEAS WITH SPECIFIC EXAMPLES FROM HOLARCTIC FISHES J Carney, T Dick

To cite this version:

J Carney, T Dick. PARASITE BIOGEOGRAPHY : A REVIEW OF THE ORIGINS AND IDEAS WITH SPECIFIC EXAMPLES FROM HOLARCTIC FISHES. Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, 2000, pp.221-243. ￿hal-03186918￿

HAL Id: hal-03186918 https://hal.sorbonne-universite.fr/hal-03186918 Submitted on 31 Mar 2021

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. VIE ET MILIEU, 2000, 50 (4) : 221-243

PARASITE BIOGEOGR APH Y : A REVIEW OF THE ORIGINS AND IDEAS WITH SPECIFIC EXAMPLES FROM HOLARCTIC FISHES

J.P. CARNEY, T.A. DICK Department of Zoology, University of Manitoba, Winnipeg Manitoba, Canada, R2T 2N2 E-Mail: tadick@cc. UManitoba. CA

HOST-PARASITE BIOGEOGRAPHY ABSTRACT. - The origins and major ideas underpinning parasite biogeography HOLARCTIC started in western Europe and North America with von Ihering who used parasites HISTORICAL ECOLOGY to study host distributions. A similar approach was used by Metcalf, Johnston, Har- FISH PARASITES rison and Manter whereas Dogiel and coworkers used parasites of fish to recognize différent biogeographic zones. More recently, Brooks advanced the field by intro- ducing phylogenetic systematics as a method to investigate parasite biogeography and historical ecology. Although infrequently combined to date, two complementa- ry approaches to parasite biogeography are historical and ecological. Historical bio- geography considers questions relating to the origins of parasite distributions and host associations while ecological biogeography is concerned with contemporary factors that contribute to présent distributions and abundances. Data from Holarctic fishes are used to outline ideas relevant to parasite ecological biogeography at the scale of continental distributions. Thèse data support the hypothesis that most of the parasites have continental distributions even though the hosts have interconti- nental distributions. While hosts contribute to the distribution of parasites, many parasites of Holarctic fishes show stronger affinities to geography than to the host. This suggests that parasite distributions, although ultimately dépendant on a host, are influenced by factors in addition to host factors. Strict host-specificity does not confirm coevolutionary roots for predictable host-parasite associations. However, predictable associations exist at higher taxonomic levels and thèse may or may not have coevolutionary origins. Widespread parasite distributions can be a consé- quence of having numerous hosts across taxa. Historical ecological associations and sympatric hosts sharing food items that transmit parasites, ensures homogeni- zation of the parasitofauna. Predictable associations at higher host taxonomic le- vels, combined with widespread Holarctic distributions at higher parasite taxonomic levels, suggests an ancient origin for many of thèse parasite species. Thèse observations are true for parasites of Holarctic fish species and may also be true for fish parasites in the north-south axis of the major continents. The combina- tion of widespread distribution of parasite species with numerous fish hosts, and endémie parasite species with restricted géographie and host associations, makes parasites fruitful models for comprehensive biogeographic studies.

BIOGEOGRAPHIE DES PARASITES RÉSUMÉ. - les origines et notions fondamentales de la biogéographie des parasites ET DES HÔTES remontent aux travaux de von ihering qui se servit de parasites afin d'étudier la ré- HOLARCTIQUE partition des hôtes dans la partie ouest de l'Europe et en Amérique du Nord. Met- ÉCOLOGIE HISTORIQUE PARASITES DE POISSONS calf, Johnston, Harrison et Manter utilisèrent une approche similaire, tandis que Dogiel et ses collaborateurs se servirent de parasites de Poissons pour reconnaître les différentes zones biogéographiques. Plus récemment, des progrès dans le do- maine ont été réalisés par Brooks qui s'est servi de la systématique phylogénétique comme méthode d'étude de la biogéographie des parasites et de l'écologie histo- rique. Bien qu'étant rarement associées, l'histoire et l'écologie sont deux approches complémentaires de la biogéographie des parasites. La biogéographie historique tient compte des questions relatives aux origines des associations d'hôtes et de la répartition des parasites, tandis que la biogéographie écologique se rapporte aux facteurs contemporains qui contribuent aux répartitions et aux abondances présen- tes. Les données brutes sur les Poissons Holarctiques servent à mettre en valeur les idées pertinentes de la biogéographie écologique des parasites à l'échelle continen- tale de la distribution. Ces données confirment l'hypothèse selon laquelle la plupart des parasites se répartissent en fonction des continents même si les hôtes se répar- tissent sur plusieurs continents. Alors que les hôtes contribuent à la répartition des parasites, de nombreux parasites de Poissons Holartiques dépendent plus de la géo- 222 CARNEY Y, DICK TA

graphie que de leurs hôtes. Cela sous-entend que même si la répartition des parasi- tes dépend finalement d'un hôte, les facteurs qui influencent cette répartition ne proviennent pas uniquement de cet hôte. La stricte spécificité des hôtes ne confirme pas les causes co-évolutives des associations prévisibles parasites-hôtes. Cepen- dant, on peut prévoir des associations à des niveaux de taxonomie plus élevés, que ces associations aient ou non des origines co-évolutives. Les répartitions très répan- dues de parasites peuvent être une des conséquences du nombre important d'hôtes parmi les nombreux groupes taxonomiques. Les associations écologiques à travers le temps et les hôtes découverts au même endroit et qui ont partagé la même nourri- ture transmettant les parasites, assurent une homogénéisation de l'ensemble des pa- rasites. A des niveaux taxonomiques plus élevés, des associations prévisibles d'hôtes combinées à la répartition Holarctique de parasites très répandue, suggèrent que la plupart de ces espèces de parasites ont eu une toute autre forme de vie dans le passé. Ces observations sont vraies en ce qui concerne les parasites de l'espèce des Poissons Holarctiques et il se peut qu'il en soit de même en ce qui concerne les parasites de Poissons de l'axe nord-sud des continents majeurs. Des espèces de pa- rasites à vaste répartition combinées avec de nombreux Poissons-hôtes, et des espè- ces endémiques de parasites confrontées à une géographie restreinte et des associations d'hôtes, font des parasites des modèles fructueux pour de vastes études biogéographiques.

ecological and historical biogeographic approaches INTRODUCTION are not exclusive, only recently are there studies di- rectly reporting both (Choudhury & Dick in re- view, Carney & Dick in review). Biogeography is defined as the science that stud- ies géographie distribution and abundance of or- The purpose of this review is to summarize ganisais (Darlington 1957, Brown & Gibson 1983). briefly some of the significant historical contribu- Thèse studies may incorporate data from geology, tions of parasite biogeography, consider methods palaeontology, systematics, évolution, behaviour to investigate parasite biogeography, and outline and ecology. Unlike free-living organisms, parasite some current contributions from parasitology to the biogeography is not limited to explaining geo- study of historical biogeography and ecological graphical distribution and abundance patterns, as biogeography. Data from Holarctic fishes will be the distribution and abundance of parasites in their used as examples to illustrate ecological aspects. hosts also can be investigated. Such studies can Thèse data will show that, although parasites by range in scale from explaining différences in the définition require a host, their distributions show distribution and abundance of parasites in host in- géographie affinities ranging in scale from water- dividuals to how parasites distribute and associate sheds to continents that may not correspond ex- with host taxa. Host related attributes such as be- actly with host distribution. As a conséquence par- haviour, feeding, âge, size, immunological status asites are a good model to study biogeography. and host distributions, as well as abiotic factors that are frequently water related contribute to the distribution and abundance of parasites in hosts. CONCEPTS There are two gênerai and complementary ap- proaches to parasite biogeography: historical and ecological. Historical parasite biogeography is in- The effect of scale is important when studying terested in the evolutionary origins for parasite parasite distributions and abundance as parasites géographie distributions and host associations and and their communities occur hierarchically. This dépends on estimâtes for the phylogeny of the taxa, allows studies at the scale of the individual host both parasite and host. Thèse phylogenies form the (infrapopulation or infracommunity [Bush & basis for determining géographie patterns among Holmes 1986]), within the population of a single monophyletic taxa and congruence in thèse pat- host species (component community [Holmes & terns is taken as évidence for common cause for the Price 1986]) within ail hosts in a given géographie distribution of thèse organisms. Ecological parasite location (compound community) and how they dis- biogeography describes présent zoogeographic distri- tribute with différent hosts across continental butions, abundances, and host associations of para- scales. Approaches to questions at one scale may sites, and how thèse distributions and associations are be inappropriate for questions at another scale. For maintained. Explanations are found in parasite and example, host attributes such as âge, feeding be- host ecology, behaviour and physiology. Historical haviour, or immunological compétence may affect and ecological approaches are mutually reinforcing the distribution of a parasite species among indi- but are rarely studied in concert. Although thèse vidual hosts. On the other hand, thèse attributes PARASITE BIOGEOGRAPHY REVIEW 223

