ecological versus phylogenetic determinants of helminth parasite community richness

20

Click here to load reader

Upload: albert-o-bush

Post on 10-Jul-2016

220 views

Category:

Documents


5 download

TRANSCRIPT

Page 1: Ecological versus phylogenetic determinants of helminth parasite community richness

Evolutionary Ecology, 1990, 4, 1-20

Ecological versus phylogenetic determinants of helminth parasite community richness

A L B E R T O. BUSH* Department of Zoology, Brandon University, Brandon, Manitoba R7A 6A9, Canada

JOHN M. A H O Savannah River Ecology Laboratory, University of Georgia, Drawer E, Aiken. South Carolina 29801, USA

CLIVE R. K E N N E D Y Department of Biological Sciences, Hatherly Laboratories, University of Exeter, Exeter, EX4 4PS, UK

Summary

We examine patterns of community richness among intestinal parasitic helminth communities in fishes, herptiles, birds and mammals with respect to the comparative number of component species in a host population. We show that terrestrial hosts have, on average, fewer component species than aquatic hosts. We also show that the mean number of component species in aquatic hosts increases from fishes through herptiles to birds before declining slightly in mammals. For terrestrial hosts, the mean number of component species increases from herptiles, through birds, reaching a maximum in mammals. We conclude that: (i) habitat of the host is more important in determining community richness than is host phylogeny; (ii) the phenomenon of 'host capture' may be largely responsible for increased species richness in some host groups; (iii) aquatic birds harbour the richest intestinal helminth communities; and (iv) as we interpret them, our data refute the time hypothesis, which would predict that fishes as the oldest lifestyle should have the richest helminth communities.

Keywords: Community development; community richness; component species; evolution; habitat; helminths; host capture; parasites; phylogeny; species richness; time hypothesis.

Introduction

Interpreting the species richness component of community structure is a common challenge to many ecologists. Several recent authors address the time hypothesis in an attempt to explain different patterns of species richness. Its most frequent application is to communities of herbivorous insects, the essential prediction being that the longer the 'host' has been available (i.e. in evolutionary time), the greater the likelihood that it will have more herbivores than a host which is recent (i.e. evolutionarily young). The hypothesis seems intuitive, at least in a general sense, and it supports an evolutionary argument as a determinant of species richness.

There are data which both support and refute the hypothesis. Southwood (1961) presents data to suggest that those species of trees with a more extensive fossil record support more species of insects. Birks (1980), using new estimates for the evolutionary age of trees in Britain, confirms

* Order of authorship determined by random draw and does not imply seniority.

0269-7653/90 $03.00+. 12 �9 1990 Chapman and Hall Ltd.

Page 2: Ecological versus phylogenetic determinants of helminth parasite community richness

2 Bush, Aho and Kennedy

a time effect for the number of insects on trees. Lawton and Price (1979) argue that evolutionary time might be important in the enrichment of herbivorous insect communities. In marked contrast, Boucot (1983) presents paleontological data which refute the hypothesis. Strong et al. (1977) and Rey et al. (1981) argue against the hypothesis using data on phytophagous insects attacking introduced plants. In all these studies, authors had to infer host age (i.e. time) by using fossil records or they had to derive age from data on introduced monocultures (which, although very accurate about time, represent very short evolutionary intervals). To our knowledge, no one has addressed the predictions of the time hypothesis using extant data on natural systems, where the comparative age of the host groups is undisputable, and as an hypothesis supporting a phylogenetic argument for the development of species rich communities.

We believe that helminth parasites in vertebrate hosts are ideal for testing this hypothesis, since all groups of vertebrates, from the oldest to the youngest, have a wide variety of heiminth parasites. For helminth communities in vertebrates, the time hypothesis would predict that phylogenetically older groups (e.g. fishes) would have greater species richness than phylogeneticaily younger groups (e.g. mammals). Recognizing that all vertebrates have a common ancestor, and in that sense are the same 'age', what we actually examine are adaptations of helminths to the derived characteristics of the vertebrate groups, which we will call their 'lifestyles'.

In this paper we evaluate the time hypothesis, specifically by comparing richness of gut helminths in the major vertebrate groups (fishes through mammals). Based on our collective years of experience in looking at helminth communities, we have an a priori expectation that aquatic hosts (regardless of taxa) will have more parasites than terrestrial hosts. We will thus evaluate phylogenetic differences ('evolutionary age') within major habitats, e.g. the four vertebrate groups within aquatic systems and the three vertebrate groups within terrestrial systems; we will then evaluate major habitat differences (aquatic versus terrestrial) within the major vertebrate groups.

Methods

Data sets

The four vertebrate groups we examine include fishes, herptiles, birds and mammals. We combine amphibians and reptiles since a study by one of us (Aho, 1990) shows no difference between those classes, with respect to the parameters we examine. In compiling the data, we relied solely on published literature dating from the early 1900s to the present. Although we attempted to obtain data from throughout the World, most published accounts are from hosts in north temperate regions; very few data are available (at least to us) on tropical systems. For fishes, the global coverage was much better than for all other groups. We regard the minimum usable host population size as ten individuals of each host species (i.e. all surveys provide data on at least ten individual hosts) except for marine mammals where, to obtain more data, it was necessary to lower the minimum to seven. We accept the original author's taxonomy and use only studies in which data on the entire intestinal helminth community, from immediately posterior to the stomach through the anus/cloaca/rectum, are available. We restrict our examinations to intestines as that region is the most preferred site for adult helminths (Mettrick and Podesta, 1974). These restrictions inevitably result in uneven coverage among host groups and habitats and limit our database. For example, we were unable to obtain large samples of aquatic herptiles.

Component species list

We were unable to obtain data on the actual number of helminth species found in each host

Page 3: Ecological versus phylogenetic determinants of helminth parasite community richness

Helminth parasite community structure 3

individual; most of the data available to us are summaries, e.g. prevalence or frequency of a particular helminth in a given sample of a host population. This meant that we could not reconstruct actual infracommunities, e.g. we could not determine that host individual A had 3 species, host individual B had 5 species, etc. This forced us to analyze the data at the component community level (sensu Root, 1973; Holmes and Price, 1986). The measure we adopt is the maximum number of helminths (which we will call 'component species' and which we describe below) reported from any survey on any host species. For multiple surveys on the same host species, we record the maximum number of helminths for each survey. While theuse of data at the component level has the disadvantage of obscuring observations at the individual host level, it is the best descriptor of community richness at the host population level.

In an attempt to eliminate accidental infections, we count, as component species, only those helminths found in -> 10% of the host sample, recognizing that this could also eliminate some host specific and generalist species occurring infrequently. With respect to our subsequent analyses, this would predetermine our results only if one of the major groups (e.g. aquatic birds) we examine has large numbers of such species. We are unaware of any data that would substantiate such an idea. We recorded the number of component species regardless of host age, sex or season of collection.

We have prepared a data file, in a more readable form than the Appendix, with the following features: we subdivide the major host groups into aquatic, amphibious or terrestrial; under each of the appropriate headings, we provide the scientific name for hosts used in the analyses, the number of studies on each host, the number of component species recorded in each study and the author(s) for each study. Interested individuals can send a formatted disk to AOB (Microsoft Word [31/z or 51/4]) or JMA (Wordstar [51/4]).

Statistical analyses The best fit for our data was a log normal distribution. We therefore use a log10 (N + 1) transformation. We use programs in Systat (Wilkinson, 1988) to calculate ANOVA and Tukey- Kramer HSD tests. For derived values in Fig. 1, means are I0 ~ - 1 and asymmetric confidence

i

intervals are means + 2 SE - 1 (Sokal and Rohlf, 1981; p. 418).

Results

We were able to obtain data on 582 different host species based on 1222 studies (i.e. there were multiple studies for some host species; Appendix 1). Our data include 587 studies on 245 species of fishes, 197 studies on 112 species of herptiles, 128 studies on 84 species of birds and 310 studies on 141 species of mammals. There was no significant difference in the mean number of component species between freshwater and marine fishes (2.9 + 1.9 and 3.2 + 2.3, respectively [t = 0.9, p = 0.32]). Therefore, we combine data on all fishes for our analyses. Our sample sizes for marine herptiles, birds and mammals are too small to make similar comparisons and we arbitrarily combine such hosts with their freshwater counterparts as being aquatic. For illustrative purposes, we include data on amphibious herptiles in Table 1 and Fig. 1. We do not include those data (53 species, 98 studies) in our analyses since neither we nor our colleagues could consistently assign individual species as either truly aquatic or terrestrial.

In Table 1, we present comparative data on the number of component species among the four host groups we examine. Two features are apparent. Combining aquatic and terrestrial habitats within each major taxonomic group (i.e. looking strictly for phylogenetic differences) there is little change in the median between groups, but there are obvious differences in the 75th quartiles (Table 1). This parameter decreases from fish to herptiles before increasing to birds and then

Page 4: Ecological versus phylogenetic determinants of helminth parasite community richness

4 Bush, Aho and Kennedy

co ii i

13. CO

F- Z UJ Z o a . :E 0 o u . 0

n - i i i m

z

2

1

0 , i i i 1 ~ i

,- . " -," / Sio, , o

Figure 1. Comparison of mean numbers of component parasite species between the major groups. Open bars represent aquatic groups, diagonal lines within bars represent terrestrial groups and the cross-hatched bar represents amphibious herptiles. Data are means + 95% confidence intervals (see text for elaboration).

Table 1. Summary data for the number of component helminth parasites among vertebrate groups from different habitats.

Component Species Number of Studies Mean (+ SD) 25% Median 75%

Fishes 587 3.0 + 2.1 1.0 3.0 4.0 Herptiles 197 2.0 + 1.7 1.0 2.0 3.0

Aquatic 27 4.0 + 2.8 2.0 4.0 5.5 Amphibious 98 1.8 + 1.3 1.0 2.0 2.0 Terrestrial 72 1.6 + 1.2 1.0 1.0 2.0

Birds 128 4.3 + 4.3 1.0 3.0 6.0 Aquatic 59 6.3 + 5.4 2.5 5.0 8.5 Terrestrial 69 2.6 + 1.9 1.0 2.0 4.0

Mammals 310 3.4 + 2.5 2.0 3.0 5.0 Aquatic 63 4.9 + 2.9 3.0 4.0 6.0 Terrestrial 247 3.1 _+ 2.2 1.0 3.0 4.0

Page 5: Ecological versus phylogenetic determinants of helminth parasite community richness

Helminth parasite community structure 5

declining in mammals (but not as low as in either fishes or herptiles). It is clear that birds have the greatest potential for richer component communities (Fig. 1). When we examine the data by major habitat groupings within host taxa (i.e. looking for habitat associated differences) terrestrial hosts consistently have fewer component species than aquatic hosts (Fig. 1).

We use two methods to evaluate phylogenetic versus ecological differences. First, we examine for differences between vertebrate groups but within the same habitat, e.g. ANOVA on the number of component species in fishes, aquatic herptiles, aquatic birds and aquatic mammals. Comparing aquatic taxa, there was significant variance (F3.733 = 19.4, p < 0.001). Fish have significantly fewer component species than either birds (p < 0.001) or mammals (p < 0.002); herptiles have significantly fewer component species than birds (p < 0.02). The difference between herptiles and mammals was equivocal (p = 0.085). Comparing terrestrial taxa, there was also significant variance (F2,385 = 14.4, p < 0.001). Here, herptiles have significantly fewer component species than either birds (p < 0.01) or mammals (p < 0.001). Second, we make comparison, within each vertebrate group, between aquatic and terrestrial species, e.g., aquatic versus terrestrial birds. For all comparisons, aquatic hosts have more component species than their terrestrial counterparts (one degree of freedom and p < 0.001 for all tests): herptiles (t = 4.7), birds (t = 4.7), mammals (t = 5.2).

Discussion

Because of the nature of the data available, two caveats are necessary. First, we recognize that, ideally, it would be preferable to use data at the individual host level. However, to do so would restrict us largely to the use of our own data sets and we could not then have achieved the necessary breadth of coverage. Second, we recognize that the terms aquatic and terrestrial may have a phylogenetic connotation (e.g. the Class Pisces is de facto aquatic). Instead, we use them to make distinctions based on ecological grounds, since different habitats and environments pose different problems to the acquisition of helminths by hosts.

In the present study, we find little evidence that phylogenetic aspects play a major role in the development of helminth communities. We find fish and herptiles to have the least number of component species; the numbers increase significantly in birds and then decline slightly to mammals. This pattern of change refutes the time hypothesis which would predict that fishes, as the oldest group, would have the richest communities. Additional evidence against the time hypothesis is the lack of any significant difference in community richness between older marine and younger freshwater fishes. Before we pursue this line of reasoning, we first address the implications of the time hypothesis as we have used it.