may not answer questions at larger scales such as pating Wegener's theory of continental drift, ar- why a parasite species is absent in an area where gued for an ancient land connection between South the host is présent, or, how the parasite and host America and Australia, including as évidence the originally came to be associated. présence of the commensal Temnocephalus Parasites are not randomly distributed among ail chiliensis with closely related freshwater crusta- available host species and this reflects différences ceans found in New Zealand and South America. in host-specificity. Host-specificity is recognized Ihering (1902) reinforced this belief in an ancient by parasite species occurring only in phylogeneti- New Zealand/South America connection with in- cally related hosts. However, ail hosts are phylo- terprétations of the distribution and association of genetically related at some level and this imprécise Acanthocephala with fish, birds and mammals. définition has resulted in host-specificity being This contention of an affinity between Australia recognized at the taxonomic level of host species, and South America was buttressed by Metcalf genus and even family. In fact, ail parasites have (1929, 1940) who reported the présence of opalinid predictable associations to hosts at some taxo- protozoans in leptodactylid frogs from South nomic level. It is well documented that parasites America and Australia. Metcalf (1920, 1923, 1929) have predictable associations at higher host taxo- proposed that parasites could be used to explain the nomic levels. We believe that thèse predictable as- geographical distribution and migration routes of sociations occur as a continuum across host taxo- animais and plants. Other researchers also used nomic ranks, and that for many fish parasites the parasites to investigate the biogeography of hosts important association may be at the level of host (Johnston 1913, 1914, Harrison 1926, 1928) and family. For example, a given parasite species may Manter (1940, 1955, 1963, 1966) extended it to in- be associated with many, or ail, of the species in a clude the Atlantic and Pacific distributions of ma- host family, and will be found rarely, if at ail, in rine fishes and their digenean parasites. Manter host species outside of that host family. We define (1955) did not suggest continental drift to explain a host-specific parasite as one that reaches repro- biotic similarities between New Zealand and the ductive maturity in a single host species, with re- northern hémisphère suggesting instead that dis- productive maturity being recognized by the prés- persai was assisted by oceanic currents. ence of sexually mature and/or gravid adults. This Weaknesses in the early use of parasites to infer strict définition is consistent with that used by host évolution and biogeography was the assump- parasitologists studying monogenean parasites on tion of coevolution and the non-independence of the gills of fishes. methods used to construct host and parasite The capacity for a parasite to diversify among phylogenies and distributions (Klassen 1992a). hosts is constrained by strict host-specificity. Be- Furthermore, because the emphasis was on the cause a host-specific parasite is unable to colonize host, parasite géographie distribution was rarely new hosts then not only is its distribution among studied. Exceptions include parasites causing dis- host species limited, but the opportunity for the ease in humans where interest centered on delimit- parasite to enter new géographie areas is limited by ing zones of infection rather than biogeography of the dispersai abilities of the associated host spe- the parasite and studies of Dogiel and coworkers cies. This suggests that parasites with larger num- (Dogiel et al. 1958) who conducted large scale and bers of potential hosts i.e., broader associations, wide spread parasite surveys of fishes. A resuit of should have greater géographie distributions. Fur- thèse efforts by Dogiel et al. (1958) was the récog- thermore, while the géographie distributions of nition of différent biogeographic régions based strict host-specific parasites is limited by the distri- solely on parasite distributions (Shulman 1958). A bution of the host, parasites with broader host asso- major advance in parasite biogeography came ciations may have their géographie distributions when Brooks (1977) applied the phylogenetic limited by factors unrelated to host distributions methodology of Hennig (1966) to develop phylo- (e.g. Lawler & Scott 1954). genetic hypothèses for parasites and compare thèse to host phylogenies to interpret coevolutionary and biogeographic relationships for both. This pioneer- ing work resulted in investigations relating to the HISTORICAL BACKGROUND origins of parasite-host associations and parasite géographie distributions (Brooks & McLennan 1991, 1993, Hoberg 1992, Choudhury & Dick in There is a long and productive history in the review, Carney & Dick in review). study of biogeography derived from the discipline of parasitology. Early efforts utilized parasites to Parasite data have also been used to test existing explain the geographical distributions of hosts biogeographical théories. For example, Dritschilo and/or using parasites as biological data to discuss et al. (1975) substituted hosts for islands in apply- geological history and frequently invoked assump- ing the concepts of island biogeography (MacAr- tions of host-parasite coevolution (see Klassen, thur & Wilson 1967) to study mites of North Ame- 1992a for historical review). Ihering (1891), antici- rican cricetid rodents. Dritschilo et al. (1975) 224 CARNEY Y, DICK TA concluded that hosts with greater géographie distri- view). Thèse methods differ in their underlying bution had more parasites and this was consistent assumptions and the way in which rare and wide- with the prédictions of island biogeography theory. spread taxa are treated. Clearly, the choice of meth- The substitution of hosts for islands and their con- ods is far from settled (Morrone & Carpenter 1994, clusions were critieized by Kuris & Blaustein Morrone & Crisci 1995). (1977). Other applications of this theory to hosts One of the key pioneering studies dealing with and parasites reached inconsistent and conflicting parasite biogeography is by Brooks et al. (1981). interprétations. For example, Kennedy (1978) The stingray family Potamotrygonidae is entirely found that island populations of Arctic charr freshwater and is présent only in the major Atlantic {Salvelinus alpinus) had more parasites than main- drainages of South America. Brooks et al. (1981) land populations. By contrast, Coneely & McCar- developed hypothèses of phylogeny for several thy (1984) and Marcogliese & Cone (1991) re- parasite taxa inhabiting thèse stingray hosts to infer ported that hosts on islands had fewer parasites the origins of Potamotrygonidae, consistent with than those hosts on the nearest mainland. As the previous history of using parasites to infer host Marcogliese (1992) has pointed out, this réduction biology (Metcalf 1920, 1929, Manter 1966). Thèse in parasite species may reflect an inability of the parasite phylogenetic hypothèses were the basis for colonizing host to carry its parasites with it, and the hypothesis that the freshwater stingrays of have less to do with island biogeographic theory as South America were derived from Pacific Océan it relates to parasites. Priée & Clancy (1983) found ancestors. This conclusion has been criticised on that increased host range was significantly corre- both empirical grounds and for the use of parasites lated with increased numbers of parasite species to infer host ancestry (Straney 1982, Caira 1990, for fishes in the British Isles, a pattern also noted 1994, Lovejoy 1997). Nevertheless, the research by Gregory (1990) for parasites of waterfowl. initiated by Brooks et al. (1981), (and subséquent However, Guégan & Kennedy (1993) reanalyzed studies [Brooks & McLennan 1991, 1993 and référ- the data used by Price & Clancy (1983) and found ences therein]) into the parasites of South Ameri- that increased parasite richness was correlated with can freshwater stingrays is important as it contrib- the amount of time the host species had been in the uted significantly to the development and area. Host size has also been used as a predictor of refinement of méthodologies for biogeographic parasite community richness (e.g. Guégan et al. analysis (Brooks 1981, 1992, Wiley 1988) and 1992) but Poulin (1995) has demonstrated that stimulated further studies on the évolution and when host phylogeny is taken into account the cor- biogeography of stingrays (Lovejoy 1996). Inter- relation can disappear. estingly, Brooks, who has long argued that the évo- lution of parasites can be and should be studied in- dependent of the host (Brooks & McLennan 1991, PRESENT CONTRIBUTIONS 1993) has made studying the évolution of the sting- ray host dépendent on the parasites. Parasite historical biogeography also has gener- The two areas of research in parasite ated interesting zoogeographic hypothèses such as biogeography are 1) historical biogeography which in the studies of Hoberg (1986, 1992) and Hoberg seeks explanations for the evolutionary origins for & Adams (1992). The Arctic usually is considered parasite géographie distributions and host associa- to be a région of extinction, particularly in associa- tions based on vicariance, dispersai, coevolution tion with Pleistocene glaciation (Pielou 1979, Vrba and host-switching as mechansims to explain pat- 1985) but this idea was questioned by Hoberg terns and 2) ecological biogeography which seeks (1986, 1992) and Hoberg & Adams (1992) who ex- explanations for how parasite géographie distribu- amined the historical biogeography of cestode pa- tions and host associations are maintained based on rasites of seabirds and pinnipeds in the Arctic. contemporary biotic and abiotic influences. Hoberg (1986, 1992) and Hoberg & Adams (1992) Parasite historical biogeography requires the de- incorporated hypothèses of phylogeny for 2 différ- velopment of hypothèses of phylogeny for the taxa ent groups of cestode parasites with existing host of interest based in phylogenetic systematics phylogenies and contemporary distributions, and (Hennig 1966, Wiley 1981). Generally, the major knowledge of past géologie events, to arrive at a approaches used in parasite biogeography include novel marine refugium hypothesis. During periods comparison of parasite and host clades and com- of maximum glaciation host ranges contracted re- parison of clades with régions (e.g. Hoberg 1986, sulting in vicariant isolation of host and parasite Hoberg & Adams 1992, Carney & Dick in review). populations leading to parasite speciation and Methods include Brooks Parsimony Analysis or host-specificity. During interstadials, host ranges BPA (e.g. Brooks 1981, 1990, Wiley 1988), com- expanded and the intermingling of host species ponent compatibility (e.g. Page 1988, 1989, 1990, with shared feeding habits made colonization of 1994a, b) and panbiogeography of Croizat (1958) new hosts possible, depending on the degree of (e.g. Brooks 1977, 1979, Choudhury & Dick in re- host-specificity attained by the parasites during PARASITE BIOGEOGRAPHY REVIEW 225 stadials. Thèse investigations indicate that the Arc- there were very few parasite species shared be- tic was an area of biological diversification, at least tween the North American yellow perch {Perça for some species. Some other studies incorporating flavescens) and its sister species the Eurasian perch a historical approach to parasite biogeography in- {Perça fluviatilis). Carney & Dick (in review) dem- clude Adamson & Richardson (1989), Brooks & onstrated that the historical basis for the associa- O'Grady (1989), Brooks & McLennan (1991, 1993 tion between yellow perch and its parasites was a and références therein), Platt (1992) and conséquence of extensive host switching from Choudhury & Dick (1996, 1998). Because parasite other sympatric hosts (e.g. Centrarchidae, historical biogeography requires the incorporation Ictaluridae). The basis of this host switching was of host data, results from thèse studies give new in- postulated to be ecological overlap, in particular sights into the évolution of biotic associations and shared feeding habits (Carney & Dick 2000 in re- provide novel hypothèses explaining the origins for view). Studies of Choudhury & Dick (2000, in re- animal distributions. view) and Carney & Dick (2000 in review) were able to propose time frames for some of the associ- Ecological parasite biogeography deals with ations based on the geological record. what affects and maintains présent day distribu- tions and abundances and searches for patterns in abundance and distribution of parasites both geo- graphically and among host taxa. Abiotic factors ECOLOGICAL BIOGEOGRAPHY such as température and aquatic characteristics in- OF HOLARCTIC FISHES fluence parasite distributions. For example, Lawler & Scott (1954) showed that the southern limit of tapeworms in the genus Triaenophorus correlates Parasites of Holarctic fishes, especially freshwa- with température and not with the potential hosts ter fishes, provide a useful model System to study that are more widely distributed. Chubb (1970) and ecological parasite biogeography that can subse- Esch (1971) concluded that lake trophic status was quently be used to frame questions relating to the significant in determining the distribution of para- historical biogeography of thèse organisms. There site species, a conclusion not supported by Carney are many monophyletic groups of fishes in this ré- & Dick (2000). Biotic factors such as host type, gion that are endémie to their continents, are wide- physiology, ecology and behaviour have also been spread among continents, and have strict host-spe- used to explain patterns of parasite distribution and cific parasites, predictable associations and non abundance (Kennedy et al. 1986, Aho & Bush host-specific parasites. Furthermore, the geological 1993, Carney & Dick 2000). Some other studies in- history of the Holarctic région is well known and corporating a distributional or ecological approach involves épisodes of continental connection and to parasite biogeography include Khalil (1971), fragmentation and has comparatively récent peri- Rohde (1978, 1982, 1986), Price & Clancy (1983), ods of glaciation. Cone & Wiles (1985), Bailey & Margolis (1987), Carney & Dick (1999) investigated the associa- Gregory (1990), Guégan & Lambert (1990), tion of parasite species with Perça flavescens in Byrnes & Rohde (1992), Klassen (1992b), North America and Perça fluviatilis in Eurasia and Marcogliese (1992, 1995), Esch & Fernandez demonstrated the parasite communities of each (1993 and références therein), Kennedy (1993) and host were comprised of taxonomically distinct but Marcogliese & Cone (1993). ecologically similar parasites. Thèse hosts are sis- Only recently have studies combined ecological ter taxa but are found on différent continents. De- and historical approaches to explain the présent spite the close phylogenetic relationship of thèse distributions of parasites among hosts and across hosts they share few parasites species and those geography. Choudhury & Dick ( in review) study- that are shared were uncommon. The majority of ing historical and ecological associations between parasites common to perch hosts in North America sturgeons and their parasites demonstrated that and Eurasia are those that either mature in birds sturgeon parasites had predictable associations (e.g. Diplostomum spp.), or in other hosts (e.g. (considered by Choudhury & Dick to be host-spe- Triaenophorus nodulosus matures in pike; cific but at différent taxonomic levels) some of Diphyllobothrium spp. matures in mammals). For which could be explained by coevolution. How- thèse parasites, the percid fish host is not the final ever, there was a substantial group of parasite spe- host within which the parasite matures. Enteric par- cies that were characterized by host switching and asites that mature in the percid host show a more affinities to géographie régions distinct from the gênerai pattern of association with the continent in- géographie distributions of the sturgeon hosts. stead of the host. Enteric parasites with Holarctic Similarly, Carney & Dick (1999, 2000 in review) distributions with many host taxa are not strictly investigated the parasites of perch using both eco- host-specific, but may have predictable associa- logical and historical approaches. Carney & Dick tions at higher host taxonomic ranks. For example, (1999) demonstrated that, in spite of extensive para- Crepidostomum farionis is reported from many site lists with essentially no spécifie parasites, Holarctic host species but is predictably associated 226 CARNEY Y, DICK TA