A fair test? We adopt an accepted tenet, namely, fish are older than herptiles; birds and mammals are recent contemporaries. For our analyses and subsequent test of the time hypothesis, the uncritical acceptance of this tenet, in its broadest interpretation, could be misleading. For example, we attempted to gather all data, on all vertebrate groups, that were reasonably available to us. As such, our data on fishes include examples spanning the range from acknowledged 'old' fishes (e.g. Amia, Acipenser) to more recent fishes (e.g. the Cyprinidae). It is perfectly reasonable to argue that some of the most recent cyprinids are, in fact, younger than some of the 'older' herptiles or even some of the 'older' birds or mammals. Unfortunately, the 'age' of various taxa (e.g. orders, families, species) within the major vertebrate groups are not clearly resolved, making more detailed analyses difficult and/or of questionable interpretation. A further problem is that there are few data on 'old' hosts (regardless of major group). We are currently generating

Page 6: Ecological versus phylogenetic determinants of helminth parasite community richness

6 Bush, Aho and Kennedy

new data sets on fishes, the group for which we feel that comparative age of different levels of taxa are clearest, and will attempt a more fine-grained analysis in the future (e.g. 'old' versus 'young' species). Finally, when attempts are made to interpret data at too fine a scale, e.g. a particular species of parasite in a particular host species, the resolution of phylogenetic versus ecological determinants is debatable (e.g. Brooks, 1980a, b; Holmes and Price, 1980).

For our interpretation, we use the time hypothesis as a method to evaluate the importance of phylogenetic factors on the development of species-rich helminth communities. For example, we would argue that fish, as a lifestyle (i.e. their derived characters which make them a 'fish') represent the 'oldest' form. For that reason, there has been a greater period of time for helminths to exploit that particular lifestyle. In short, even 'recent' fishes should encounter parasites which have had more time to surmount the difficulties in exploiting the 'fish' lifestyle. Helminths exploiting the herptile lifestyle are intermediate and helminths of birds and mammals have had a correspondingly shorter evolutionary interval to overcome the same obstacles.

Interpretation of patterns

Price (1983) suggests apparent parallels of the time hypothesis with Wilson's (1969) four evolutionary phases of community development. In fact, these phases suggest a mechanistn for why the time hypothesis would predict increasing species richness with increasing age. For example, fishes, as the oldest group, should harbour the greatest species richness because of niche diversification; whereas birds and mammals, the most recent evolutionary contemporaries, should harbour less rich communities but there should be more evidence for interactions between helminth species. As we have already argued for the time hypothesis, neither fishes nor herptiles fit the predicted pattern. While much of the evidence from birds might appear to support the predictions for Wilson's interactive (phase 2) communities (e.g. Riley and Owen, 1975; Pojmanska, 1982; Bush and Holmes, 1986a; Stock and Holmes, 1987; Goater and Bush, 1988; Edwards and Bush, 1989), their species richness clearly places them near the evolutionary end (phase 4). In mammals, the evolutionary contemporaries of birds, we find less evidence for interactive communities, despite the fact that they exhibit similar levels of species richness. We therefore conclude that our data, as we interpret them, do not conform to Wilson's four evolutionary phases. We again acknowledge that when evolutionary relationships within the major vertebrate groups are more clearly resolved and more data on ancient hosts are available, different patterns may emerge within such groups.

Although our data fail to support host phylogeny as a major determinant of community richness, we can occasionally detect a phylogenetic component. When, from a group that is primarily terrestrial, some mammals secondarily return to water, they may retain a depauperate heiminth fauna, characteristic of (sometimes even less than) terrestrial members of their group (e.g. Delphinapterus leucus (Wazura et al., 1986)). But, since we found a greater number of examples where they acquire the species richness we observe for other aquatic vertebrates, this is not universally true (e.g. Ondatra zibethicus (Beckett and Gallicchio, 1967; Rigby and Threlfall, 1981); Eumetopias jubatus (Stroud and Dailey, 1978; Shults, 1986)). In fact, the major patterns suggest the importance of ecological determinants. This is shown by the overwhelming differences in community richness between aquatic and terrestrial hosts. Within every vertebrate group there were significantly more component species in the aquatic members. Anecdotally, our data on amphibious herptiles lend additional support for this observation. Most evolutionary ecologists tend to think of amphibians as being the 'first' land vertebrates, as opposed to the 'last' aquatic vertebrates. Data in Table 1 and in Fig. 1 show that, with respect to the number of component parasites, amphibious herptiles are comparable to their terrestrial, not their aquatic, counterparts. However we look at the data, we reach the conclusion that habitat is a far more important determinant of community richness than is phylogeny.

Page 7: Ecological versus phylogenetic determinants of helminth parasite community richness

Helminth parasite community structure 7

Why should this be so? We interpret the patterns we see as follows. Aquatic hosts encounter a greater diversity of heiminth species. The Cestoda exploit mostly aquatic hosts. Though found in all groups of hosts, most orders are exclusively aquatic, many are primarily so; all orders have aquatic members and only one, the Cyclophyllidea, has a substantial number of terrestrial species (Wardle and McLeod, 1952). Trematodes are primarily linked to aquatic systems because of the dependence of their free-living miracidia and cercaria upon water. Only a minority of species circumvent these requirements, e.g. by retention of the miracidia in the egg or by elimination of the free-living cercarial stage (Dawes, 1946). In very rare cases, there may also be transmammary transfer of adult trematodes from mother to offspring (Shoop, 1988). Acantho- cephala infect aquatic and terrestrial hosts almost equally, with a slight edge for more taxa in aquatic hosts. Thus, the greatest numbers of species are in the fishes and the aquatic herptiles, birds and mammals (Yamaguti, 1959; Petrochenko, 1971a, b). Only the parasitic Nematoda flourish on land (Anderson, 1984, 1988). Although some use intermediate hosts or vectors, the majority have direct life cycles and a resistant cuticle and thus are particularly well adapted to exploiting terrestrial hosts, primarily grazing mammals. The nematodes also seem to have the most catholic distributions. A good example is the family Capillariidae which is parasitic in virtually all vertebrate classes (Moravec et al., 1987). Their unparalleled success at widespread exploitation appears to be a function of the diversity of life cycles they employ.

Although we recognize that host-helminth phylogenetic tracking contributes to increasing richness of helminth communities (Brooks, 1979, 1980a; Glen and Brooks, 1986), the phenomenon of 'host capture' (an ecological argument; Chabaud, 1959, 1965; Bartlett and Greiner, 1986) may be of far greater importance. We are unable to find any evidence that fish have captured helminths from any other group of vertebrates. By contrast, while herptiles harbour some terrestrial helminth species specifically adapted to them (e.g. Schad, 1963; Baker, 1984), we would argue that they have also captured several helminths from fish, e.g. bothriocephalid cestodes, acanthostomid trematodes and neoechinorhynchid acanthocephalans. In addition some of their other helminths are clearly related to fish helminths, e.g. polystomatid monogeneans. Similarly, birds and mammals have also captured helminths from fishes (e.g. tetrabothriid cestodes (Hoberg, 1987); and, we would suggest, diphylobothriid cestodes), birds have captured trichostrongylid nematodes from mammals (Chabaud, 1965) and mammals have captured filarioid nematodes from birds (Bartlett and Greiner, 1986). By contrast, we know of no examples of capture, by older groups, from more recent groups. Capture always appears to proceed from older groups to more recent groups or between contemporaries. Where mammal helminth communities are speciose, it is often because they have captured an entire suite of host generalists, e.g. microphallid trematodes in Oryzomys and Procyon. This pattern is particularly exemplified in some mammals. When they return to the sea, they can acquire a helminth assemblage qualitatively similar to that of marine birds (i.e. tetrabothriid and diphylobothriid cestodes, anisakid nematodes and microphallid trematodes), in essence, making them 'honorary birds'.

With rare exception, we observe similar patterns in the use of intermediate hosts by helminths. All major groups use fish as intermediate hosts, e.g. fish-fish (triaenophorid cestodes), fish-herptile (proterodiplostomatid trematodes), fish-bird (ligulid cestodes, diplo- stomatid trematodes), fish-mammal (diphylobothriid cestodes, anisakid nematodes). Herptiles can be true intermediate hosts for other herptiles (proteocephalid cestodes or lechriorchid trematodes), for birds (tylodelphid trematodes) or mammals (sparganid cestodes and alarid trematodes). Birds may use mammalian links (parauterinid cestodes) and mammals may use mammal-mammal links (taeniid cestodes), but birds themselves appear never to act as intermediate hosts. (There may be a rare exception to this; Bartlett et al. (1987) have described an encysted spirurid nematode associated with the mesenteries of two species of shorebirds. It

Page 8: Ecological versus phylogenetic determinants of helminth parasite community richness

8 Bush, Aho and Kennedy

is unclear if these are accidental or whether the infected birds are, in fact, acting as an intermediate host. Further, if they are acting as-an intermediate host, whether the final host is a bird of prey or a mammal is not known.) The known exception to this general pattern, anisakid nematodes, matures in snakes and uses mammals for intermediate hosts.

Fish as the oldest group, have the least rich helminth communities among aquatic hosts, but they are still comparable to all terrestrial groups (Fig. 1). Aquatic birds are clearly the 'tropics' of the parasite world. And, just as species flocks characterize the tropics e.g. cichlid fishes, geospizid finches, pseudomid rodents, drosophilid flies, eucalyptid trees, so too do they appear to characterize the helminth communities in aquatic birds (e.g. Bush and Holmes, 1986b; Stock and Holmes, 1987; Goater and Bush, 1988; Edwards and Bush, 1989).

Acknowledgements

We thank Professors J. C. Holmes and V. L. Kontrimavichus for stimulating our ideas on this subject. We thank Professors John C. Holmes, Stuart L. Pimm and Michael L, Rosenzweig for valuable comments on an earlier version of this manuscript and we thank Professor Jeff Williams for statistical advice. The research of A.O.B. is supported by N.S.E.R.C. Canada operating grant A-8090, of J .M.A. by Contract DE-AC09-76SR00819 between the U.S. Depar tment of Energy and the University of Georgia's Savannah River Ecology Laboratory, and of C.R.K. by the University of Exeter.

References

Aho, J. M. (1990) The structure of helminth communities of amphibians and reptiles. Parasite Communities: Patterns and Processes (G. W. Esch, A. O. Bush and J. M. Aho, eds) pp. 157-96. Chapman and Hall, London.

Anderson, R. C. (1984) The origins of zooparasitic nematodes. Canad. J. Zool. 62, 317-28. Anderson, R. C. (1988) Nematode transmission patterns. J. Parasitol. 74, 30-45. Baker, M. R. (1984) Nematode parasites in amphibians and reptiles. Canad. J. Zool. 62, 747-57. Bartlett, C. M. and Greiner, E. C. (I986) A revision of Pelecitus Raillet and Henry, I910 (Fflarioidea,

Dirofilariinae) and evidence for the "capture' by mammals of filarioids from birds. Bull. Musee Natle. d'Hist. Natur., Paris 8A, 47-99.

Bartlett, C. M., Bush, A. O. and Anderson, R. C. (1987) Unusual finding of encapsulated nematode larvae (Spiruroidea) in Bartramia longicauda and Numenius americanus (Charadriiformes) in western Canada. J. Wildl. Dis. 23, 591-5.

Beckett, J. V. and Gallicchio, V. (1967) A survey of helminths of the muskrat, Ondatra z. zibethica Miller, 1912, in Portage County, Ohio. J. Parasitot. 53, 1169-72.

Birks, H. J. B. (1980) British trees and insects: a test of the time hypothesis over the last 13,000 years. Amer. Natur. 115, 600-5.

Boucot, A. J. (1983) Area-dependent-richness hypothesis and rates of parasite/pest evolution. Amer. Natur. 121,294--300.

Brooks, D. R. (1979) Testing hypotheses of evolutionary relationships among parasites: the digeneans of crocodilians. Amer. Zool. 19, 1225-38.

Brooks, D. R. (1980a) Allopatric speciation and non-interactive parasite community structure. Syst. Zool. 29, 192-203.

Brooks, D. R. (1980b) Brooks' response to Holmes and Price. Syst. Zool. 29, 214-15. Bush, A. O. and Holmes, J. C. (1986a) Intestinal helminths of lesser scaup ducks: an interactive

community. Canad. J. Zool. 64, 142-52. Bush, A. O. and Holmes, J. C. (1986b) Intestinal helminths of lesser scaup ducks: patterns of association.