Table L - Parasites recorded from species of Stizostedion from North America and Eurasia.

Stizostedion Stizostedion Stizostedion Stizostedion vitreum Parasite Species canadense lucioperca volgensis North America North America Eurasia Eurasia

ECTOPARASITES

MONOGENEA Ancyrocephalus paradoxus Cleidodiscus sp. Dactylogyrus extensus Gyrodactylus longiradix X Gyrodactylus luciopercae X Gyrodactylus mizellei Gyrodactylus schmidti Tetraonchus sp. Urocleidus aculeatus

CRUSTACEA Ancyrocephalus paradoxus Achtheres percarum Argulus appendiculosus x Argulus biramosus x Argulus canadensis x Argulus coregoni Argulus foliaceus Argulus stizostethii Argulus versicolor Caligus lacustris Ergasilus caeruleus Ergasilus centrarchidarum Ergasilus confusus Ergasilus luciopercarum Ergasilus sieboldi Ergasilus versicolor Lernaea cruciata Lernaea cyprinacea Lernaea esocina Lernaea variabilis Lernaeocera sp.

ENTERIC PARASITES

DIGENEA Allocreadium lobatum Aponurus tschugunovi Azygia acuminata Azygia angusticauda Azygia bulbosa Azygia longa Azygia lucii X Brachyphallus crenatus (marine) X Bucephaloides ozakii Bucephalus markewitschi Bucephalus polymorphus Bucephalus pusilla Bunocotyle cingulata Bunodera luciopercae Bunodera sacculata Centrovarium lobotes Crepidostomum cooperi Crowcrocaecum skrjabini X Phyllodistomum angulatum X Phyllodistomum folium X Phyllodistomum pseudofolium X Phyllodistomum superbum x Prosorhynchoides pusilla x Ptychogonimus fontanus Rhipidocotyle illense Rhipidocotyle papillosa X Sanguinicola occidentalis X PARASITE BIOGEOGRAPHY REVIEW 227

Stizostedion Stizostedion Stizostedion vitreum Stizostedion Parasite Species canadense lucioperca volgensis North America North America Eurasia Eurasia CESTODA Biacetabulum macrocephalum Bothriocephalus claviceps X Bothriocephalus cuspidatus X Bothriocephalus scorpii (marine) Caryophyllaeus laticeps Cyathocephalus truncatus Eubothrium sp. Proteocephalus cernuae Proteocephalus fluviatilis x Proteocephalus luciopercae X Proteocephalus macrocephalus X Proteocephalus pearsei X Proteocephalus percae Proteocephalus pinguis X Proteocephalus stizostethi X Proteocephalus torulosus Triaenophorus stizostedionis

NEMATODA Camallanus ancylodirus Camallanus lacustris Camallanus oxycephalus Camallanus truncatus Capillaria catenata Coitocaecum skrjabini Contracaecum bidentatum Contracaecum spiculigerum Contracaecum squalii Cucullanus cirratus Cystidicola lepisostei Dichelyne cotylophora Hysterothylacium brachyurum Philometra abdominalis Philometra cylindracea Raphidascaris acus Rhabdochona canadensis Spinitectus carolini Spinitectus gracilis

ACANTHOCEPHALA Acanthocephalus anguillae X Acanthocephalus lucii X Echinorhynchus salmonis X X Leptorhynchoides thecatus X Neoechinorhynchus crassus X Neoechinorhynchus cylindratus X Neoechinorhynchus rutilii X Neoechinorhynchus strigosus X Neoechinorhynchus tenellus X Pomphorhynchus bulbocolli X Pomphorhynchus laevis X Pseudoechinorhynchus clavula X

LARVAL PARASITES

DIGENEA Apophallus americanus Apophallus muhlingi Apophallus venustus Ascocotyle coleostoma Bucephalus polymorphus Bunocotyle cingulata Centrovarium lobotes X Clinostomum complanatum X Crassiphiala bulboglossa 228 CARNEY Y, DICK TA

Stizostedion Stizostedion Stizostedion Stizostedion vitreum Parasite Species canadense lucioperca volgensis North America North America Eurasia Eurasia Diplostomum sp. X Diplostomum clavatum X Diplostomum scheuringi Diplostomum spathaceum X X Hysteromorpha trilobata X X Ichthyocotylurus communis x Ichthyocotylurus pileatus X X Ichthyocotylurus platycephalus X Metagonimus yokogawai X Neascus sp. Ornithodiplostomum ptychocheilus Paracoenogonimus ovatus Posthodiplostomum angulatum Posthodiplostomum minimum Ptychogonimus fontanus Rhipidocotyle illense Rossicotrema donicum Tetracotyle communis X Tetracotyle diminuta X Tetracotyle percae-fluviatilis X Tetracotyle variegatus X Tylodelphys clavata X Uvulifer ambloplitis

CESTODA Diphyllobothrium latum Ligula intestinalis Proteocephalus ambloplitis Triaenophorus crassus Triaenophorus nodulosus

NEMATODA Agamospirura sp. Anisakis sp. (marine) Contracaecum spiculigerum Contracaecum squalii X Desmidocercella sp. X Eustrongylides sp. Eustrongylides excisus Eustrongylides mergorum Eustrongylides tubifex Gnathostoma sp. Hysterothylacium brachyurum X Philometra cylindracea X Philometra obturans X Porrocaecum reticulatum X Raphidascaris acus X

ACANTHOCEPHALA Corynosoma semerme (marine) Corynosoma strumosum (marine) Leptorhynchoides thecatus Pomphorhynchus bulbocolli

Sources: Barysheva & Bauer 1957, Bykhovskaya-Pavlovskaya et al. 1962, Craig 1987, Dontsov & Markov 1981, Hoff- man 1999, Margolis & Arthur 1979, McDonald & Margolis 1995, Molnar 1980, Ozcelik & Deufel 1989, Pojmanska et al. 1980, Rokicki 1975, Scholz & Hanzelova 1998, Waluga & Wlasow 1988. PARASITE BIOGEOGRAPHY REVIEW 229

Table II. - Number of shared parasites recorded from species of Stizostedion from North America and Eurasia. # of species indicates how many parasite species have been reported from thèse hosts.

S. vitreum S. canadense S. lucioperca S. volgensis

North America North America Eurasia Eurasia

# species 95 35 74 20

S. vitreum X 32 12 5 North America

S. canadense X 3 0 North America

S. lucioperca X 18 Eurasia

S. volgensis X Eurasia with Salmoniformes. Similarly, Bunodera rather than with congeners across continents (Table luciopercae is reported from percids, and other II) . For example, Stizostedion canadense in North hosts, throughout the Holarctic. The nematode America shares only 4 parasite species with Camallanus oxycephalus and the cestodes Stizostedion luciopercae and no parasite species Bothriocephalus claviceps and Cyathocephalus with Stizostedion volgensis, both European species. truncatus are reported from Stizostedion and Perça By contrast, the 2 North American species, S. on both continents. There are 2 différent vitreum and S. canadense, share 33 parasite species Acanthocephala species, Echinorhynchus salmonis and the 2 European Stizostedion species have 17 and Neoechinorhynchus rutili, reported from Perça parasite species in common (Table II). The para- hosts on both continents and neither show predict- sites shared by Stizostedion spp. in Eurasia and able associations to any hosts other than freshwater North America are not strictly host-specific (e.g. fish. Thèse observations confirm that an absence of Camallanus lacustris, E. salmonis, and N. rutili) strict host-specificity contributes to an increased or are larval species that have fish-eating birds as géographie distribution of a parasite species. final hosts and use a wide variety of fish species as In a subséquent investigation Carney & Dick intermediate host. Thèse three species are an exam- (2000) emphasized the importance of ecology re- ple of parasites with transcontinental distributions porting that distributions and abundance of para- which have no predictable host association except for freshwater fish in the northern hémisphère. sites in yellow perch (Perça flavescens) were based in the feeding habits of the host, enhanced by the Even though parasites of percids revealed that présence of other hosts, particularly birds, and con- their parasitofauna was more affected by continent strained by the local biotic conditions. Carney & and ecology than by host phylogenetic association Dick (in review) then examined the historical ecol- it was not clear if this pattern was présent for other ogy of the parasites of yellow perch in North Holarctic species of fish. Interestingly, when we America and found that they were best character- compared several additional fish groups from ized by host-switching from other endémie North North America and Eurasia a similar pattern American fish species with shared feeding habits. émerges. For example, the parasites of Esox lucius This is consistent with the basis for host switching in North America and Eurasia shared compara- postulated by Hoberg (1986, 1992) and Hoberg & tively few parasite species from the différent conti- Adams (1992) for arctic seabirds and pinnipeds and nents (Dick & Choudhury, 1996). Those that are suggests that ecological factors are dominant in shared included 2 parasites predictably associated colonization of new host species. with Esox spp. (Triaenophorus spp. and Raphidascaris acus), larval forms that mature in Some might argue that the results of Carney & Dick (1999, 2000) from parasites of yellow perch fish-eating birds (e.g. Diplostomum spp.), and those with no évidence of host predictability (E. will not hold at higher taxonomic levels. For this reason, we considered the parasites from fish spe- salmonis, N. rutili). In the case of the pike parasites cies in the family Percidae that often associate with there are predictable associations at the generic the genus Perça given that taxa within this group level that play a rôle in shaping the parasite are closely related and widely distributed in North communites on both continents. America and Eurasia. Parasites associated with Comparisons of parasites from species of Core- species of Stizostedion, also in the family Percidae gonus in North America and Eurasia show similar (Table I), show a similar pattern to perch with their patterns to those reported for the percids (Table parasites having greater affinity with the continent III) . The Arctic cisco, Coregonus autumnalis, oc- 230 CARNEY Y, DICK TA

Table III. - Helminth and arthropod parasites recorded from Coregonus and Thymallus species from North America and Eurasia.

Coregonus Coregonus Coregonus Coregonus Coregonus Coregonus Thymallus Thymallus Parasite Species autumnalis autumnalis nasus nasus sardinella sardinelk arcticus arcticus Eurasia North Eurasia North Eurasia North Eurasia North Amerca Amerca Amerca Amerca

ECTOPARASITES

MONOGENEA Discocotyle sagittata Tetraonchus alaskensis Tetraonchus borealis Tetraonchus grumosus Tetraonchus rauschi Tetraonchus sp.

CRUSTACEA Achtheres coregonorum Achtheres extensus Achtheres strigatus Argulus coregoni Argulus foliaceus Coregonicola orientalis Coregonicola producta Ergasilus nerkae Ergasilus sieboldi Salmincola carpionis Salmincola corpulentis Salmincola edwardsi Salmincola extensus Salmincola thymalli

ENTERIC PARASITES

DIGENEA Allocreadium isoporum Ariella baikalensis Azygia lucii Brachyphallus crenatus Clinostomum complanatum Crepidostomum farionis Crepidostomum isostomum Crepidostomum metoecus Derogenes varicus (marine) Lecithaster sp. (marine) Phyllodistomum conostomum Phyllodistomum folium Phyllodistomum megalorchis Phyllodistomum simile Sphaerostoma bramae

CESTODA Bothrimonas sturionis (marine) Cyathocephalus truncatus Eubothrium crassum Eubothrium salvelini Proteocephalus arcticus Proteocephalus exiguus Proteocephalus longicollis Proteocephalus thymalli Proteocephalus tumidocollis

NEMATODA Ascarophis skrjabini (marine) Ascarophis sp. (marine) Camallanus lacustris Coregonema sibirica Cystidicola farionis Hysterothylacium aduncum (marine) Philometra ovata Rhabdochona cascadilla Rhabdochona denudata Sterliadochona ephemeridarum Truttaedacnitis truttae PARASITE BIOGEOGRAPHY REVIEW 231

ACANTHOCEPHALA Acanthocephalus anguillae x Echinorhynchus clavula x Echinorhynchus gadi x x Echinorhynchus leidyi x x Echinorhynchus salmonis x x x x x x x Neoechinorhynchus rutili x x x x Neoechinorhynchus tumidus x x x x Neoechinorhynchus venustus x Neoechinorhynchus sp. x Pomphorhynchus laevis x

LARVAL PARASITES

DIGENEA Clinostomum complanatum x Diplostomum baeri x Diplostomum scheuringi x Diplostomum spathaceum x x x Diplostomum sp. x Ichthyocotylurus erraticus x x x Tetracotyle intermedia x x

CESTODA Diphyllobothrium dendriticum x x x Diphyllobothrium ditremum x Diphyllobothrium latum x x Diphyllobothrium minus x x Diphyllobothrium x norvegi'cum Diphyllobothrium strictum x x x x Diphyllobothrium sp. x Proteocephalus sp. x Triaenophorus crassus x x x x x x Triaenophorus nodulosus x

NEMATODA Raphidascaris acus x x

Sources: Bykhovskaya-Pavlovskaya a/. 1962, Choudhury & Dick 1977, Hoffman 1999, Margolis & Arthur 1979, McDonald & Margolis 1995, Pronin et al. 1979, Pugachev 1984, Scholz and Hanzelova 1998, Shostak et al. 1986, Val- tonen 1980, van Maren 1979. curs in North America and Eurasia. One of two par- reagion. This is a good example of the importance asite species that occurs in this host species from of past and current ecological associations on para- both North America and Eurasia (Table IV) is site distributions. Bothrimonus sturionis. It is a marine parasite and it The digenean Crepidostomum farionis also is is acquired by this anadromous host species on commonly reported from Coregonus host species both continents likely as a conséquence of ecologi- and provides an example of the distinction between cal overlap while in the marine environment. By strict host-specificity and predictable associations contrast, Coregonus autmunalis shares 11 parasite at higher host taxonomic ranks. Crepidostomum species with C. nasus and 12 species with C. farionis is a parasite associated with hosts belong- sardinella if only Eurasian populations are consid- ing in the Salmoniformes and it is at this taxonomic ered (Table IV). Similarly, C. sardinella from Eur- level that the association is predictable. Given that asia also shares more parasites with Eurasian con- Salmoniforme species have a natural Holarctic dis- geners than with Coregonus sardinella from North tribution, and that C. farionis is associated with America. Parasites with little évidence of strict Salmoniformes, it should not be surprising that this host-specificity and wide distribution include the parasite has a Holarctic distribution. cestode Cyathocephalus truncatus and the acantho- Coregonus nasus is an exception to this pattern cephalans Echinorhynchus salmonis and Neoechino- of hosts sharing more parasites with congeners rhynchus rutili and N. tumidus. from the same continent than with conspecifics Larval parasites seem to be less important in from another continent. Coregonus nasus from contributing to intercontinental similarity in the North America shares more parasites with C. nasus parasite fauna of Coregonus hosts, unlike the from Eurasia than with other Coregonus species Stizostedion example. Triaenophorus spp. predict- from North America. By contrast, C. nasus from ably are shared among coregonid hosts from Eur- Eurasia shares more parasites with Eurasian C. asia and North America and are occasionally re- sardinella than with C. nasus from North America. ported from lake trout. Thèse parasites mature in There is a paucity of reports on parasites from C. pike, a host that is widespread in the Holarctic nasus throughout its distribution, particularly from 232 CARNEY Y, DICK TA

Table IV. - Number of shared parasites recorded from species of Coregonus and Thymallus from North America and Eurasia. # of species indicates how many parasite species have been reported from thèse hosts.

Coregonus Coregonus Coregonus Coregonus Coregonus Coregonus Thymallus Thymallus autumnalis autumnalis nasus nasus sardinella sardinella arcticus arcticus Eurasia North Eurasia North Eurasia North Eurasia North Amerca Amerca Amerca Amerca # species 20 7 18 18 26 13 28 30

Coregonus autumnalis X 2 11 4 13 4 6 4 Eurasia Coregonus autumnalis X 2 2 3 3 3 2 North Amerca Coregonus nasus X 8 14 5 4 9 Eurasia Coregonus nasus X 6 4 4 7 North Amerca Coregonus sardinella X 7 5 9 Eurasia Coregonus sardinella X 5 4 North Amerca Thymallus arcticus X 8 Eurasia Thymallus arcticus X North Amerca

North America, and more information may reveal If the distribution of parasite species among host greater similarity of the parasitofauna with différ- species is host-driven, as is often believed, then ent host species from the same continent than with hosts of the same species should share more para- the same host species from différent continents. sites despite being on différent continents, than The grayling, Thymallus arcticus, présents an with différent hosts on the same continent. Our interesting case as it appears to share more para- data do not support this contention, at least for sites with Eurasian species of Coregonus than with Holarctic freshwater fish hosts. Parasites of thèse either North American species of Coregonus or hosts have a greater affinity for the continent than Eurasian Thymallus arcticus. By contrast, Eurasian with the host species. This indicates that the para- Thymallus arcticus share fewer species with any of sites have a unique evolutionary history that, al- the above hosts and have more shared parasites though inevitably tied to a host, is based more on with Thymallus arcticus from North America (Ta- geography than on the host's identity, at least at the ble IV). If parasite data really do provide insights level of species. The degree of predictability of the into host origins then thèse data would support the association between a parasite and its host(s) is rel- testable hypothesis that Thymallus arcticus has a evant to this assertion. It may be that the relevant North American origin. association between parasite and host in thèse ex- Even if anadromous species of Oncorhynchus amples is not at the level of host species, but at a are compared there is a greater similarity among higher taxonomic level. For example, parasite gên- the parasites shared among congeneric hosts from era may associate with host gênera or family. As a the same continent than conspecific hosts from dif- conséquence, parasite species belonging in wide- férent continents (Table V, VI). For example, spread gênera may then have continental affinities Asian O. gorbuscha shares more parasite species that may not track the intercontinental distributions with other Eurasian Oncorhynchus species than of the individual host species, but would track in- with Oncorhynchus gorbuscha from North Amer- tercontinental distributions of a host family (e.g. ica (Table VI). When the parasites reported from Choudhury & Dick, in review). This would pro- other species of Oncorhynchus are compared, it is duce the pattern of the same host species on différ- clearly seen that thèse hosts share more parasites ent continents having différent parasite species. with différent host species from the same continent Furthermore, it suggests that for thèse Systems, than they do with the same host species from a dif- parasites are speciating as a conséquence of geo- férent continent. Similarly, sticklebacks of différ- logical vicariance despite the apparent lack of host ent gênera on the same continent share more speciation, and that sharing of parasites among parasites than do hosts of the same species from hosts species is based on ecological considérations différent continents (Tables VII, VIII). This pattern and enhances the géographie distribution of the is not unique to a single host family (Percidae, parasite. Byrnes & Rohde (1992) reported a similar Esocidae, Salmonidae, Coregonidae, Gasterosteidae), pattern for ectoparasites of marine fishes in Austra- nor is it unique to strictly freshwater (Percidae, lian waters. The monogenean parasites had a wider Esocidae) or anadromous (Salmonidae, Coregonidae) géographie distribution than any of the individual fish hosts. host species, and the distribution of the parasites PARASITE BIOGEOGRAPHY REVIEW 233

Table V. - Helminth and arthropod parasites recorded from 5 species of Oncorhynchus from North America and Eurasia.