Canad. J. Zool. 64, 132--41. Chabaud, A. G. (1959) Remarques sur l'evolution et la taxonomic chez les nematodes parasites de

Vertebres. Proc. Int. Congr. Zool. 15, 679-80.

Page 9: Ecological versus phylogenetic determinants of helminth parasite community richness

Helminth parasite community structure 9

Chabaud, A. G. (1965) Specificite parasitaire. I. Chez les nematodes parasites de Vertebres. In Traite de Zoologie. Anatomie, Systematique, Biologie. Vol. 4, Part 2. Nemathelminthes (Nematodes) (P. P. Grasse ed.) pp. 548-64. Masson et Cie, Paris.

Dawes, B. (1946) The Trematoda. Cambridge University Press, Cambridge. Edwards, D. D. and Bush, A. O. (1989) Helminth communities in avocets: Importance of the compound

community. J. Parasitol. 75, 225-38. Glen, D. R. and Brooks, D. R. (1986) Parasitological evidence pertaining to the phylogeny of the hominoid

primates. Biol. J. Linn. Soc. 27, 331-54. Goater, C. P. and Bush, A. O. (1988) Intestinal helminth communities in long-billed curlews: The

importance of congeneric host-specialists. Holarctic Ecol. 11, 140-5. Hoberg, E. P. (1987) Recognition of larvae of the Tetrabothriidae (Eucestoda): Implications for the origin

of tapeworms in marine homeotherms. Canad. J. Zool. 65, 997-1000. Holmes, J. C. and Price, P. W. (1980) Parasite communities: The roles of phylogeny and ecology. Syst.

Zool. 29, 203-13. Holmes, J. C. and Price, P. W. (1986) Communities of parasites. In Community Ecology: Pattern and

Process (D. J. Anderson and J. Kikkawa eds) pp. 187-213. Blackwell Scientific, Oxford. Lawton, J. H. and Price, P. W. (1979) Species richness of parasites on hosts: agromyzid flies on the British

Umbelliferae. J. Anita. Ecol. 48, 619-37. Mettrick, D. F. and Podesta, R. B. (1974) Ecological and physiological aspects of helminth-host interactions

in the mammalian gastrointestinal canal. Adv. Parasitol. 12, 183-278. Moravec, F., Prokopic, J. and Shilikas, A. V. (1987) The biology of nematodes of the family Capillariidae

(Neveu-Lemaire, 1936). Folia Parasitologia 34, 39-56. Petrochenko, V. I. (1971a) Acanthocephala of domestic and wild animals. Vol. I. (Translated from Russian,

Akademiya Nauk SSSR Vsesoyuznoe Obshchestvo Gel'Mintologov; K. I. Skrjabin ed.). Israel Program for Scientific Translations, Jerusalem.

Petrochenko, V. I. (1971b) Acanthocephala of domestic and wild animals. Vol. II. (Translated from Russian, Akademiya Nauk SSSR Vsesoyuznoe Obshchestvo Gel'Mintologov; K. I. Skrjabin ed.). Isreal Program for Scientific Translations, Jerusalem.

Pojmanska, T. (1982) The co-occurrence of three species of Diorchis Clerc 1903 (Cestoda: Hymenolepididae) in the European coot, Fulica atra. Parasitology 84, 419-29.

Price, P. W. (1983) Hypotheses on organization and evolution in herbivorous insect communities. In Variable Plants and Herbivores in Natural and Managed Systems (R. F. Denno and M. S. McClure eds) pp. 559-96. Academic Press, New York.

Rey, J. R., McCoy, E. D. and Strong, D. R. (1981) Herbivore pests, habitat islands, and the species-area relation. Amer. Natur. 117, 611-22.

Rigby, M. D. and Threlfall, W. (1981) Helminth parasites of the muskrat (Ondatra zibethicus (L.)) in Newfoundland. Canad. J. Zool. 59, 2172-6.

Riley, J. and Owen, R. W. (1975) Competition between two closely related Tetrabothrius cestodes of the fulmar ( Fulmarus glacialis L.). Z. Parasitenkunde 46, 221-8.

Root, R. B. (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol. Monogr. 43, 95-124.

Schad, G. A. (1963) Niche diversification in a parasitic species flock. Nature 198, 194-6. Shoop, W. (1988) Trematode transmission patterns. J. Parasitol. 74, 46-59. Shults, L. M. (1986) Helminth parasites of the Steller sea lion, Eumetopiasjubatus, in Alaska. Proc. Helm.

Soc. Wash. 53, 194--7. Sokal, R. R. and Rohlf, F. J. (1981) Biometry. W. H. Freeman and Company, San Francisco. Southwood, T. R. E. (1961) The number of species of insect associated with various trees. J. Anita. Ecol.

30, 1-8. Stock, T. M. and Holmes, J. C. (1987) Host specificity and exchange of intestinal helminths among four

species of grebes (Podicipedidae). Canad. J. Zool. 65, 669-76. Strong, D. R., McCoy, E. D. and Rey, J. R. (1977) Time and the number of herbivore species: The pests

of sugarcane. Ecology 58, 167-75. Stroud, R. K. and Dailey, M. D. (1978) Parasites and associated pathology observed in pinnipeds stranded

along the Oregon coast. J. Wildl. Dis. 14, 292-8. Wardle, R. A. and McLeod, J. A. (1952) The Zoology of Tapeworms. University of Minnesota Press,

Minneapolis. Wazura, K. W., Strong, J. T., Glenn, C. L. and Bush, A. O. (1986) Helminths of the Beluga whale

(Delphinapterus leucas) from the Mackenzie River delta, Northwest Territories. J. Wildl. Dis. 22, 440-2.

Page 10: Ecological versus phylogenetic determinants of helminth parasite community richness

10 Bush, Aho and Kennedy

Wilkinson, L. (1988) SYSTAT: The System for Statistics. Systat, Inc., Evanston, IL. Wilson, E. O. (1969) The species equilibrium. Brookhaven Symp. Biol. 22, 207-64. Yamaguti, S. (1959) Systema Helminthurn. Vol. II. The cestodes of vertebrates. Interscience Publishers

Inc., New York.

Appendix 1. Data

The following are the data on which the paper is based. The form of the list is Host Species, Number of Component Parasite Species, Reference Number. When more than one study of a host species has been used, the species name is not repeated.

Fish

Abramis brama 4 R231; 3 R232; 1 R480; 2 R207; 1 R9; 3 R255; 1 R427; 2 R368; 3 R115; 3 R329. Acipenser baeri 2, 2, :2 R425. A. guldenstadti 3, 2, 3, 4, 4 R425. A. nudiventris 1, 1 R425. A. ruthenus 2, 2, 3, 3, 4 R425. A. stellatus 2, 2, 4, 6 R425. A. transmontanus 1 R307. Agosia chrystogaster 0 R333. Alepocephalus agassizi 5, 8 R512. A. bairdi 3, 7, 8 R512. Alosa brashnikovi 2, 1 R359. A. caspia 0, 0, 0, 0, 1, 1, 2, 2 R359. A. fallax 5 R15. A. kessleri 0, 0, 0, 0, 0, 1, 1, 2, 2, 3, 4 R359. A. saposhnikovi 3 R359. Ambloplitis rupestris 6 R40; 5 R167. Amia calva 4 R39. Ammodytes hexapterus 0 R370. Anarhichas lupus 7 R370. Anchoviella indica 1 R350. Anguilla anguilla 3 R236; 3 R255; 2 R256 and Kennedy, unpub, data; 4, 4, 7 Rl16. Artediellus europeus 1 R370. Barbus barbus 3 R475; 3 R75. Blicca bjoerkna 3 R232; 0 R207. Brachymystax lenck 4 R440. Carpoides carpio 3, 3 R271. C. cyprinus 3 R451. Carassius carrasius 0 R9; 1 R75. Catostomus catostomus 1 R101; 3 R283. C. commersoni 3 R40; 4, 2 R7; 3 R283. C. insignis 2 R333. Chaenicthys rhinocephalus 7 R289. C. velifer 6 R289. Champsocephalus gunnari 4 R289. Chondrosoma polylepis 1 R75. C. nasus 2, 4 R426. Chrosomus eos 0 R40. Cichlosoma urophthalmus 6 Selgado-Maldonado, pers. comm. Clevelandia ios 2 R72. Clupea harengus 5 R17; 0 R370. Coregonus albula 1 R13. C. artedii 3 R40; 2 R486; 2 R283. C. autumnalis 2 R205. C. clupeaformis 3 R40; 6, 6 R18; 2 R101; 4 R486; 3 R283; 1 R217. C. hoyi 4 R40. C. lavaretus 5 R171; 2 R440; 3 R152; 3 R13. C. nasus 4, 4 R45; 5 R270; 2 R476. C. peled 4, 4 R45. C. spp. 5, 5, 7, 8, 1, 1, 4, 8 R45. Cottus cognatus 3, 1 R18. Ctenopharyngodon idella 2 R46. Culaea inconstans 2 R40; 5 R178. Cyclopterus lumpus 2 R370. Cynoscion regalis 2 R314. Cyprinus carpio 1 R152; 4 R328; 2 R75; 3 R100. Damalichthys vacca 0, 0, 0, 1, 2 R332. Dormitator maculatus 0 R39. Dorosoma cepedianum 0 R39; 1 R226. D. petenense 1 R226. Embiotoca lateralis 1, 2, 3, 3 R332. Engraulicypris argenteus 0 R258. Engraulis encrasicholus 6 R350. E. japonicus 3 R350. Enneacanthus gloriosus 0 R38. Eopsetta jordani 0 R199. Erimyzon sucetta 1 R39. Esox lucius 5 R40; 8 R232; 2 R440; 5 R152; 2 R9; 2, 2, 3, 3 R106; 3 R207; 1 R250 and Kennedy, unpub, data; 2 R255; 2 R88; 3 R427; 3 R270; 3 R18; 3 R101; 5 R327; 5 R368; 4 R487; 3 R273; 3 R283; 2 R115; 2 R381. E. niger 3 R39. Etheostoma nigrum 2 R40. E. radiosum 0 R406. Etrumens micropus 1 R350. Eucinostomus gula 0 R39. Fundulus chrysotus 1 R39. F. cingulatus 1 R39. F. majalis 2 R39. F. parvipinnis 1 R510. F. seminolis 2 R39. F. similis 2 R39. Gadus morhua 5 R369; 5 R370; 11 R501; 3 R323; 12 R14; 4 R222; 3, 7, 7 R465. Gambusia affinis 2 R39. Gasterosteus aculeatus 1 R369; 2 R370; 2 R99; 2 R88; 1 R270. Gila robusta 3 R333. Gobio gobio 0 R440; 0 R9; 1 R255; 0 R75; 0 R277. Gymnacanthus tricuspis 1 R370. Gymnocephalus cernua 0 R255; 1 R427; 1 R380; 2 R277. Haplochromis elegans 2 R258. H. nigripinnus 2 R258. H. schubotzi 1 R258. H. squamipinnus 1 R258. H. wingatti 0 R258. H. sp. 1 R258. Heterandia formosa 2 R39. Hiodon tergisus 3 R195. Hippoglossus hippoglossus 4 R370. Hippoglossoides platessoides 7 R370; 0, 4, 5, 5, 5 R513. Hucho taiman 2 R440. Huso huso 0, 2, 2, 5 R425. Hybopsis plumbea 1 R461. Ictalurus melas 5 R210. L natalis 3 R39; 3 R210. I. nebulosus 3 R39; 4 R40. I. punctatus 5 R210; 7 R219; 4 R39; 4 R40. Ictiobus cyprinellus 1 R279. Ilypnus gilberti 2 R72. Jordanella floridae 2

Page 11: Ecological versus phylogenetic determinants of helminth parasite community richness

Helrninth parasite community structure 11

R39. Labidesthes sicculus 2 R39. Lateolabrox ]aponicus 8 R100. Lepisosteus osseus 1 R95. L. platyrhincus 1 R39. L. productus 2 R95. L. spatula 1 R95. Lepomis cyanellus 1 R296; 4 R297. L. gibbosus 3 R40; 1 R167; 0 Rl13. L. gulosus 1 R38; 6 R219; 7 R107. L. humilis 2 R296; 0 R297. L. rnacrochirus 2 R38; 2 R296; 4 R167; 5 R219; 2 R297; 6 R107. L. rnegalotis 2 R38; 1 R296; 3 R297. L. microlophus 3 R38. L. punctatus 3 R38. Leucioperca leucioperca 6 R231, 7 R152; 2 R368. Leuciscus cephalus 3 R249 and Kennedy, unpub, data; 2 R75. L. idus 3 R440. L. leuciscus 1 R440; 1 R255; 5 R249 and Kennedy, unpub, data. Limanda lirnanda 2 R370. Liopsetta putnami 8 R77. Liparis atlanticus 4 R335. Lota Iota 1 R440; 2 R207; 5 R427; 1 R270; 2 R283; 2 R381, 6 R40. Mallotus viUosus 1 R370. Meda fulgida 1 R333. Melanogrammus aeglefinus 5 R411; 4 R370. Menidia beryllina 1 R39. Merluccius albida 3 R413. M. bilinearis 2 R314; 2 R413. M. capensis 1 R466. M. gagi 2 R93. M. productus 2, 4 R405. Micromesistus poutassou 2, 2, 2 R246. Micropterus dolornieui 7 R40; 5 R49; 6 R167. M. punctulatus 4 R49; 5 R219. M. salmoides 2 R38; 3 R167; 5 R219; 4 R107; 4 R48. Microstomus pacificus 2 R216. Morone saxatilis 4 R220. Mugil auratus 4 R369. M. capilo 2 R330. M. cephalus 2 R330. M. sp. 3 R438. Myxocephalus quadricornis 2 R461. M. scorpius 5 R370. Notemigonus crysoleucas 0 R39. Notropis chalybaeus 0 R39. N. emiliae 1 R39. N. heterolepis 1 R40. N. hudsonius 5 R40. N. volucellus 0 R40. Oncorhynchus gorbuscha 4 R338; 5, 4, R62. O. keta 5, 5 R62; 3 R495. O. kisutch 5 R270; 1 R283; 4 R239; 8 R338. O. nerka 3 R270. O. tshawytscha 4 R239; 7 R338. Onus musteltus 4 R443. Oreochromis andersonii I R44. O. macrochir 1 R44. Osmerus mordax 1 R40; 2, 4 R461. Pantosteus clarki 2 R333. Paralichthys dentatus 2 R314. Parasilurus arctus 7 R100. Pelecus cultralis 2 R231. Pellona ditchela 1 R350. Perca flavescens 5 R40. P. fluviatilis 7 R231; 3 R480; 2 R440; 2 R152; 4 R9; 4 R207; 0, 1 R424; 2 R88; 2 R427; 4 R8; 1 R253; 1 R254; 3 R10; 4 R380; 4 R368; 3 Rl15; 6 R410; 3 R277. Percopsis omiscomaycus 4 R40. Pholis gunnellus 2 R370. Phoxinus phoxinus 2 R57; 2 R381. Physis chesteri 1 R413. Pimephales notatus 0 R40. Platichthys ftesus 6 R235; 5 R370; 9 R191; 4 R322. Pleuronectes platessa 4 R370; 9 R292. Poecilia latipinnis 0 R39. Pollachius virens 3 R370; 4 R412. Pomatomus salaltis 2 R314. Pomoxis annularis 4 R219. P. nigromaculatus 5 R38; 3 R219. Prosopium coulteri 0 R340. P. cylindraceum 3 R40; 3 R18; 3 R217. P. williamsoni 2 R340. Pseudopleuronectes americanus 0 R314. Pungitius pungitius 1 R137; 2, 1, 2 R270; 3 R283. Puntius binotatus 2 R282. Quietula y-corda 2 R72. Ra]a batis 5 Williams, H. H., pers. comm. R. clavata 5 Williams, H. H., pers. comm. R. radiata 7 R370; 4 R501. Rhinichthys meleagris 0 R452. R. osculus 1 R274; 2 R333. Rutilus arcasi 1 R75. R. rutilus 1 R480; 0 R440; 6 R152; 1 R9; 2, 3, 4, 4 R106; 1 R207; 1 R249; 0 R250; and Kennedy, unpub, data; 0, 1 R424; 0 R255; 1 R427, 1 R368; 1 R329; 0 R277. Salmo apache 3 R333; 2 R334. S. gairdneri 5 R40; 3 R404. S. gilae 2 R333; 2 R334. S. mykis 6, 7, 6 R270. S. salar 5 R404; 5 R321; 5 R370; 3, 4, 6 R365; 5 R217; 6, 3 R366. S. trutta 3 R394; 4 R456; 3 R370; 8 R375; 3 R404; 6, 4, 4 R106; 5 R88; 6 Kennedy, unpub, data; 1 R254, 4, 6, 4, 4, 4, 7, 6, 4, 4, 4, 4, 6, 3, 5, 5, 5, 7, 5, 6, 6, 6 R4; 6 Rl15; 2 R334; 2 R337. Salvelinus alpinus 7 R153; 1 R375; 6 R217; 3, 4, 5, 6 R270; 5 R83; 4 R84; 2, 2, 2, 1 R251; 1 R252; 4, 8 R148; 5 R303; 4 Rl15; 3 R134. S. fontinalis 1 R40; 7 R217; 5 R404; 3 R101; 3 R337. S. leucomyensis 5, 5, 5, 0 R270; 2 R309. S. malma 5 R84; 3 R309. S. namaycush 3 R40; 8 R217; 4 R101; 7 R18; 2 R283. Sardinapilchardus 6 R350. Sardinella aurita 5 R350. S. eva 0 R350. S. ]ussieu 2 R350. S. longiceps 1 R350 S. rnaculata 2 R350. S. melanura 2 R350. Sardinops ocellata 0 R350. Scardinius erythrophthalmus 0 R250; 1 R329. Scomber scomber 1 R370. Scophthalmus aquosus 2 R314. Sebastes alutus 5 R418. S. fasciatus 3 R64. S. marinus 3 R370; 4 R64. S. menteUa 3 R64. S. paucispinis 2 R242. Semotilus atromaculatus 1 R40. Siluris glanis 5 R152. S. soldatovi 8 R100. Somnicus rnicrocephalus 3 R370. Stizostedion vitreum 4 R40; 3 R283. Synodus foetens 6 R346. S. lucioceps 1 R241. Theragra chalcogramma 5, 5, 5, 5 R16. Thrisocles rnalabaricus 0 R350. Thunnus albaceres 6 R485. ThymaUus arcticus 1 R440; 2, 4, 4 R270; 7 R18. T. thymallus 3 R249 and

Page 12: Ecological versus phylogenetic determinants of helminth parasite community richness

12 Bush, Aho and Kennedy

Kennedy, unpub, data; 2 R475. Tilapia rendalli 1 R44. T. sp. 2 R258. Tinca tinca 0 R75. Trachurus picturatus 5, 7 R186. T. trachurus 2 R466. Urophycis chuss 2 R413. U. tenuis 4 R413. Xiphias gladius 2 R221. Xyrauchen texanus 2 R333. Zoarches viviparus 2 R370; 3 R324.

Aquatic herptiles

Alligator mississippiensis 6 R214. Amphiuma tridactylum 3 R53; 3 R52. Caretta caretta 4 R422. Chelydra serpentina 8 R211; 7 R503; 2 R286; 4 R387. Chrysemys picta 4 R168; 4, 5 R464; 2 R387; 2 R367. Clemmys marmorata 3 R455. Emydoidea blandingii 2 R367. Kinosternon subrubrum 1 R211; 0 R286. Siren lacertina 1 R52. Sternothaerus minor 1 R190. S. odoratus 0 R286; 3 R54. Trachemys scripta 6 R211; 8 R399; 9 R169; 9 R233; 4 R286; 4, 4 R170.

Amphibious herptiles

Acris gyrillus 1 R211. A. crepitans 0 R21. Agkistrodon piscivorous 3 R146; 6 Rl l0 . Ambystoma laterale 1 R109. A. macrodactylum 3 R483. A. maculatum 1 R384; 2 R109. A. opacum 3 R384. A. texanum 0 R379. A. tigrinum 1 R109. Batrachoseps attenuatus 1 R278. Desmognathus fuscus 1 R174; 1 R175; 1 R157; 2 R162; 2 R384. D. monticola 4 R157; 4 R196. D. ochrophaeus 2 R384; 4 R157; 4 R196. D. quadrimaculatus 3 R384; 1 R157; 3 R196. Ensatina escholtzii 1 R278. Eurycea bislineata 2 R384; 1 R174; 0 R175. E. guttolineata 1 R384. E. lucifuga 0 R161. Gyrinophilus porphyriticus 1 R174; 4 R96. Hemidactylium scutatum 1 R109. Hyla crucifer 2 R69; 1 R21. H. regilla 0 R483. H. squirrela 2 R211. H. versicolor 2 R89. Leurognathus marmorata 2 R196. Nerodia erythrogaster 2 R146. N. rhombifera 2 R146. N. sipedon 6 Rl l0 ; 1 R146; 2 R192. N. taxispilota 2 R87; 2 Rl l0 . Notophthalmus viridescens 2, 2, 4, 4 R384; 3 R174; 3 R175; 2, 2 R377. Plethodon cinereus 1 R384; 0 R174; 0 R175; 0 R157; 1 R109. P. dorsalis 1 R161. P. elongatus 1 R348. P. glutinosus 2 R384; 2 R174; 1 R157; 1 R161. P. ]ordani 1, 1 R160. P. larselli 0 R348. P. metcalfi 2 R384. P. richmondi 1 R157. P. vandykei 1 R483. P. vehiculum 1 R348. Pseudacris brimleyi 3 R69. P. triseriata 3 R21. Pseudotriton montanus 1 R96. P. ruber 1 R384; 2 R96. Rana catesbeiana 3 R211; 3, 2 R69; 3 R89; 0 R483; 1, 2, 2, 2 R276; 2 R21. R. clamitans 4 R89; 2 R500. R. pipiens 2 R500; 0 R483. R. pretiosa 2 R470; 2 R483. R. pretiosa • R. sylvatica 2 R483. R. sphenocephala 4 R211; 2 R69. Storeira dekayi 0 R386. Taricha granulosa 1 R490; 3 R278. T. torosa 1 R278.

Terrestrial herptiles

Acanthodactylus erythrurus 0 R395. Agama colonarum 4 R28. Anniella pulchra 2 R453. Anolis carolinensis 0 R211; 1, 0 R420; 1 Rl14. A. cristatellus 3 R2. A. grahami 2 R76. A. lineatopus 3 R76. A. opalinus 1 R76. A. sagrei 2 R76. Bufo americanus 2 R21; 2 R109. B. boreas 0 R490. B. fowleri 5 R89; 2 R69. B. houstonensis 3 R457. B. valliceps 1 R211. Callisaurus draconoides 1 R453. Cnemidophorus murinus 2 R442. C. sexlineatus 2 R159. C. tigris 1 R27; 2 R453; 0 R51; 1 R290. Coleonyx variegatus 1 R453; 1 R51. Crotalus viridis 0, 2, 2 R498. Crotaphytus collaris 1 R294; 3 R360. C. wislizeni 1 R290. Dipsosaurus dorsalis 2 R453. Eumeces gilberti 0 R453. Gerrhonotus multicarinatus 1 R453. Klauberina riversiana 5 R453. Phrynosoma platyrhinos 1 R25; 2 R290. P. solare 2 R51. Psammodromus algirus 1 R395. P. hispanicus 0 R395. Sauromalus obesus 4 R453. Scaphiophus holbrooki 3 R69. Sceloporus graciosus 3 R351; 1 R496; 0 R290. S. magister 1 R453; 2 R351; 0 R51. S. occidentalis 2 R453; 1 R351; 2 R496; 2 R290. S. orcutti 3 R453. S. undulatus 1 R351. ScinceUa lateralis 2 R211. Streptosaurus mearnsi 2 R453. Terrapene carolina 5 R211. Thamnophissirtalis 1 R192; 0 R385; 1, 1 R386. Urea notata 2, 1 R453. Urosaurus graciosus 0 R453. U. ornatus 1 R51. Uta stansburiana 0 R51; 0 R290. Xantusia henshawi I R453. X. vigilis 1 R453.