O. Q O. Q O. Q O. O. O. Q Parasite Species gorbuscha^^10 keta kisutch nerka tshawytscha tsha^ha Eurasia ^erica *~ ^fca ^urasta Eurasia ^ Eu/asia

ECTOPARASITES

MONOGENEA Gyrodactyloides strelkovi Gyrodactylus nerkae Gyrodactylus salmonis Laminiscus strelkovi Octomacrum lanceatum Tetraonchus alaskensis

ARTHROPODA Argulus coregoni Argulus pugettensis (marine) Bomolochus cuneatus (marine) Bomolochus sp. (marine) Caligus clemensi (marine) Elthusa vulgaris (marine) Ergasilus briani Ergasilus nerkae Ergasilus turgidus (marine) Lepeophtheirus salmonis (marine) Lernaeopodafulculata Rocinela maculata (marine) Salmincola beani Salmincola californiensis Salmincola carpionis Salmincola edwardsi Salmincola falculata Salmincola lata Salmincola salmonea

DIGENEA Brachyphallus crenatus (marine) Copiastes katuwo (marine) Copiastes filiferum (marine) Crepidostomum farionis Derogenes aspina (marine) Derogenes varicus (marine) Genolinea anura (marine) Genolinea laticauda (marine) Genolinea oncorhynchi (marine) Hemiurus appendiculatus (marine) Hemiurus levinseni (marine) Isoparorchis hypselobagri Lampritrema miescheri (marine) Lampritrema nipponicum (marine) Lecithaster gibbosus (marine) Lecithaster salmonis (marine) Lecithaster stetlatus (marine) Lecithophyllum botryophorum (marine) Parahemiurus merus (marine) Phyllodistomum umblae Plagioporus shawi Podocotyle shawi (marine) Pronoprymna petrowi (marine) Pronoprymna umblae (marine) Prosorhynchoides gracilescens (marine) Prosorhynchoides basargini (marine) Tubulovesicula lindberghi (marine) 234 CARNEY Y, DICK TA

0 ch a u « • !?■ gorbuscha 0. keta 0. kisutch -^% 0. nerka %™£ ° tshawytscha ParasitD e Spec.es IfgS*' h ' Norg Eurasia ^orth^ ^orth^ tsha ytscha Amcncâ Eurasia Eurasia

CESTODA Bothriocephalus sp. x x Bothriomonas sturionis x x (marine) Cyathocephalus truncatus x x x x Diplocotyle olrikii x x Eubothrium crassum x x x x x x x Eubothrium salvelini x x x x x Nybelinia lingualis (marine) x x Nybelinia surmincola (marine) x x x x x x Pelichnibothrium speciosum x x x x x x x (marine) Phyllobothrium ketae (marine) x Phyllobothrium salmonis x (marine) Proteocephalus ambloplitis x Proteocephalus arcticus x x Proteocephalus exiguus x x x Proteocephalus laruei x Proteocephalus parallacticus x x x Proteocephalus salmonidicola x x

NEMATODA Ascarophis sebastodis (marine) x x Ascarophis skrjabini (marine) x Ascarophis sp. (marine) x Capillaria bakeri x Contracaecum spiculigerum x x Cucullanus laevis x Cystidicola farionis x x Cystidicola tenuissima x Hysterothylacium aduncum xx xxxxxx (marine) Philonema agubernaculum x Philonema oncorhynchi x x x x x x Pseudocapillaria salvelini x Rhabdochona canadense x x Rhabdochona kisutchi x x Rhabdochona sp. x Salvelinema salmonicola x x Salvilinema walkeri x x Spinitectus gracilis x x x Truttaedacnitis truttae x

ACANTHOCEPHALA Acanthocephalus aculeatus x Acanthocephalus x

Echinorhynchus gadi (marine) xxxxxxxx x Neoechinorhynchus rutili x x x x x Neoechinorhynchus salmonis x x x Neoechinorhynchus tumidus x x x Neoechinorhynchus sp. x Paracanthocephalus x fenu/ros/nis Rhadinorhynchus trachuri x x x x (marine)

LARVAL PARASITES

DIGENEA Apophallus donicus x Diplostomum baeri x x Diplostomum spathaceum x x Galactosomum phalacrocoracis x x (marine) Isoparorchis hypselobagri x Nanophyetus salmincola x x x Neascus sp. x x x Tetracotyle intermedia x Tetracotyle sp. x x PARASITE BIOGEOGRAPHY REVIEW 235

CESTODA Diphyllobothrium sp. x x x Diphyllobothrium dendriticum x x Diphyllobothrium ditremum x x x Diphyllobothrium latum x Diphyllobothrium sp. x x Diplocotyle olrikii x x Gilquinia squali (marine) x Hepatoxylon trichiuri (marine) x Nybelinia lingualis (marine) x x Nybelinia surminicola (marine) x x x x x x

Paradilepis simoni (marine) x Pelichnibothrium speciosum x x x x x x x (marine) Phyllobothrium caudatum x x x x (marine)

Phyllobothrium salmonis x (marine) Scolex pleuronectis (marine) x x x x x x x Triaenophorus crassus x x

NEMATODA Anisakis simplex (marine) x x Anisakis sp. (marine) x x x x Contracaecum spiculigerum x x Contracaecum sp. x Cucullanus laevis x Eustrongylides sp. x Hysterothylacium aduncum x x x x x Truttaedacnitis truttae x x

ACANTHOCEPHALA Bolbosoma caenoforme x x x x x (marine) Corynosoma semerme (marine) x Corynosoma strumosum x x (marine) Corynosoma villosum x x x (marine) Sources: Bailey et al. 1989, Bakke & Bailey 1987, Bykhovskaya-Pavlovskaya et al. 1962, Hoffman 1999, Margolis & Arthur 1979, McDonald & Margolis 1995, Nagasawa et al. 1983, Scholz & Hanzelova 1998, Whitaker 1985.

did not conform to biogeographic régions that were with other host species due to ecological overlap recognized based on free-living organisms. It may among the relevant host taxa. This overlap was ei- be that the parasites have unique biogeographical ther sympatry, shared feeding habits, or both. There patterns that are distinct from those of individual was little évidence for a phylogenetic basis for the host species, despite the requirement of a host for associations between parasite species and Perça the survival of the parasite. Phylogenetic analyses flavescens, even for the host-specific monogenean of the parasites and hosts would contribute to re- Urocleidus adspectus. Regardless, historical con- solving thèse possible hypothèses. Alternatively, sidérations need to be investigated to demonstrate the association may be dépendent on the host ecol- the ecological basis for thèse observations. ogy. Hosts belonging to the same gênera or family Many studies of parasite biogeography using a may have similar écologies, in particular with re- historical phylogenetic approach examine hosts gard to feeding. If this is the case, then the distribu- with many apparently strictly host-specific para- tion of parasites in Holarctic freshwater fishes may sites (e.g. Brooks, 1992). This may bias estimâtes be driven by ecological factors and less by histori- of coevolution (but see Hoberg 1992) as a source cal phylogenetic factors. This is consistent with the of zoogeographic pattern. Carney & Dick (1999, observations of Carney & Dick (in review) for para- 2000, in review) have demonstrated there are re- sites of yellow perch (Perça flavescens) in North coverable patterns across géographie and taxo- America. Carney & Dick (in review) demonstrated nomic scale for parasite-host assemblages that are that the origin of the association of several parasite not characterized by strict host-specificity. Further- species with the perch host was host-switching more, the data reported here for other species of 236 CARNEY Y, DICK TA

Table VI. - Number of shared parasites recorded from species of Oncorhynchus from North America and Eurasia. # of species indicates how many parasite species have been reported from thèse hosts.

0. O. 0. O. 0. 0. 0. 0. 0. 0. gorbuscha gorbuscha keta keta kisutch kisutch nerka nerka tshawytscha tshawytscha Eurasia North Eurasia North Eurasia North Eurasia North Eurasia North America America America America America # species 32 38 27 29 15 51 19 73 9 45

0. gorbuscha X 11 18 11 11 12 13 16 9 10 Eurasia 0. gorbuscha X 9 14 7 16 6 26 4 12 North America 0. keta X 10 9 8 8 14 6 8 Eurasia 0. keta X 8 17 9 22 4 12 North America 0. kisutch X 9 12 12 8 4 Eurasia O. kisutch X 10 28 4 26 North America 0. nerka X 13 7 7 Eurasia 0. nerka X 7 24 North America 0. tshawytscha X 3 Eurasia 0. tshawytscha X North America

percids in North America and Eurasia, indicates tion for A. tahlequahensis and A. alabamensis are that parasites of thèse hosts seem to originate with consistent with our earlier observation that strict their géographie location rather than the percid host-specificity may constrain parasite géographie hosts. This observation is supported by Carney & distribution (Price 1980). Dick (in review) who demonstrated that 3 of the In summary, parasite biogeography is histori- parasites species predictably associated with yel- cally rich and has contributed to our understanding low perch had their evolutionary origins in North of biogeographic patterns. Data from Holarctic fish America and the extant association with yellow and parasite communities are providing the basis perch resulted from host switching. The idea of for some interesting insights into factors past and géographie affinity rather than host affinity for par- présent which have and will continue to shape fish asites of North American freshwater fishes is sup- and parasite communities. Undoubtedly strict ported by Amin (1985, 1986) who considered the host-specificity and predictable associations at biogeography of 3 species of North American higher taxonomic levels contribute to defining and Acanthocephalus by combining a cladistic analysis predicting biogeographic patterns. However, in fu- of the parasites with géologie information and data ture studies we must clearly define at what level of regarding contemporary parasite géographie distri- parasite-host association we are working i.e., indi- butions. Amin (1985, 1986) proposed that thèse vidual species, genus, etc. The predictable associa- parasites were derived from an ancestor associated tions of the parasites and hosts we have discussed with the Mississippi basin prior to Wisconsinian at the highest taxonomic levels are undoubtedly an- glaciation. Retreat of the glaciers permitted wide- cient given their widespread Holarctic distribu- spread dispersai of one species, Acanthocephalus tions. It is apparent that we can not fully explain dirus, producing 3 extant parasite populations with host-parasite associations, at whatever level, only a large number of suitable hosts. The other 2 spe- on the basis of cospeciation or phylogenies of the cies have restricted géographie distributions, and a parasites and/or of the hosts, but that ecological as- small number of suitable hosts. One species, sociations and sympatric hosts with shared feeding Acanthocephalus tahlequahensis, is postulated to patterns are also important. Moreover the paucity have its géographie distribution limited by the dis- of shared parasite species across continents by tribution of its host (Amin, 1985). The other spe- closely related fish hosts for several major fish cies, A. alabamensis, may be a conséquence of groups is additional support for strong ecological vicariance associated with the Mobile River basin. and geographical influences. The application of The large number of suitable hosts and wide géo- thèse ideas is évidence of the important contribu- graphie distribution for Acanthocephalus dirus, and tions that host parasite Systems make to the study few suitable hosts and narrow géographie distribu- of biogeography. PARASITE BIOGEOGRAPHY REVIEW 237

Table VII. - Helminth and arthropod parasites recorded from Gasterosteus aculeatus and Pungitius pungitius from North America and Eurasia.

Gasterosteus Gasterosteus Pungitius Pungitius Parasite Species aculeatus aculeatus pungitius pungitius Eurasia North America Eurasia North America ECTOPARASITES

MONOGENEA Diplozoon paradoxum Gyrodactylus aculeati Gyrodactylus alexandri Gyrodactylus arcuatus Gyrodactylus armatus Gyrodactylus avalonia X Gyrodactylus bychowskyi x X Gyrodactylus canadensis X X Gyrodactylus elegans x X X Gyrodactylus eucaliae X Gyrodactylus lairdi X Gyrodactylus memorialis X Gyrodactylus rarus X X Gyrodactylus pungitii X Gyrodactylus stephanus Gyrodactylus terranovae

CRUSTACEA Argulus alosae (marine) Argulus foliaceus Argulus funduli Argulus stizostethi Bomolochus cuneatus (marine) Caligus clemensi (marine) Caligus lacustris (marine) Elthusa californica (marine) Ergasilus auritus Ergasilus manicatus Ergasilus turgidus Holobomolochus sp. (marine) Lepeophtheirus sp. (marine) Lernaea cyprinacea x Thersitina gasterostei (brackish) X

ENTERIC PARASITES

DIGENEA Azygia lucii Brachyphallus crenatus x Bunodera eucaliae Bunodera luciopercae x Bunodera mediovitellata Crepidostomum cooperi Crepidostomum farionis Derogenes varicus (marine) Hemiurus appendiculatus (marine) Hemiurus communis (marine) x Lecithaster gibbosus (marine) x Lecithaster salmonis (marine) Parahemiurus merus (marine) Peracreadium gasterostei (marine) Phyllodistomum folium Phyllodistomum pungitii Phyllodistomum sp. Podocotyle atomon (marine) x Podocotyle reflexa (marine) X Sphaerostoma bramae 238 CARNEY Y, DICK TA

Gasterosteus Gasterosteus Pungitius Pungitius Parasite Species aculeatus aculeatus pungitius pungitius Eurasia North America Eurasia North America CESTODA Bothriocephalus claviceps Bothriocephalus scorpii (marine) Cyathocephalus truncatus Eubothrium crassum Eubothrium salvelini Proteocephalus ambiguus Proteocephalus cernuae x Proteocephalus exiguus X Proteocephalus filicollis x x X Proteocephalus longicollis x Proteocephalus percae X Proteocephalus pugetensis

NEMATODA Ascarophis morrhuae (marine) Camallanus lacustris X Camallanus truncatus X Cystidicola farionis X Hysterothylacium aduncum X (marine) Philonema agubernaculum

ACANTHOCEPHALA Acanthocephalus clavula Acanthocephalus dirus Acanthocephalus lucii X X Echinorhynchus clavula X X Echinorhynchus lateralis Echinorhynchus salmonis X Leptorhynchoides thecatus Neoechinorhynchus cristatus X Neoechinorhynchus pungitius Neoechinorhynchus rutili X Paracanthocephalus curtus X Pomphorhynchus bulbocolli Pomphorhynchus laevis

LARVAL PARASITES

DIGENEA Apatemon gracilis Apophallus brevis Bucephalus polymorphus Cotylurus pileatus X Cryptocotyle concavum X Diplostomum gasterostei X X Diplostomum pungitii X Diplostomum spathaceum X X Hemiurus appendiculatus X (marine) Holostephanus lukei Ichthyocotylurus erraticus Nanophyetus salmincola Neascus sp. Posthodiplostomum cuticola Posthodiplostomum minimum Pygidiopsis ardea Tetracotyle sp. Tylodelphys clavata PARASITE BIOGEOGRAPHY REVIEW 239

Gasterosteus Gasterosteus Pungitius Pungitius Parasite Species aculeatus aculeatus pungitius pungitius Eurasia North America Eurasia North America

CESTODA Diphyllobothrium dendriticum x XXX Diphyllobothrium ditremum X X Diphyllobothrium norvegicum x X Diphyllobothrium sp. X X Ligula intestinalis Schistocephalus gasterostei X X Schistocephalus pungitii X x x Schistocephalus solidus X XXX Triaenophorus nodulosus X X X

NEMATODA Anisakis sp. (marine) x Contracaecum sp. X X Cosmocephalus obvelatus x x Eustrongylides sp. x x Hysterothylacium aduncum X (marine) Paracuaria adunca x x Pseudoterranova decipiens X X (marine) Raphidascaris acus X XXX

ACANTHOCEPHALA Corynosoma semerme (marine) X Corynosoma strumosum X X (marine)

Sources: Barysheva & Bauer 1957, Bykhovskaya-Pavlovskaya et al. 1962, Chubb 1970, Dartnall & Wackey 1979, Do- noghue 1988, Harris 1998, Hoffman 1999, Kennedy 1974, Koie 1992, 1995, Marcogliese 1992, 1995, Margolis & Arthur 1979, McDonald & Margolis 1995, Orlovskaya et al. 1995, Rokicki 1975, Scholz & Hanzelova 1998, Soleng & Bakke 1998, Sysoev et al. 1992, Wootten 1973.

Table VIII. - Number of shared parasites recorded from Gasterosteus aculeatus and Pungitius pungitius from North America and Eurasia. # of species indicates how many parasite species have been reported from thèse hosts.

Gasterosteus Gasterosteus Pungitius Pungitius aculeatus aculeatus pungitius pungitius

Eurasia North Eurasia North America America

# parasite species 53 67 35 43

Gasterosteus aculeatus X 21 25 15 Eurasia Gasterosteus aculeatus X 12 27 North America Pungitius pungitius X 12 Eurasia Pungitius pungitius X North America

ACKNOWLEDGEMENTS. - We thank an anonymous re- through a graduate fellowship and TAD thanks the Natu- viewer for constructive comments on the manuscript and ral Sciences and Engineering Research Council of Cana- Dr A Choudhury for lively discussions on the topic. JPC da for an operating grant. thanks the University of Manitoba for financial support 240 CARNEY Y, DICK TA