Page 13: Ecological versus phylogenetic determinants of helminth parasite community richness

Helminth parasite community structure 13

Aquatic birds

Aechmophorus occidentalis 12 R445. Aix sponsa 3 R300; 8 R462. Alca torda 0 R459. Alle aUe 0 R459. Ammospiza maritima 7 R229. Anas acuta 13 R132. A. americana 5 R423. A. clypeata 4 R71. A. crecca 3 R409; 5 R423; 6 R90. A. cyanoptera 7 R499. A. discors 11 R300; 3 R423; 12 R484. A. platyrhynchos 13 R132; 12 R267; 4 R423; 7 R172. A. rubripes 15 R300. Aramus guarauna 4 R120. Aythya affinis 29 R80. A. collaris 8 R342; 6 R300. Bubulcus ibis 1 R497; 1 R449. Ceryle alcyon 2 R68; 3 R414. Dendrocygna autumnalis 1 R189. Eudocimus albus 10 R79. Fratercula arctica 0 R459. Fulica americana 7 R263. F. atra 7 R29. Gallinago gallinago 2 R284. Gallinula chloropus 5 R268. Grus canadensis 2 R181; 4 R180; 0 R230; 1 R187. Khaki Campbell Duck 9 R437. Larus argentatus 6 R74. L. californicus 4 R478. L. canus 10 R33, R34, R35, R36. L. delawarensis 6 R478. L. fuscus 3 R165. L. philadelphia 5 R204. Lophodytes cucullatus 9 R32. Pelecanus occidentalis 8 R130. Phalacrocorax auritus 7 R460. Podiceps grisegena 18 R445. P. nigricollis 18 R445. Porphyrula martinica 2 R268. Puffinus gravis 1 R65. Rallus elegans 3 R43. R. longirostris 4 R43. Somateria mollissima 13 R58. Uria aalge 1 R459. U. lomvia 1 R459.

Terrestrial birds

Agelaius phoeniceus 0 R123; 2 R124; 1 R225. Anthus pratensis 1 R234. Aphelocoma coerulescens I R264. Bonasa umbellus 3 R141. Bubo virginianus 6 R383. Callipepla californicus 1 R272; 1 R98. C. squamata 2 R136. Colinus virginianus 0 R492; 4 R248; 5 R142; 5 R182; 4 R326. Columba fasciata 0 R345. Corvus brachyrhynchos 2 R135; 2 R215; 4 R12; 2 R339. C. cryptoleucus 1 R361. Cyanocitta cristata 1 R67; 4 R125. Geothlypis trichas 1 R494. Lagopus lagopus 0 R22; 3 R505. L. leucrurus 2 R22. L. mutus 4 R22. Meleagris gallopavo 1 R419; 7 R311; 8 R224; 4 R352; 6 R94. Nyctea scandiaca 1 R383. Oreortyx pictus 0 R272. Ortalis vetula 0 R105. Passer domesticus 1 R504. Passerella iliaca 3 R243. Phasianus colchicus 2 R200; 0 R358; 1 R155. Pica pica 4 R468; 4 R481. Pyrrhula pyrrhula 0 R502. Quiscalus quiscula 4 R126; 5 R73; 1 R30. Seiurus noveboracensis 2 R243. Sturnus vulgaris 3 R66; 4 R234; 3 R397; 2 R479; 2 R92; 5 R128. Turdus iliacus 3 R234. T. migratorius 4 R432; 7 R127. T. philomelos 2 R234. T. pilaris 3 R234. Tympanuchus cupido 2 R331. T. pallidicinctus 3 R355. T. phasianellus 4 R331. Tyrannus tyrannus 3 R291. T. verticali 2 R291. Zenaida auriculata 2 Rl17. Z. macroura 0 R42; 2 Rl17; 3 R183.

Aquatic mammals

Castor canadensis 3 R23; 3 R102; 1, 2 R81; 1 R173. Delphinapterus leucas 2 R489. Eumetopias jubatus 6, 7 R429; 6 R448. Globicephala melaena 2 R131. Leptonychotes weddelli 4 R56. Lutra canadensis 2 R316; 5 R176. Marmota monax 3 R177. Mirounga angustirostris 5 R448. Mustela vison 6 R421; 6 R315; 3 R154; 2 R238. Myocastor coypus 5 R26. Ondatra zibethicus 3 R37; 1 R193; 5 R421; 4, 4, 4, 4 R156; 9 R50; 6 R202; 3, 2 R1; 7 R293; 6 R299; 3, 4, 7 R393. Oryzomys palustris 14 R266. Phoca fasciata 3, 4, 5 R430; 5 R373; 2 R374; 5 R431; 4 R144; 5 R145. P. largha 5 R428. P. vitulina 4 R448. Procyon lotor 4 R245; 5, 8, 8, 9, 10, 13, 15 R209; 6 R31; 2 R378; 2, 7 R218; 4 R435; 6 R436. Trichecus manatus 4 R47. Zalophus californianus 3 R448.

Terrestrial mammals

Alces alces 4 R401; 3 R444. Alouatta caraya 1 R372. Alopex lagopus 6 R389. Ammospermophilus leucurus 1 R237; 1 R203. Antilocapra americana 2 R61; 8 R194; 3 R198. Apodemusflavicollis 1 R454. A. sylvaticus 4 R275. Arvicola terrestris 2 R454. Balantiopteryx plicata 0 R85. Bassariscus astutus 2 R356. Blarina brevicauda 5 R318; 6 R506; 4 R227. Bos taurus 0 R509. Canis aureus 4 R400. C. familiarus 4 R305; 3 R304; 3 R20; 6 R285; 3 R281; 5 R400; 1 R458; 5 R l l l ; 1 R347;

Page 14: Ecological versus phylogenetic determinants of helminth parasite community richness

14 Bush, Aho and Kennedy

2 R7. C. latrans 3 R82; 4 R5; 4 R223; 3 Rl12; 3 R184; 6 R403; 8 R354; 4 R417; 7 R357; 3 R474. C. lupus 5 R391; 5 R223; 4, 5, 7 R103; 4 R403. Cervus elaphus 3 R61; 2 R444. C. unicolor 4 R139. Clethrionomys gapperi 3 R261. C. glareolus 3 R454; 2 R212. C. rufocanus 1 R213; 1 R212. C. rutilus 2 R212. Crocidura russula 5 R310. Cynomys ludovicianus 1 R396; 0 R363. Dama dama 3 R140. Dicotyles tajacu 1 R129; 3 R402. Didelphis virginiana 6 R317. Dipodomys deserti 1 R260. D. merriami 0 R260. D. microps 1 R203. D. ordii 1 R203; 0 R362. Eptesicus fuscus 2 R493; 3 R59; 9 R288; 1 R364; 0 R85. Equus asinus 14 R477. E. cabaUus 4 R469. Eutamias amoenus 4 R295. E. minimus 1 R298; 1 R203. Felis catus 8 R86; 3 R305; 5 R304; 4 R20; 4 R285; 5 R281; 1 R458; 1 R320; 4 R376; 4 R7. F. canadensis 4 R434. F. concolor 5 R390. Glaucomys sabrinus 2 R298. Glossophaga soricina 0 R85. Gulo gulo 2 R388; 4 R3. Herpestes auropunctatus 0 R491. Hipposideros caffer 2 R164. Lasionycteris noctivagans 5 R493. Leptonycteris sanborni 0 R85. Lepus americanus 4 R63; 2 R247. L. californicus 1 R70. L. europaeus 2 R439. L. timidus 2 R439; 3 R60. L. townsendii 0 R259. Lynx rufus 3 R398; 8 R316; 5 R446; 7, 8 R488; 6 R463; 3 R306. Macropus agilis 2 R441. M. fuliginosus 4 R55. M. giganteus 7 R55. M. rufus 1 R19. Martes americana 2, 2 R371. M. pennanti 2 R313; 2 R149. Meles meles 2 R244. Mephitis rnephitis 6 R197; 10 R24; 3 R312; 2 R158. Microtus longicaudus 5 R261. M. montanus 2 R261. M. oeconomus 1 R212. M. pennsylvanicus 2, 2 R206; 4 R261. M. nivalis 5 R454. M. agrestris 5 R454; 2 R212. Molossus ater 1 R85. Mus musculus 1 R208; 0, 1 R206; 0 R310; 0 R396. Mustela erminea 6 R238. Myotis grisescens 5 R471; 5 R341. M. californicus 3 R301. M. lucifugus 2 R493; 7 R59; 0 R341; 2 R85. M. thysanodes 0 R85. M. yumaensis 0 R85. Natalus stramineus 0 R85. Neotoma cinerea 3 R319. N. floridana 3 R336. Nycteris gambiensis 2 R164. Ochotona princeps 4 R41; 4 R416; 5 R201; 5 R203. Ochrotomys nuttalli 1 R287. Octodon degus 5 R97. Odocoileus hemionus 2 R61; 6 R508; 1 R242; 0 R450. O. virginianus 0 R61; 1 R151; 2 R179; 1 R450; 1, 4 R382; 3 R121; 5 R140; 1 R482. Onychomys leucogaster 1 R362. Oreamnos americanus 1 R257. Oryctolagus cuniculus 3 R60. Oryzomys couesi 3 R473. O. melanotis 3 R473. Ovis aries 4 R509. O. canadensis 6 R472; 6 R269. Peromyscus leucopus 2 R208; 2 R206; 1 R511. P. maniculatus 2 R407; 1 R511; 1 R203. Pipistrellus subflavus 1 R341. P. hesperus 1 R85. Pitymys subterraneus 6 R454. P. tatricus 5 R454. Pteronotus davyi 0 R85. Rattus norvegicus 2 R208; 5 R91; 2 R206; 1 R408; 5 R143. R. rattus 2 R228; 4 R78. Sciurus carolinensis 1 R208; 1 R349; 6 R138; 4 Rl19. Sigmodon hispidus 3 R228; 6, 10 R265; 5 R415; 2 R108; 3 R325; 4 R396; 4 R308. Sorex cinereus 3 R506. Spermophilus armatus 2 R237. S. beldingi 0 R237. S. franklinii 2 R298. S. lateralis 0 R237. S. richardsonii 1 R298. S. townsendi 1 R237. S. tridecemlineatus 4 R396; 2 R298. S. variegatus 2 R237; 2 R203. Sus scrofa 4 R392; 2 R122. Sylvilagusfloridanus 4 R208; 1 R343; 9 R l l l ; 5 R447; 4 R259. Tamiasciurus hudsonicus 1 R302; 2 R298. Tadarida chaerephon 1 R164. Taxidea taxus 3 R166; 7 R280; 6 R507; 4 R353. Thomomys bulbivorus 4 R188. T. talpoides 4 R467; 3 R203. Trichosurus vulpecula 3 R344. Urocyon cinereoargenteus 4 R316. Ursus americanus 2 R150; 3 R133; 2 R185; 4 Rl18. U. arctos 4 R104. Vulpes vulpes 1 R163; 5 R433; 4 R147. Zapus princeps 1 R262.

Appendix 2. Literature sources

The following references provide the data used in the analyses. Each appears in alphabetical order in the form: Reference number, Author, Year, Journal, Volume, Page. Where there is more than one author, a plus sign (+) appears. Only the first page of the article is given. R1 Abram 1969 Proc. Helm. Soc. Wash. 36, 93. R2 Acholonu 1976 Proc. Helm. Soc. Wash. 43, 106. R3 Addison + 1978 Canad. J. Zool. 56, 2241. R4 Alvarez Pellitero 1979 (PhD Diss.) Univ. Leon, Spain. R5 Ameel 1955 J. Parasitol. 41,325. R6 Amin, 1974 Proc. Helm. Soc. Wash. 41, 81. R7 Amin 1980 Trans Wisconsin Acad. Sci. Arts, Letters 68, 106. R8 Andersen 1978 Z.