REFERENCES Brooks DR, Thorson TB, Mayes MA 1981. Freshwater stingrays (Potamotrygonidae) and their helminth pa- rasites: Testing hypothèses of évolution and coevolu- tion. In Advances in Cladistics. Proc first meeting of Adamson ML, Richardson JP 1989. Historical biogeo- the Willi Hennig Soc VA Funk and DR Brooks ed. graphy and host distribution of Chabaudgolvania New York Botanical Garden, New York: 147-175. spp., nematode parasites of salamanders. J Parasitol 75: 892-897. Brown JH, Gibson AC 1983. Biogeography. C.V. Mos- Aho JM, Bush AO 1993. Community richness in parasi- by, St. Louis. 643 p. tes of some freshwater fishes from North America. In Bush AO, Holmes JC 1986. Intestinal parasites of lesser Species diversity in ecological communities, histori- scaup ducks: patterns of association. Can J Zool 64: cal and geographical perspectives, RE Ricklefs & D 132-141. Schluter eds. Univ Chicago Press, Chicago: 185-193. Bykhovskaya-Pavlovskaya IE, Gusev AV, Dubinina Amin OM 1985. Hosts and géographie distribution of MN, Izyumova NA, Smirnova TS , Sokolovskaya IL, Acanthocephalus (Acanthocephala: Echinorhyn- Shtein GA, Shul'man SS, Epshtein VM 1962. Opre- chidae) from North American freshwater fishes, with delitel' parazitov, presnovodnykh ryb SSSR. Key to a discussion of species relationships. Proc Helmin- parasites of freshwater fish of the U.S.S.R. Akade- thological Soc Washington 52: 210-220. miya Nauk SSSR. Zoologicheskii Institut (Israël Pro- Amin OM 1986. On the species and populations of the gram for Scientific Translations, 1964). 919 p. genus Acanthocephalus (Acanthocephala: Echinor- Byrnes T, Rohde K 1992. Geographical distribution and hynchidae) from North American freshwater fishes: a host specificity of ectoparasites of Australian bream, cladistic analysis. Proc Biol Soc Washington 99: Acanthopagrus spp. (Sparidae). Folia Parasitologica 574-579. 39: 249-264. Bailey RE, Margolis L 1987. Comparison of parasite Caira JN 1990. Metazoan parasites as indicators of elas- fauna of juvénile sockeye salmon (Onchorhynchus mobranch biology. In Elasmobranchs as living re- nerka) from southern British Columbian and Was- sources: Advances in the biology, ecology, hington State lakes. Can J Zool 64: 420-431. systematics, and behavior, and the status of fisheries. Bailey RE, Margolis L, Workman GD 1989. Survival of HL Pratt, SH Gruber & T Taniuchi eds, NOAA Tech- certain naturally acquired freshwater parasites of ju- nical Report, NMFS 90. U.S. Dept. Commerce, vénile sockeye salmon, Oncorhynchus nerka (Wal- Seattle: 71-96. baum), in hosts held in fresh and seawater, and Caira JN 1994. Parascript: paragon or parody. Review of implications for their use as population tags. Can J Parascript: Parasites and the Language of Evolution, Zool 67: 1757-1766. by DR Brooks & DA McLennan. Bio Science 44: Bakke TA, Bailey RE 1987. Phyllodistomum umblae 771-773. (Fabricius) (Digenea, Gorgoderidae) from British Co- lumbia salmonids: a description based on light and Carney JP, Dick TA 1999. Enteric helminths of yellow scanning électron microscopy. Can J Zool 65: perch {Perça fluviatilis L.) and yellow perch {Perça 1703-1712. flavescens [Mitchill]): stochastic or predictable as- semblages ? J Parasitol 85: 785-795. Barysheyva AF, Bauer ON 1957. Parazity ryb Ladozh- skogo ozera. Izvestiya Vsesoyuznyi Nauchno-issledo- Carney JP, Dick TA 2000. Helminth assemblages of vatel'skii Institut Ozernogo i rechnogo Khozyaistva yellow perch {Perça flavescens [Mitchill]): détermi- 42: 175-226. nants of pattern. Canadian J Zool 78: 538-555. Brooks DR 1977. Evolutionary history of some plagior- Carney JP, Dick TA. Historical ecology of yellow perch chioid trematodes of anurans. Syst Zool 26: 277-289. {Perça flavescens [Mitchill]) and its parasites. J Bio- Brooks DR 1979. Testing hypothèses of evolutionary re- geography, in review. lationships among parasites: the digeneans of croco- Choudhury AC, Dick TA 1996. Observations on the sys- dilians. Am Zool 19: 1225-1238. tematics and biogeography of the genus Truttaedacni- Brooks DR 1981. Hennig's parasitological method: a tis (Nematoda: Cucullanidae). J Parasitol 82: proposed solution. Syst Zool 30: 229-249. 965-976. Brooks DR 1990. Parsimony analysis in historical bio- Choudhury A, Dick TA 1997. Parasites of the broad whi- geography and coevolution: Methodological and tefish from the Mackenzie Delta. In The proceedings theoretical update. Syst Zool 39: 14-20. of the broad whitefish workshop: the biology, tradi- Brooks DR 1992. Origins, diversification, and historical tional knowledge and scientific management of broad structure of the helminth fauna inhabiting Neotropical whitefish {Coregonuus nasus (Pallas)) in the lower freshwater stingrays (Potamotrygonidae). J Parasitol Mackenzie River (RF Tallman & JD Reist eds). Cana- 78: 588-595. dian Tech Rep Fisheries and Aquatic Sci 2193: Brooks DR, McLennan DA 1991. Phylogeny, Ecology, 167-177 p. and Behavior: A Research program in Comparative Choudhury AC, Dick TA 1998. Systematics of the De- Biology. University of Chicago Press, Chicago, xii + ropristidae Cable and Hunninen, 1942 (Trematoda) 434 p. and biogeographical considérations with sturgeons Brooks DR, McLennan DA 1993. Parascript. Parasites (Osteichthyes: Acipenseridae). Syst Parasitol 41: and the Language of Evolution. Smithsonian Institu- 21-39. tion Press, Washington, x + 429 p. Choudhury AC, Dick TA. Sturgeons (Chondrostei: Aci- Brooks DR, O'Grady RT 1989. Crocodilians and their penseridae) and their metazoan parasites: Patterns helminth parasites: macroevolutionary considéra- and processes in historical biogeography. Zool J Linn tions. Amer Zool 29: 873-883. Soc, in review. PARASITE BIOGEOGRAPHY REVIEW 241

Chubb JC 1970. The parasite fauna of British freshwater Harrison L 1928. The composition and origins of the fish. Sympos British Soc Parasitol 8: 119-144. Australian fauna, with spécial référence to the Wege- Cone DK, Wiles M 1985. The systematics and zoogeo- ner hypothesis. Rep Austral Asso Advancement Sci, graphy of Gyrodactylus species (Monogeea) parasiti- Penh 1926: 272-278 zing gasterosteid fishes in North America. Can J Zool Hennig W 1966. Phylogenetic Systematics. University 63: 956-960. of Illinois Press, Urbana, 263 p. Conneely JJ, McCarthy TK 1984. The metazoan parasi- Hoberg EP 1986. Evolution and historical biogeography tes of freshwater fishes in the Corrib catchment area, of a parasite-host assemblage: Alcataenia spp. (Cy- Ireland. J Fish Biol 24: 363-375. clophyllidea: Dilepididae) in Alcidae (Charadrifor- Craig JF 1987. The biology of perch and related fish. mes). Can J Zool 64: 2576-2589. Croom Helm Ltd., London. 333 p. Hoberg EP 1992. Congruent and synchronie patterns in Croizat L 1958. Panbiogeography. Self published. Cara- biogeography and speciation among seabirds, pinni- cas, Venezuela. 1731 p. peds, and cestodes. J Parasitol 78: 601-615. Darlington PJ, Jr 1957. Zoogeography: the geographical Hoberg EP, Adams AM 1992. Phylogeny, historical bio- distribution of animais. Wiley & Sons, Inc. 675 p. geography, and ecology of Anophryocephalus spp. (Eucestoda: Tetrabothriidae) among pinnipeds of the Dartnall HJG, Walkey M 1979. Parasites of marine stic- klebacks. J Fish Biol 14: 471-474. Holarctic during the late Tertiary and Pleistocene. Can J Zool 70: 703-709. Dick TA, Choudhury A 1996. Parasites, diseases and di- Hoffman GL 1999. Parasites of North American frews- sorders. In Pike. Biology and Exploitation. JF Craig hwater fishes. Cornell Univ Press, 539 p. ed. Chapman & Hall, London: 157-200. Holmes JC, Price PW 1986. Communities of parasites. Dogiel VA, Petrushevski GK, Polanski Yu I, eds. 1958. In Community ecology: patterns and processes. DJ Parasitology of fishes. Leningrad University Press, Anderson & J Kikkawa eds, Blackwell Sci Publ, Leningrad. Translation by Z. Kabata. T.F.H. Publica- Oxford: 187-213. tions, Hong Kong. Ihering H von 1891. On the ancient relations between Donoghue S 1988. Gasterosteus aculeatus, a new British New Zealand and South America. Transactions and host for the metacercariae of Cryptocotyle concavum Proceedings of the New Zealand Institute. 24: (Digenea). J Fish Biol 33: 657-658. 431-445. Dontsov Yu S, Markov S 1981. The effect of the régula- Ihering H von 1902. Die Helminthen als Hilfsmittel der tion of the flow of the Don on the parasite fauna of zoogeographischen Forschung. Zoologischer Anzei- Stizostedion luciopercae. Fauna, sistematika, biolo- ger 26: 42-51. giya i ekologiya gel'mintov i ikh promezhutochnykh Johnston SJ 1913. Trematode parasites and the relations- khozyaev. IzdatePstvo Gor'kovskogo Gosudarstv Pe- hips and distribution of their hosts. Rep Aust Ass dagog Inst: 17-24 (in Russian) Advancement Sci, Melbourne 14: 272-278. Dritschilo W, Cornell HD, Nafus, O'Connor B 1975. Johnston SJ 1914. Australian trematodes and cestodes: a Insular biogeography: Of mice and mites. Science preliminary study in zoogeography. Rep British Ass 190: 467-469. Advancement Sci, Australia 84: 424. Esch GW 1971. Impact of ecological succession on the Kennedy CR 1974. A checklist of British and Irish fresh- parasite fauna in centrarchids from oligotrophic and water parasites with notes on their distribution. J Fish eutrophic ecosystems. American Midland Naturalist Biol 6: 613-644. 86: 160-168. Kennedy CR 1978. The parasite fauna of résident char Esch GW, Fernandez JC 1993. A Functional Biology of Salvelinus alpinus from Arctic islands with spécial Parasitism. Chapman and Hall, London, 337 p. référence to Bear Island. J Fish Biol 13: 457-466. Gregory RD 1990. Parasites and host géographie range Kennedy CR 1993. Introductions, spread and coloniza- as illustrated by waterfowl. Functional Ecology 4: tion of new localities by fish helminth and crustacean 645-654. parasites in the British Isles: a perspective and apprai- Guégan JF, Kennedy CR 1993. Maximuim local hel- sal. J Fish Biol 43: 287-301. minth parasite community richness in British fresh- Kennedy CR, Bush AO, Aho JM 1986. Patterns in hel- water fish: a test of the colonization time hypothesis. minth communities: why are birds and fish so diffé- Parasitol 106: 91-100. rent ? Parasitology 93: 205-215. Guégan JF, Lambert A 1990. Twelve new species of Khalil LF 1971. The helminth parasites of African fresh- dactylogyrids (Platyhelminthes, Monogenea) from water fishes Part I: Zoogeographical affinities. Rev West African barbels (Teleostei, Cyprinidae), with Zool Bot Afr (Bruxelles) 84: 236-263. some biogeographical implications. Syst Parasitol Klassen G 1992a. Coevolution: a history of the macroe- 17: 153-181. volutionary approach to studying host-parasite asso- Guégan JF, Lambert A , Leveque C, Combes C, Euzet L ciations. J Parasitol 78: 573-587. 1992. Can host body size explain the parasite species Klassen G 1992b. Revision of Haliotrema species (Mo- richness in tropical freshwater fishes ? Oecologia 90: nogenea: Ancyrocephalidae) from Atlantic boxfishes 197-204. (Tetraodontiformes: Ostraciinae): morphology, mor- Harris PD 1998. Extrême morphological variation bet- phometrics, and distribution. Can J Zool 69: ween related individuals of Gyrodactylus pungitii 2523-2539. Malmberg, 1964 (Monogenea). Syst Parasitol 39: Koie M 1992. Scanning électron microscopy of cer- 137-140. cariae, metacercariae and adults of Pygidiopsis ardea Harrison L 1926. Crucial évidence for antarctic radia- Koie, 1990 (Digena: Heterophyidae). Parasitol Res tion. Am Nat 60: 374-383 78: 469-474. 242 CARNEY Y, DICK TA

Koie M 1995. The life-cycle and biology of Hemiurus Metcalf MM 1940. Further studies on the opalinid infu- communis Odhner, 1905 (Digenea, Hemiuridae). Pa- sorians and their hosts. Proc Unit St Mus 87: rasite 2: 195-202. 465-634. Kuris AM, Blaustein AR 1977. Ectoparasitic mites on Molnar K 1980. Récent observations on the developmen- rodents: Application of the island biogeography theo- tal cycle of Philometra obturans (Prenant, 1886) (Ne- ry ? Science 195: 596-597. matoda, Philometridae). Parasitol Hung 13: 65-66. Lawler GH, Scott WB 1954. Notes on the geographical Morrone JJ, Carpenter JM. 1994. In search of a method distribution and the hosts of the cestode genus Triae- for cladistic biogeography: An empirical comparison nophorus in North America. / Fish Res Board Cana- of component analysis, Brooks parsimony analysis, da 11: 884-893. and three area statements. Cladistics 10: 99-153. Lovejoy NR 1996. Systematics of myliobatoid elasmo- Morrone JJ, Crisci JV 1995. Historical biogeography: branchs: With emphasis on the phylogeny and bio- Introduction to methods. Annual Rev Ecol Syst 26: geography of Neotropical freshwater stingrays 373-401. (Potamotrygonidae). Zool J Linn Soc 117: 207-257. Nagasawa K, Egusa S, Hara T, Yagisawa I 1983. Ecolo- gical factors influencing the infection levels of sal- Lovejoy NR 1997. Stingrays, parasites, and Neotropical monids by Acanthocephalus opsariichthydis biogeography: A closer look at Brooks et al.'s hypo- (Acanthocephala: Echinorhynchidae) in Lake Yuno- thèses concerning the origins of Neotropical freshwa- ko, Japan. Fish Pathology 18: 53-60. ter rays (Potamotrygonidae). Syst Biol 46: 218-230. Orlovskaya OM, Atrashkevich GI, Barshene YV 1995. MacArthur RH, Wilson EO 1967. The Theory of Island Phyllodistomum pungitii sp. n. (Trematoda: Gorgode- Biogeography. Princeton Univ Press, Princeton, ridae) from the fish Pungitius pungitius of Chukotka. U.S.A., 203 p. Parazitologiya 29: 532-537 (in Russian). Manter HW 1940. The geographical distribution of dige- Ôzcelik A, Deufel J 1989. Unterschungen ûber fischpa- netic trematodes of marine fishes of the tropical Ame- rasitàre Wurmer im Bodensee. Zeitsch Angew Zool rican Pacific. Allan Hancock Pacific Exped 2: 76: 27-59 531-547. Page RDM 1988. Quantitative cladistic biogeography: Manter HW 1955. The zoogeography of trematodes of Constructing and comparing area cladograms. Syst marine fishes. Exper Parasitol 4: 62-86. Zool 37: 254-270. Manter HW 1963. The zoogeographical affinities of tre- Page RDM 1989. Component, Release 1.5. University of matodes of South American freshwater fishes. Syst Auckland, New Zealand. Zool 12: 45-70. Page RDM 1990. Component analysis: A valiant fai- Manter HW 1966. Parasites of fishes as biological indi- lure ? Cladistics 6: 119-136 cators of récent and ancient conditions. In Host-para- Page RDM 1994a. Maps between trees and cladistic ana- site relationships JE McCauley ed. Oregon State Univ lysis of historical associations among gènes, orga- Press, Corvallis: 59-72. nisms, and areas. Syst Biol 43: 58-77. Marcogliese DJ 1992. Metazoan parasites of stickle- Page RDM 1994b. Parallel phylogenies: Reconstructing backs on Sable Island, Northwest Atlantic Océan: the history of host-parasite assemblages. Cladistics biogeographic considérations. J Fish Biol 41: 10: 155-173. 399-407. Pielou EC 1979. Biogeography. John Wiley and Sons, Marcogliese DJ 1995. Comparison of parasites of mum- New York. 351 p. michogs and sticklebacks from brackish and freshwa- Platt TR 1992. A phylogenetic and biogeographic analy- ter ponds on Sable Island, Nova Scotia. Am Midland sis of Spirorchinae (Digenea: Spirorchidae) parasitic Nat 133: 333-343. in freshwater turtles. / Parasitol 78: 616-629. Marcogliese DJ, Cone DK 1991. Do brook charr (Salve- Pojmanska T, Grabda-Kazubska B, Kazubski SL, Ma- linus fontinalis) from insular Newfoundland have dif- chalska J, Niewiadomska K 1980. Parasite fauna of férent parasites than their mainland counterparts ? five fish species from the Konin lakes complex, artifi- Can J Zool 69: 809-811. cially heated with thermal effluents, and from Goplo Marcogliese DJ, Cone DK 1993. What metazoan parasi- Lake. Acta Parasitol Pol 27: 319-357. tes tell us about the évolution of American and Euro- Poulin R 1995. Phylogeny, ecology, and the richness of pean eels. Evolution Al: 1632-1635. parasite communities in vertebrates. Ecol Monogr 65: 283-302. Margolis L, Arthur JR 1979. Synopsis of the parasites of fishes of Canada. Bull Fish Res Board Canada 199: Price PW 1980. Evolutionary Biology of Parasites. Prin- 269 p. ceton University Press, Princeton, U.S.A., 237 p. Price PW, Clancy KM 1983. Patterns in number of hel- McDonald TE, Margolis L 1995. Synopsis of the parasi- minth parasite species in freshwater fishes. J Parasi- tes of fishes of Canada: supplément (1978-1993). Can tol 17: 209-214. Sp Publ Fish Aqu Sci 122: 265 p. Pronin NM, Ryzhova LN, Tugarina PYa, Tyutrina LI Metcalf MM 1920. Upon an important method of stu- 1979. Physiological and parasitological examination dying the problems of relationship and geographical of Thymallus arcticus nigrescens (Lake Khubsugul, distribution. Proc Nat Acad Sci USA 6: 432-433. Mongolian National Republic). Zooparazitologiya Metcalf MM 1923. The origin and distribution of the basseina ozera Baikal. Akademiya Nauk SSSR, Si- Anura. Am Nat 57: 385-411. birskoi Otdelenie: 106-121. Metcalf MM 1929. Parasites and the aid they give in Pugachev ON 1984. Monogenean fauna from the family problems of taxonomy, geographical distribution, and Tetraonchidae Bychowsky, 1937. Parazitologiya 18: palaeogeography. Smithson Miscel Coll 81: 1-36. 30-39 (in Russian). PARASITE BIOGEOGRAPHY REVIEW 243

Rohde K 1978. Latitudinal différences in host-specifici- Syosev AV, Hanzelovâ V, Yakushev VY, Freze VI. ty of marine Monogenea and Digenea. Mar Biol 47: 1992. Some peculiarities of the process of infection 125-134. transmission in cestodes of the genus Proteocephalus. Rohde K 1982. Ecology of Marine Parasites. Univ Helminthologia 29: 19-23. Queensland Press, St. Lucia, Australia, 298 p. Valtonen ET 1980. Metechinorhynchus salmonis (Mul- Rohde K 1986. Différences in species diversity of Mo- ler, 1780) (Acanthocephala) as a parasite of the whi- nogenea between the Pacific and Atlantic océans. Hy- tefish in the Bothnian Bay. I. Seasonal relationships drobiologia 137: 21-28. between infection and body size. Acta Parasitol Pol Rokicki J 1975. Helminth fauna of fishes of the Gdansk 27: 293-300. Bay (Baltic Sea). Acta Parasitol Pol 23: 37-84. van Maren MJ 1979. The amphipod Gammarus fossarum Scholz T, Hanzelovâ V 1998. Tapeworms of the genus Koch (Crustacea) as intermediate host for some hel- Proteocephalus Weinland, 1858 (Cestoda: Proteoce- minth parasites, with notes on their occurrence in the phalidae), parasites of fishes in Europe. Academia, final host. Bijdr Dierk 48: 97-110. Publ House Acad Sci Czech Republic, Praha, 118 p. Vrba ES 1985. Environment and évolution: alternative Shostak AW, Dick TA, Szalai AJ, Bernier LMJ 1986. causes of the temporal distribution of evolutionary Morphological variability in Echinorhynchus gadi, E. events. South Afr J Science 81: 229-236. leidyi and E. salmonis (Acanthocephala: Echinorhyn- Waluga D, Wlasow T 1988. Wystepowanie pasozytôw chidae) from fishes in northern Canadian waters. Can uleszcza {Ambramis brama L.), ploci {Rutilus rutilus J Zool 64: 985-995. L.) i sandacza {Stizostedion lucioperca L.) we wlo- Shulman SS 1958. Zoogeography of parasites of USSR clawskim zbiorniko zaporwym na rzece wisle. Wiad freshwater fishes. In Parasitology of Fishes. VA Do- Parazytol 34: 65-75. giel, GK Petrushevski & Yu I Polyanski eds. Lenin- Whitaker DJ 1985. A parasite survey of juvénile chum grad Univ Press Leningrad. Transi Z Kabata, T. F. H. salmon {Oncorhynchus keta) from the Nanaimo Ri- Publ Hong Kong: 180-229 p. ver. Can J Zool 63: 2875-2877. Soleng A, Bakke TA 1998. The susceptibility of Wiley EO 1981. Phylogenetics: The Theory and Practice three-spined stickleback {Gasterosteus aculeatus), of Phylogenetic Systematics. Wiley-Interscience, nine-spined stickleback {Pungitius pungitius) and New York. flounder {Platichthys flesus) to expérimental infec- Wiley EO 1988. Parsimony analysis and vicariance bio- tions with the monogenean Gyrodactylus salaris. Fol geography. Syst Zool 37: 271-290. Parasitol (Ceske Budojovice) 45: 270-274. Wootten R 1973. The metazoan parasite-fauna of fish Straney DO 1982. Review of Advances in Cladistics: from Hammingfield Réservoir, Essex in relation to Proc First Meeting Willi Hennig Society, VA Funk & features of the habitat and host populations. J Zool, DR Brooks eds. Syst Zool 31: 337-341. London 171: 323-331.