Page 15: Ecological versus phylogenetic determinants of helminth parasite community richness

Helminth parasite community structure 15

Parasitenk. 56, 17. R9 Anderson 1971 (PhD Diss.) Univ. London, UK. R10 Andrews 1979 J. Fish Biol. 15, 195. R11 Andrews + 1980 J. Wildl. Dis. 16, 395. R12 Andrews + 1975 Proc. Helm. Soc. Wash. 42, 25. R13 Anikieva + 1983 Leningrad Nauka: Leningradskoi Otdelenie. R14 Appy + 1982 Canad. J. Zool. 60, 1573. R15 Aprahamian 1985 J. Fish Biol. 27, 521. R16 Arthur 1984 Canad. J. Zool. 62, 675. R17 Arthur + 1980 Canad. J. Zool. 58, 521. R18 Arthur + 1976 J. Fish Res. Bd Canad. 33, 2489. R19 Arundel + 1979 Aust. Wild. Res. 6, 361. R20 Ash 1963 J. Parasitol. 48, 63. R21 Ashton + 1978 Proc. Helm. Soc. Wash. 45, 141. R22 Babero 1953a J. Parasitol. 39,538. R23 Babero 1953b J. Parasitol. 39, 674. R24 Babero 1960 J. Parasitol. 46, 26. R25 Babero + 1967 J. Parasitol. 53, 168. R26 Babero + 1961 J. Parasitol. 47, 378. R27 Babero + 1967 Trans Amer. Micro. Soc. 86, 173. R28 Babero + 1962 Trans Amer. Micro. Soc. 81,228. R29 Babicka + 1972 Facul. Scient. Natl. Purk Brun 13, 3. R30 Badley + 1979 Proc. Helm. Soc. Wash. 46, 149. R31 Bafundo + 1980 J. Parasitol. 66, 134. R32 Bain + 1977 Proc. Helm. Soc. Wash. 44, 219. R33 Bakke 1972 Norw. J. Zoot. 20, 165. R34 Bakke 1973 Norw. J. ZooL 21, 1. R35 Bakke 1985 Fauna Norv., Ser A 6, 42. R36 Bakke + 1976 Norw. J. Zool. 24, 7. R37 Ball 1952 J. Parasitol. 38, 83. R38 Bangham 1938 Trans. Amer. Fish Soc. 68,263. R39 Bangham 1941 Proc. Fla. Acad. Sci. 5, 289. R40 Bangham 1955 Amer. Midl Nat. 53, 184. R41 Barrett + 1970 Proc. Helm. Soc. Wash. 37, 179. R42 Barrows + 1977 J. Wildl. Dis. 13, 24. R43 Bates + 1972 Proc. Helm. Soc. Wash. 39, 146. R44 Batra 1984 Zool. J. Linn. Soc. 82, 319. R45 Bauer 1970 Biology of Coregonid Fishes (Lindsey and Woods eds). Univ Manitoba Press, Winnipeg, Canada. R46 Bauer + 1969 Z. Fischerei 17, 1. R47 Beck + 1988 J. Parasitol. 74, 628. R48 Becker + 1978 Arkansas Water Resources Res Center Publ. 54. Fayetteville, AR. R49 Becker + 1966 Trans. Amer. Fish Soc. 95, 23. R50 Beckett + 1967 J. Parasitol. 53, 1169. R51 Benes 1985 SW Natur. 30, 467. R52 Bennett + 1938 Proc. LA Acad. Sci. 4, 243. R53 Bennett + 1937 Proc. Helm. Soc. Wash. 4, 19. R54 Bennett + 1938 Proc. LA Acad. Sci. 4, 241. R55 Beveridge + 1979 Aust. Wild. Res. 6, 69. R56 Beverly-Burton 1971 Canad. J. Zool. 49, 75. R57 Bibby 1972 Z Fish Biol. 4, 289. R58 Bishop + 1974 Proc. Helm. Soc. Wash. 41, 25. R59 Blankespoor + 1970 Proc. Iowa Acad. Sci. 77, 200. R60 Boag + 1986 J. Helminthol. 60, 92. R61 Boddicker + 1969 J. Parasitol. 55, 1067. R62 Bogdanova 1963 Izvestia gosudarstvennogo nauchino-issledovatelskogo instituta ozernogo i rechnogo rybnogo khozyaistva 54, 15. R63 Bookhout 1971 J. Wildl. Dis. 7, 246. R64 Bourgeois + 1984 Canad. J. Zool. 62, 1879. R65 Bourgeois + 1979 Canad. J. Zool. 57, 1355. R66 Boyd 1951 J. Parasitol. 37, 56. R67 Boyd + 1956 J. Parasitol. 42, 332. R68 Boyd + 1971 J. Parasitol. 57, 150. R69 Brandt 1936 Ecol. Monogr. 6, 491. R70 Brittain + 1975 J. Wildl. Dis. 11, 269. R71 Broderson + 1977 J. Wildl. Dis. 13, 435. R72 Brooks + 1974 J. Parasitol. 60, 1062. R73 Buck + 1975 J. Parasitol. 61,380. R74 Buck + 1976 Proc. Helm. Soc. Wash. 43, 233. R75 Bueno 1980 (PhD Diss.) Instituto Nacional de Investigaciones Agrarias, Madrid, Spain. R76 Bundy + 1987 J. Helminthol. 61, 77. R77 Burn 1980 J. Parasitol. 66, 532. R78 Buscher + i971 Proc. Helm. Soc. Wash. 38, 96. R79 Bush + 1976 Proc. Helm. Soc. Wash. 43, 18. R80 Bush + 1986 Canad. J. Zool. 64, 132. R81 Bush + 1981 Proc. Worldwide Furbearer Conf. (Chapman and Pursley eds) pp. 678. Donnelly and Sons Co. Falls Church, VA. R82 Butler + 1954 J. Parasitol. 40, 440. R83 Butorina 1978 Nauchyne Soobshcheniya Instituta Biologii Morya (Biologicheskie issledovaniya dal'nevostochnykh morei) 3, 12. R84 Butorina 1980 Populyat- sionnaya Biologia i Sistematika Lososevykh pp. 65. Nauka, Moscow, USSR. R85 Cain + Proc. Helm. Soc. Wash. 41,113. R86 Calero + 1974 J. Parasitol. 37,326. R87 Camp 1980 Proc. Helm. Soc. Wash. 47, 276. R88 Campbell 1974 Proc. Roy. Soc. Edinburgh B 74, 347. R89 Campbell 1968 VA J. Sci. 19, 13. R90 Canaris + 1981 J. Wildl. Dis. 17, 57. R91 Carlos + 1950 J. Parasitol. 36, 426. R92 Carter + 1973 J. Parasitol. 61, 161. R93 Carvajal + 1979 J. Fish Biol. 15, 671. R94 Castle + 1984 J. Witdl. Dis. 20, 190. R95 Castro + 1967 Proc. Helm. Soc. Wash. 34, 187. R96 Catalano + 1982 Ohio J. Sci. 82, 120. R97 Cattan + 1976 Bol. Chileno Parasit. 31, 16. R98

Page 16: Ecological versus phylogenetic determinants of helminth parasite community richness

16 Bush, Aho and Kennedy

Chandler 1970 Canad. J. Zool. 48, 741. R99 Chappell 1969 J. Fish Biol. 1,339. R100 Chen 1984 Parasitic organisms of freshwater fish of China (Instit Hydrobiol Acad Sinica eds) pp. 41. Agricultural Publ. House, Beijing. R101 Chinniah + 1978 J. Fish Biol. 13, 203. R102 Choquette + 1956 Canad. J. Zool. 34, 209. R103 Choquette + 1973 Canad. J. Zool. 51, 1087. R104 Choquette + 1969 Canad. J. Zool. 47, 167. R105 Christensen + 1977 J. Parasitol. 63, 830. R106 Chubb 1970 Aspects of Fish Parasitology (Taylor and Muller eds) Symp British Soc Parasitol. 8, 119. Biackwell Sci. Publ., Oxford. R107 Cloutman 1975 Trans. Amer. Fish Soc. 104, 277. R108 Coggins + 1975 Proc. OK Acad. Sci. 55, 112. R109 Coggins + 1982 Proc. Helm. Soc. Wash. 49, 99. R l l0 Collins 1969 J Elisha Mitchell Sci. Soc. 85, 141. R l l l Coman + 1972 Aust. VetJ. 48, 456. Rl12 Conder + 1978 J. WildL Dis. 14, 247. Rl13 Cone + 1977 Canad. J. Zool. 55, 1410. Rl14 C o n n + 1984 Proc. Helm. Soc. Wash. 51,367. Rl15 Conneely + 1984 J. Fish Biol. 24,363. Rl16 Conneely + 1986 J. Fish Biol. 28, 207. Rl17 Conti + 1981 J. Wildl. Dis. 17, 529. Rl18 Conti + 1983 Proc. Helm. Soc. Wash. 50, 252. Rl~9 Conti + 1984 J. Parasitol. 70, 143. R120 Conti + 1985 Proc. Helm. Soc. Wash. 52, 140. R121 Cook + 1979 J. Wildl. Dis. 15,405. R122 Coombs + 1974 J. Wildl. Dis. 10, 436. R123 Cooper + 1974a J. Wildl. Dis. 10, 399. R124 Cooper + 1974b J. Parasitol. 60, 962. R125 Cooper + 1974c Canad. J. Zool. 52, 1421. R126 Cooper + 1974d Proc. Helm. Soc. Wash. 41,233. R127 Cooper + 1974e J. Wildl. Dis. 10, 397. R128 Cooper + 1975 J. Parasitol. 61, 161. R129 Corn + 1985 J. Wildl. Dis. 21, 254. R130 Courtney + 1974 Proc. Helm. Soc. Wash. 41, 89. R131 Cowan 1967 J. Parasitol. 53, 166. R132 Crichton + 1972 Canad. J. Zool. 50,633. R133 Crum + 1978 J. Wildl. Dis. 14, 178. R134 Curtis 1985 ICASF Inform Ser, No. 3, p~ 12. Drottingholm, Sweden. R135 Daly 1959 Proc. Helm. Soc. Wash. 26, 66. R136 Dancak + 1982 Proc. Helm. Soc. Wash. 49, 144. R137 Dartnall 1973 J. Fish Biol. 5, 505. R138 Davidson 1976 Proc. Helm. Soc. Wash. 43, 211. R139 Davidson + 1987 J. Wildl. Dis. 23, 267. R140 Davidson + 1985 J. Wildl. Dis. 21, 153. R141 Davidson + 1977 Proc. Helm. Soc. Wash. 44, 157. R142 Davidson + 1980 J. Wildl. Dis. 16,367. R143 de Leon 1964 J. Parasitol. 50, 478. R144 Delyamure + 1974 Parazity morskikh zhivotnykh 88, 27. R145 Delyamure + 1976 Parazitologiya 10, 325. R146 Detterline + 1984 Trans. Amer. Micro. Soc. 103, 137. R147 Dibble + 1983 J. Parasitol. 69, 1170. R148 Dick + 1981 J. Fish Biol. 18, 339. R149 Dick + 1979 J. Wildl. Dis. 15,409. R150 Dies 1979 J. Wildl. Dis. 15, 49. R151 Dinaburg 1939 Proc. Helm. Soc. Wash. 6, 102. R152 Dogiel 1961 Parasitology of Fishes (Dogiel, Petrushevskii and Polyanski eds). Oliver and Boyd, Edinburgh and London. R153 Dogiel + 1937 Trudy Leningradskogo Obshestva Estestvozhsrytatelen 66,434. R154 Dorney + 1969 Bull. Wildl. Dis. Assoc. 5, 35. R155 Dowell + 1983 J. Wildl. Dis. 19, 152. R156 Dunagan 1957 Trans. Amer. Micro. Soc. 76, 318. R157 Dunbar + 1979 J. TN Acad. Sci. 54, 106. R158 Dyer 1970 Proc. Helm. Soc. Wash. 37, 92. R159 Dyer 1971 Proc. Helm. Soc. Wash. 38, 256. R160 Dyer 1983 Proc. Helm. Soc. Wash. 50, 257. R161 Dyer + 1973 Trans. IL Acad. Sci. 66, 23. R162 Dyer 4- 1980 Proc. Helm. Soc. Wash. 47, 95. R163 Dyer + 1981 IL State Acad. Sci. 74, 137. R164 Edungbola 1981 J. Parasitol. 67, 287. R165 Ellis + 1973 J. Helminthol. 47, 329. R166 Erickson 1946 Amer. Midl. Natur. 36, 494. R167 Esch 1971 Amer. Midl. Natur. 86, 160. R168 Esch + 1967 J. Parasitol. 53, 818. R169 Esch + 1979 J. Parasitol. 65, 624. R170 Everhart 1958 Proc. OK Acad. Sci. 38, 38. R171 Fagerholm + 1980 Bothnian Bay Report 2, 67. R172 Farias + 1986 J. Wildl. Dis. 22, 51. R173 Fedynich + 1986 J. Wildl. Dis. 22, 579. R174 Fischthai 1955a Amer. Midl. Natur. 53, 176. R175 Fischthal 1955b Proc. Helm. Soc. Wash. 22, 46. R176 Fleming + 1977 Proc. Helm. Soc. Wash. 44, 131. R177 Fleming + 1979 Proc. Helm. Soc. Wash. 46, 115. R178 Font 1983 Canad. J. Zool. 61, 2129. R179 Foreyt + 1979 Proc. First Welder Wildlife Foundation Syrup (Drawe ed.) pp. 105. Welder Wildlife Contribution B-7. R180 Forrester + 1975 J. Parasitol. 61,547. RI81 Forrester + 1974 Proc. Helm. Soc. Wash. 41, 55. R182 Forrester + 1984 Proc. Helm. Soc. Wash. 51,255. R183 Forrester + 1983 Proc. Helm. Soc. Wash. 50,

Page 17: Ecological versus phylogenetic determinants of helminth parasite community richness

Helminth parasite community structure 17

143. R184 Franson + 1978 J. Parasitol. 64, 303. R185 Frechette + 1977 I. Wildl. Dis. 13, 432. R186 Gaevskaya + 1985 Ekologia Morya 20, 80. R187 Gaines + 1984 J. Wildl. Dis. 20, 207. R188 Gardner 1985 Canad. J. Zool. 63, 1463. R189 George + 1975 J. Wildl. Dis. 11, 17. R190 Gibbons + 1970 J. Herp. 4, 79. R191 Gibson 1972 J. Fish Biol. 4, 1. R192 Gibson + 1973 Amer. Midl. Natur. 89,239. R193 Gilford 1954 J. Parasitol. 40,702. R194 Gilmore + 1960 Proc. Helm. Soc. Wash. 27, 69. R195 Glenn 1980 Canad. J. Zool. 58,252. R196 Goater + 1987 Amer. Midl. Natur. 118,289. R197 Goldberg 1954 Proc. Helm. Soc. Wash. 21, 29. R198 Goidsby + 1954 J. Parasitol. 40, 637. R199 Gregoire + 1952 J. Parasitol. 38, 84. R200 Greiner 1972 J. Wildl. Dis. 8, 203. R201 Grundmann + 1976 Proc. Helm. Soc. Wash. 43, 39. R202 Grundmann + 1967 Trans. Amer. Micro. Soc. 86, 139. R203 Grundmann + 1976 Amer. Midl. Natur. 95, 347. R204 Hair + 1970 Canad. J. Zool. 48, 1129. R205 Haldorson 1984 Proc. Helm. Soc. Wash. 51,245. R206 Hall + 1955 J. Parasitol. 41, 640. R207 Haivorsen 1971 Norw. J. Zool. 19, 181. R208 Harkema 1936 Ecol. Monogr. 6, 151. R209 Harkema + 1964 J. Parasitol. 50, 60. R210 Harms 1960 J. Parasitol. 46, 695. R211 Harwood 1932 Proc. US Natl. Mus. 81, 1. R212 Haukisalmi 1986 Annals Zool. Fenn. 23, 141. R213 Haukisalmi + 1987 J. Wildl. Dis. 23, 233. R214 Hazen + 1978 J. Wildl. Dis. 14, 435. R215 Hendricks + 1969 Proc. Helm. Soc. Wash. 36, 150. R216 Hendrickson + 1987 Proc. Helm. Soc. Wash. 54, 111. R217 Hicks + 1973 J. Fish Biol. 5,399. R218 Hoberg + 1982 Canad. J. Zool. 60, 53. R219 Hoffman + 1974 Arkansas Water Resources Res Center Publ., Fayetteville, AR. R220 Hogans 1984 J. Wildl. Dis. 20, 61. R221 Hogans + 1983 J. Parasitol. 69, 1178. R222 Hoglund + 1985 Abstracts Fifth Int. Conf. Wildl. Dis. Uppsala, Sweden, R223 Holmes + 1968 Canad. J. Zool. 46, 1193. R224 Hon + 1975 Proc. Helm. Soc. Wash. 42, 119. R225 Hood + 1980 Canad. J. Zool. 58, 528. R226 Hopkins 1966 J. Parasitol. 52, 843. R227 Huffman + 1981 Proc. Helm. Soc. Wash. 48, 209. R228 Hugghins 1951 Amer. Midl. Natur. 46, 230. R229 Hunter + 1953 Amer. Midl. Natur. 50, 407. R230 Iverson + 1983 J. Wildl. Dis. 19, 56. R231 Izyumova 1958 Trudy Biologicheskoi 'Borok' 3, 384. R232 Izyumova 1960 Trudy Instituta Biologii Bodochranilishch 3, 283. R233 Jacobson 1986 (MS thesis) Wake Forest Univ, USA. R234 James + 1967 J. Helminthol. 41, 19. R235 Janiszewska 1939 Mere de l'Acad Pollon Sci et Lettres. Ser. B 14 (1938), 1. R236 Jeacock 1969 Parasitology 59, 16P. R237 Jenkins + 1973 Proc. Helm. Soc. Wash. 40, 76. R238 Jennings + 1982 Canad. J. Zool. 60, 180. R239 Jennings + 1982 Proc. Helm. Soc. Wash. 49, 279. R240 Jensen + 1982 Proc. Helm. Soc. Wash. 49, 314. R241 Jensen + 1979 Proc. Helm. Soc. Wash. 46, 281. R242 Jensen + 1982 Proc. Helm. Soc. Wash. 49, 317. R243 Jewer + 1978 Proc. Helm. Soc. Wash. 45,270. R244 Jones + 1980 Mammal Rev. 10, 163. R245 Jordan + 1959 J. Parasitol. 45, 249. R246 Karasev 1984 Ecological and Parasitological Investigations of Northern Seas pp. 82. Apatity, Izvestiya Kola Branch AN USSR. R247 Keith + 1986 J. Wildl. Dis. 22, 349. R248 Kellogg + 1968 I. Wildl Manage. 32, 468. R249 Kennedy 1972 Essays in Hydrobiology (Clark and Wootton eds) pp. 53. Univ. Exeter Press, Exeter, UK. R250 Kennedy 1975 Field Studies 4, 177. R251 Kennedy i977 Astarte 111, 49. R252 Kennedy 1978 J. Fish Biol. 13, 457. R253 Kennedy 1985 Ecology and Genetics of Host-Parasite Interactions (Rollinson and Anderson eds) p. 1. Linn. Soc. Symp. Ser. 11. Academic Press, London. R254 Kennedy + 1978 Field Studies 4,617. R255 Kennedy + 1974 Suffolk Natur. Hist. 17, 49. R256 Kennedy + 1987 Parasitology 95, 301. R257 Kerr + 1966 J. Wildl. Manage. 311, 786. R258 Khalil + 1973 Rev. Zool. Botan Africaines 87, 209. R259 Kietzmann + 1986 J. Wildl. Dis. 22, 276. R260 King + 1974 Proc. Helm. Soc. Wash. 41,241. R261 Kinsella 1967 Canad. J. Zool 45,269. R262 Kinsella 1968 J. Parasitol. 54, 309. R263 Kinsella 1973 Proc. Helm. Soc. Wash. 411, 240. R264 Kinsella 1974a Proc. Helm. Soc. Wash. 41, 127. R265 Kinsella 1974b Amer. Mus. Nov. 2540, 1. R266 Kinsella 1988 Proc. Helm. Soc. Wash. 55, 275. R267 Kinsella + 1972 Proc. Helm. Soc. Wash. 39, 173. R268 Kinsella + 1973 Amer. Midl. Natur. 89, 467. R269 Kistner + 1977 J. Wildl. Dis. 13, 125. R270 Konovalov 1975 Univ. Washington Publ.

Page 18: Ecological versus phylogenetic determinants of helminth parasite community richness

18 Bush, Aho and Kennedy

in Fisheries, New Series VI. Seattle, Washington. R271 Kritsky + 1972 J. Parasitol. 58, 723. R272 Krogsdale 1950 Trans. Amer. Micro. Soc. 69, 398. R273 Kuperman 1981 Tapeworms of the genus Triaenophorus, Parasites of Fishes. Amerind Publ. Co. Pvt Ltd, New Delhi. R274 Lang + 1976 J. Parasitol. 62, 93. R275 Langley + 1982 J. Zool. London 198, 249. R276 Lank 1971 IN Acad. Sci. 81,359. R277 Lee 1977 London Natur. 56, 57. R278 Lehmann 1956 J. Parasitol. 40, 231. R279 Leiby + 1972 J. Parasitol. 58, 447. R280 Leiby + 1971 Proc. Helm. Soc. Wash. 38, 225. R281 Lengy + 1969 J. Parasitol. 55, 1239. R282 Leong 1986 J. Fish Biol. 28, 9. R283 Leong + 1981 J. Fish Biol. 18,693. R284 Leyva + 1980 J. Wildl. Dis. 16, 549. R285 Lillis 1967 J. Parasitol. 53, 1082. R286 Limsuwan + 1978 J. TNAcad. Sci. 53, 111. R287 Linzey 1968 Amer. MidL Natur. 79, 320. R288 Lotz + 1985 Canad. J. Zool. 63, 2969. R289 Lyadov + 1981 Zoologicheskii Zhurnat 60, 142. R290 Lyon 1986 Proc. Helm. Soc. Wash. 53, 291. R291 MacKenzie + 1979 Canad. J. Zool. 57, 1143. R292 MacKenzie + 1970 Aspects of Fish Parasitology. (Taylor and Muller eds) Symp British Soc. Parasitol. 8, 1. Blackwell Sci. Pubi., Oxford. R293 MacKinnon + 1978 Canad. J. Zool. 56, 350. R294 McAIlister + 1985 SW Natur. 30, 363. R295 McBee + 1973 J. Parasitol. 59, 322. R296 McDaniei 1963 Trans. Amer. Micro. Soc. 82, 423. R297 McDaniel + 1974 SW Natur. 18, 403. R298 McGee 1980 Canad. J. Zool. 58, 2040. R299 McKenzie + 1979 Canad. J. Zool. 57, 640. R300 McLaughlin + 1979 Canad. J. Zool. 57, 801. R301 Macy 1947 Amer. Midl. Natur. 37, 375. R302 Mahrt + 1972 J. Parasitol. 58, 639. R303 Makhovenko 1972 Parazitologiaya 6, 369. R304 Mann 1955 J. Parasitol. 41,637. R305 Mann + 1952 J. Parasitol. 38,496. R306 Marchiondo + 1986 Proc. Helm. Soc. Wash. 53, 113. R307 Margolis + 1986 J. Parasitol. 72, 794. R308 Martin + 1980 Proc. Helm. Soc. Wash. 47, 247. R309 Martyanova-Glebova 1962 Trudy Germintologicheskoi Laboratorii 12, 52. R310 Mas-Comas + 1977 Vie et Milieu 27,231. R311 Maxfield + 1963 J. Wildl. Manage. 27, 261. R312 Mead 1963 Amer. Midl. Natur. 70, 164. R313 Meyer + 1951 J. Parasitol. 37,320. R314 Meyers 1978 Proc. Helm. Soc. Wash. 45, 120. R315 Miller + 1964 J. Parasitol. 50, 717. R316 Miller + 1968 Proc. Helm. Soc. Wash. 35, 118. R317 Miller + 1970 Proc. Helm. Soc. Wash. 37, 36. R318 Miller + 1974 J. Parasitol. 60, 523. R319 Miller + 1982 Proc. Helm. Soc. Wash. 49, 109. R320 Mirzayans 1971 J. Parasitol. 57, 1296. R321 Mitenev 1984 Ecological and Parasitological Investigations of Northern Seas pp. 88. Apatity, Izvestiya Kola Branch AN, USSR. R322 Moiler 1974 Ber Deutsch Wissenschaftlichen Komm Meeresforschung 23, 136. R323 Moiler 1975a Ber Deutsch Wissenschaftlichen Komm Meeresforschung 24, 63. R324 Moiler 1975b Ber Deutsch Wissenschaftlichen Komm Meeresforschung 24, 71. R325 Mollhagan 1978 SW Natur. 23, 401. R326 Moore + 1986 J. Wildl. Dis. 22, 497. R327 Moravec 1979 Vest. Cesk. Spol. Zool. 43, 174. R328 Moravec 1984 Vest. Cesk. Spol. Zool. 48,261. R329 Moravec 1986 Vest. Cesk. Spol. Zool. 50, 49. R330 Moravec + 1975 Folia Parasitol. 22, 279. R331 Morgan + 1941 J. Wildl. Manage. 5, 194. R332 Moser + 1982 J. Parasitol. 68,733. R333 Mpoame + 1983 SW Natur. 28, 399. R334 Mpoame + 1984 SW Natur. 29, 505. R335 Munson 1974 J. Wildl. Dis. 10, 256. R336 Murphy 1952 Amer. Midl. Natur. 48, 204. R337 Muzzall 1986 Canad. J. Zool. 64, 1549. R338 Muzzall + 1986 Canad. J. Zool. 64, 508. R339 Naderman + 1980 Proc. Helm. Soc. Wash. 47, 100. R340 Newell + 1969 Proc. Helm. Soc. Wash. 36, 274. R341 Nickel + 1967 Amer. Midt. Natur. 78, 481. R342 Noseworthy + 1978 J. Parasitol. 64, 365. R343 Novlesky + 1970 Amer. Midl. Natur. 84, 267. R344 O'Callaghan + 1986 Proc. Helm. Soc. Wash. 22, 589. R345 Olsen + 1980 J. Wildl. Dis. 16, 65. R346 Overstreet 1968 Bull. Mar. Sci. 18, 444. R347 Palmieri + 1978 J. Parasitol. 64, 1149. R348 Panitz 1969 Canad. J. Zool. 47, 157. R349 Parker 1968 J. Parasitol. 54, 633. R350 Parukhin 1975 Trudy Biologo-pochvennogo Instituta, Novaya Seriya 26, 143. R351 Pearce + 1973 Great Basin Natur. 33, 1. R352 Pence + 1977 Proc. Helm. Soc. Wash. 44, 104. R353 Pence + 1979a Proc. Helm. Soc. Wash. 46, 245. R354 Pence + 1979b Intl. J. Parasitol. 9, 339. R355 Pence + 1983 Proc. Helm. Soc. Wash. 50, 345. R356 Pence + 1978 J. Parasitol. 64, 568. R357

Page 19: Ecological versus phylogenetic determinants of helminth parasite community richness

Helminth parasite community structure 19

Pence + 1984 J. Parasitol. 70, 735. R358 Pence + 1980 Proc. Helm. Soc. Wash. 47, 144. R359 Petrushevski 1957 Izvestiya vsesoyuznogo nauchno-issledovatel'skogo instituta ozernogo i rechnogo rybnogo khozyaistva 42, 299. R360 Pfaffenberger + 1986 J. Parasitol. 72, 803. R361 Pfaffenberger + 1981 J. Wildl. Dis. 17, 563. R362 Pfaffenberger + 1985 J. Parasitol. 71, 592. R363 Pfaffenberger + 1984 Proc. Helm. Soc. Wash. 51,241. R364 Phillips 1966 Amer. Midl. Natur. 75, 168. R365 Pippy 1969 Fish Res. Bd Canada Techn. Rep. 134, 1. R366 Pippy 1980 Rapp Process Verb Reunions Cons Internat l'Exploration de la Mer 176, 76. R367 Platt 1977 Ohio J. Sci. 77, 97. R368 Pojmanska + 1980 Acta Parasitol. Polon 27, 319. R369 Polyanski 1961 Parasitology of Fishes (Dogiel, Petrushevskii, and Polyanski eds) pp. 48. Oliver and Boyd, London. R370 Polyanski 1966 Trudy Zoologicheskogo lnstituta Akademii Nauk SSSR 19. IPST, Jerusalem. R371 Poole + 1983 J. Wildl. Dis. 19, 10. R372 Pope 1966 J. Parasitol. 52, 166. R373 Popov 1975 Parazitologiya 9, 31. R374 Popov 1976 Nauchnye Doklady Vysshei Shkoly, Biologicheskie Nauki 1, 49. R375 Powell 1966 (PhD Diss.) Univ. Liverpool, UK. R376 Power 1971 J. Parasitol. 57, 610. R377 Price + 1982 Proc. Helm. Soc. Wash. 49, 285. R378 Price + 1983 Proc. Helm. Soc. Wash. 50, 343. R379 Price + 1980 Proc. Helm. Soc. Wash. 47,273. R380 Priemer 1979 Zool. Anz. 203, 241. R381 Pugachev 1984 Leningrad. Izd. Zoologicheskii Instityt A N SSSR. R382 Pursglove 1977 Proc. Helm. Soc. Wash. 44, 107. R383 Ramalingam + 1978 Canad. J. Zool. 56, 2454. R384 Rankin 1937 Ecol. Monogr. 7, 170. R385 Rau + 1978 Canad. J. Zool. 56, 1765. R386 Rau + 1980 Canad. J. Zool. 58, 929. R387 Rausch 1947 Amer. Midl. Natur. 38, 434. R388 Rausch 1959 J. Parasitol. 45, 465. R389 Rausch + 1983 Canad. J. Zool. 61, 1847. R390 Rausch + 1983 J. Wildl. Dis. 19, 14. R391 Rausch + 1959 J. Parasitol. 45,395. R392 Riddle + 1972 Proc. Helm. Soc. Wash. 39, 55. R393 Rigby + 1981 Canad. J. Zool. 59, 2172. R394 Robertson 1953 Rep. Brown Trout Res. Lab., Scottish Home Dept. Unpubl. report. R395 Roca + 1986 Bol. R. Soc. Espanola Hist. Nat. 81, 69. R396 Rodenberg + 1978 Occasional Papers, The Museum, Texas Tech. Univ. 56, 1. R397 Rodrick + 1971 Trans. Amer. Micro. Soc. 90,253. R398 Rollings 1945 J. Wildl. Manage. 9, 131. R399 Rosen + 1978 J. Parasitol. 64, 1148. R400 Sadighian 1969 J. Parasitol. 55,372. R401 Samuel + 1976 Canad. J. Zool. 54, 307. R402 Samuel + 1970 J. Wildl. Dis. 6, 16. R403 Samuel + 1978 Canad. J. Zool. 56, 2614. R404 Sandeman + 1967 J. Fish. Res. Bd Canad. 24, 1935. R405 Sankurathri + 1983 Syesis 16, 5. R406 Scalet 1971 J. Parasitol. 57, 900. R407 Schad 1956 Canad. J. Zool. 34, 208. R408 Schiller 1952 J. Mammal 33, 38. R409 Schiller 1953 Proc. Helm. Soc. Wash. 20, 7. R410 Scholtz 1986 Vest. Cesk. Spol. Zool. 50, 300. R411 Scott 1981 Canad. J. Zool. 59, 2244. R412 Scott 1985 Canad. J. Zool. 63, 1695. R413 Scott 1987 Canad. J. Zool. 65, 304. R414 Scott 1984 Canad. J. Zool. 62, 2679. R415 Seidenberg + 1974 Amer. Midl. Natur. 92, 320. R416 Seesee 1973 Amer. Midl. Natur. 89,257. R417 Seesee + 1983 J. Wildl. Dis. 19, 54. R418 Sekerak + 1973 Canad. J. Zool. 51, 475. R419 Self + 1950 J. Parasitol. 36, 502. R420 Sellers 1971 J. Parasitol. 57, 355. R421 Senger + 1955 J. Parasitol. 41,637. R422 Sey 1977 Acta Zool. Acad. Sci. Hungary 23,387. R423 Shaw + 1980 J. Wildl. Dis. 16, 59. R424 Shiilcock 1972 (PhD Diss.) Univ. London, UK. R425 Shulman 1954 Trudy Leningradskogo obshestva estestvoispytatelei 72, 190. R426 Shulman + 1980 Parazitologicheskii Sbornik 29, 35. R427 Shulman + 1974 Leningrad Nauka Leningradskoi Otdelenie. R428 Shults 1982 J. Wildl. Dis. 18, 59. R429 Shults 1986 Proc. Helm. Soc. Wash. 53, 194. R430 Shults + 1988 Proc. Helm. Soc. Wash. 55, 68. R431 Shustov 1965 Izvestiya TINRO 59, 193. R432 Slater 1967 Amer. Midl. Natur. 71, 190. R433 Smith 1978 J. Wildl. Dis. 14, 366. R434 Smith + 1986 Canad. J. Zool. 64, 358. R435 Smith + 1985 J. Parasitol. 71,599. R436 Snyder + 1985 J. Parasitol. 71,274. R437 Soliman 1955 J. Helminthol. 29, 17. R438 Solonchenko + 1985 Ecologia Morya 20, 38. R439 Soveri + 1983 J. Wildl. Dis. 19, 337. R440 Spasskii + 1960 Voprosy Iktiologii 15, 183. R441 Speare + 1983 Aust. Wild. Res. 10, 89. R442 Specian + 1980 Proc. Helm. Soc. Wash. 47, 275. R443 Srivastava 1966 Ann. Mag. Natl. Hist., Ser 13, 9, 469.

Page 20: Ecological versus phylogenetic determinants of helminth parasite community richness

20 Bush, Aho and Kennedy

R444 Stock + 1983 Proc. Helm. Soc. Wash. 50, 246. R445 Stock + 1987 Canad. J. Zool. 65, 669. R446 Stone + 1978 J. Parasitol. 64,295. R447 Strohlein + 1983 J. Wildl. Dis. 19, 20. R448 Stroud + 1978 J. Wildl. Dis. 14, 292. R449 Stuart + 1972 J. Parasitol. 58,518. R450 Stubblefieid + 1987 J. Wildl. Dis. 23, 113. R451 Szalai + 1987 J. Parasitol. 73, 446. R452 Tarter 1969 Trans. Amer. Micro Soc. 88, 425. R453 Telford 1970 Amer. Midl. Natur. 83, 516. R454 Tenora 1967 Acta Sci. Natl. Acad. Sci. Bohem. Brno 1,161. R455 Thatcher 1954 J. Parasitol. 40, 481. R456 Thomas 1964 J. Anita. Ecol. 33, 83. R457 Thomas + 1984 J. Parasitol. 70, 1012. R458 Threlfall 1969 Canad. J. Zool. 47, 197. R459 Threlfall 1971 Canad. J. Zool. 49,461. R460 Threlfall 1982 Proc. Helm. Soc. Wash. 41, 89. R461 Threlfail + 1971 J. Parasitol. 57,684. R462 Thul + 1985 Proc. Helm. Soc. Wash. 52, 297. R463 Tiekotter 1985 J. Parasitol. 71,227. R464 Timmers + 1979 Canad. J. Zool. 57, 1046. R465 Timofeeva + 1984 Ecological and Parasitological Investigations on Northern Seas pp. 62. Apatity, Izvestiya Kola Branch AN USSR. R466 Tkachuk 1985 Ecologia Morya 20, 31. R467 Todd + 1971 J. Wildl. Dis. 7, 100. R468 Todd + 1967 J. Parasitol. 53, 364. R469 Torbert + 1986 J. Parasitol. 72, 926. R470 Turner 1959 J. Parasitol. 44, 182. R471 Ubelaker 1966 Amer. Midl. Natur. 75, 199. R472 Uhazy + 1971 Canad. J. Zool. 49, 507. R473 Underwood + 1986 SW Natur. 31,410. R474 Van Den Bussche + 1987 J. Parasitol. 73, 327. R475 Van Maren 1979 Bull. Zool. Mus. Univ. Amsterdam 6, 189. R476 Vaitonen + 1980 Bothnian Bay Reports 2, 17. R477 Vercruysse + 1986 Z. Parasitenk. 72, 821. R478 Vermeer 1969 Canad. J. Zool. 47, 267. R479 Vincent 1972 J. Parasitol. 58, 1020. R480 Vojtkova 1959 Publ. Fac. Sci. Univ. Brno, Czech 401, 97. R481 Wacha + 1971 Proc. Helm. Soc. Wash. 38,268. R482 Waid + 1985 J. Wildl. Dis. 21,264. R483 Waitz 1962 J. Parasitol. 47, 1989. R484 Wallace + 1986 Canad. J. Zool. 64, 1765. R485 Ward 1962 J. Parasitol. 48, 155. R486 Watson + 1979 J. Fish Biol. 15, 579. R487 Watson + 1980 J. Fish Biol. 17, 255. R488 Watson + 1981 J. Wildl. Dis. 17, 547. R489 Wazura + 1986 J. Wildl. Dis. 22, 440. R490 Weatherly + 1962 J. Parasitol. 47, 230. R491 Webb 1980 J. Parasitol. 66, 176. R492 Webster 1951 J. Parasitol. 37, 322. R493 Webster + 1973 Canad. J. Zool. 51,633. R494 Wells + 1960 J. Parasitol. 46, 623. R495 Whitaker 1985 Canad. J. Zool. 63, 2875. R496 White + 1979 Proc. Helm. Soc. Wash. 46, 270. R497 Whittaker + 1971 Proc. Helm. Soc. Wash. 38, 262. R498 Widmer 1967 J. Parasitol. 53, 362. R499 Wilkinson + 1977 J. Wildl. Dis. 13, 62. R500 Williams + 1980 Proc. Helm. Soc. Wash. 47, 278. R501 Williams + 1970 Aspects of Fish Parasitology. (Taylor and Muller eds). Symp. British Soc. Parasitol. 8, 43. Blackwell Sci. Publ., Oxford. R502 Williams + 1969 Proc. Helm. Soc. Wash. 36, 76. R503 Williams 1953 Trans. Amer. Micro. Soc. 72, 175. R504 Wilson 1956 J. Parasitol. 42, 41. R505 Wissler + 1977 J. Wildl. Dis. 13,409. R506 Wittrock + 1979 J. Parasitol. 65, 985. R507 Wittrock + 1974 IA State J. Res. 48, 319. R508 Worley + 1972 Proc. Helm. Soc. Wash. 39, 135. R509 Wright + 1972 J. Parasitol. 58,959. R510 Yoshino 1972 J. Parasitol. 58,635. R511 Zenchak + 1971 J. Parasitol. 57,542. R512 Zubchenko 1984 Eco-parasitological Investigations on Northern Seas pp. 77. Apatity, USSR. R513 Zubchenko 1985 J. NW Atlantic Fish Sci. 6, 165.