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Flea (Siphonaptera) species richness in the Great Basin Desert and island biogeography theory Robert L. Bossard Westminster College, Salt Lake City, UT 84105, U.S.A., [email protected] Received 12 December 2014; Accepted 11 February 2014 ABSTRACT: Numbers of flea (Siphonaptera) species (flea species richness) on individual mammals should be higher on large mammals, mammals with dense populations, and mammals with large geographic ranges, if mammals are islands for fleas. I tested the first two predictions with regressions of H. J. Egoscue’s trapping data on flea species richness collected from individual mammals against mammal size and population density from the literature. Mammal size and population density did not correlate with flea species richness. Mammal geographic range did, in earlier studies. The intermediate-sized (31 g), moderately dense (0.004 individuals/m2) Peromyscus truei (Shufeldt) had the highest richness with eight flea species on one individual. Overall, island biogeography theory does not describe the distribution of flea species on mammals in the Great Basin Desert, based on H. J. Egoscue’s collections. Alternatively, epidemiological or metapopulation theories may explain flea species richness. Journal of Vector Ecology 39 (1): 164-167. 2014. Keyword Index: host size, host density, host range, fleas, species richness, island biogeography theory.
INTRODUCTION Island biogeography theory is a simple, influential model of species richness reflecting an equilibrium between species immigration and extinction. The theory predicts that species richness will be less on small or distant islands (MacArthur and Wilson 1967, Brown and Lomolino 1989, Wilkinson 1993). Islands are depauperate of fleas (Siphonaptera) (Bengtson et al. 1986, Durden 1995, Wilson and Durden 2003, Sánchez et al. 2013), but Scharf (1991) found no effect in Lake Michigan of island size or distance on species richness of fleas. An interesting extension of the original island biogeography theory is to assume that, like geological islands, hosts themselves are islands for parasites. Island size and distance are a function of the “host size, host population size, or magnitude of host geographic range” (Price 1980)(Kuris et al. 1980, Tallamy 1983, Holmes and Price 1986, Esch et al. 1990, Morand and Poulin 1998, Combes 2000, Luque et al. 2004, Poulin 2004, Zander 2005, Reperant 2010). Results of testing island biogeography theory with parasites have been mixed (Choe and Kim 1987, Ròzsa 1993, Poulin 1997, 2007). For example, species richness of ectoparasitic mites on some rodents is correlated with host range (Dritschilo et al. 1975, O’Connor et al. 1977), and parasite species richness of fissiped carnivores is correlated with host body mass, host population density, and host geographic range (Lindenfors et al. 2007). However, parasite species richness of freshwater fish is not correlated with host range (Guegan and Kennedy 1993), for shrews is not correlated with population density (Laakkonen et al. 2003), and for bats is not correlated with host body size, but is with population density. Poulin (2007) wrote that with “every positive relationship between a host trait and parasite species richness currently published, one can find a negative relationship and some nonsignificant relationships.” Remarkably, Kamiya et al. (2014)
claimed that all three variables were “universal predictors of parasite richness across host species, namely host body size, geographical range size and population density, applicable regardless of the taxa considered.” For fleas, “hosts can be considered as biological islands... and so the parasite communities should conform to principles of classical insular biogeography” (Krasnov et al. 1997). Because mammals are small patches of favorable habitat for fleas, supplying food, shelter, and mates in an expanse of unfavorable habitat, the situation resembles that for terrestrial animals and plants on geological islands in an expanse of water. However, flea species richness is not correlated with host species body size (Stanko et al. 2002, Krasnov et al. 2004), but it is correlated with host species geographic range (Krasnov et al. 2004, Bossard 2006), and host population density (Stanko et al. 2002). Mammals infested with many species of flea could be important in epidemics, if any fleas were vectoring pathogens, but to measure flea species richness on mammals requires extensive data on flea occurrence on mammals. H. J. Egoscue trapped mammals in the Great Basin Desert and recorded their fleas from 1950 to 2002 in a variety of life zones throughout the seasons. He studied flea taxonomy and distribution, and host ecology and behavior, especially for the kit fox (Vulpes macrotis Merriam), deer mouse (Peromyscus maniculatus (Wagner)), and woodrat (Neotoma spp.), but did not analyze his data for species richness (Egoscue 1957, 1962, 1964, 1976, 1977, 1988, etc.). In preliminary analyses of Egoscue’s data, Bossard (2006) clustered mammals and their fleas using multivariate statistics. The data for the current analysis are primarily from Egoscue’s specimens of fleas and associated field data. The fleas are slidemounted and identified to species with their host and locality and, along with his laboratory and field records for fleas and mammals, are deposited in the H. J. Egoscue collections (University of Utah, Salt Lake City). In this paper, I evaluate the correlation of flea species richness
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on individual hosts and host species with host body size and population density using H. J. Egoscue’s trapping data in the Great Basin Desert. MATERIALS AND METHODS The Great Basin Desert is a mountainous desert in the western U.S. and consists of a variety of life zones, including salt deserts, grass and shrublands, wetlands, and high altitude forests (Trimble 1989, Bryce et al. 2003). Fleas and mammals examined in this study were recorded from Egoscue’s data and from Parker and Howell (1959) (Bossard 2006). In addition, the current study considers the following hosts: Microtus pennsylvanicus (Ord) (meadow vole), Mustela frenata Lichtenstein (long-tailed weasel), Mustela erminea L. (short-tailed weasel), Tamias umbrinus (Allen) (Uinta chipmunk), Ursus americanus (Pallas) (American black bear), and Vulpes vulpes (L.) (red fox), and does not include the mountain cottontail (Sylvilagus nuttallii (Bachman)) due to insufficient samples. For species with a large number of trapping records, such as P. maniculatus, only a portion of the data were used. For each mammal species, body mass (average, in g), and population density (mean number of individuals/m2) were estimated from the literature for the species throughout their ranges, including the Great Basin Desert. Because there was variation in the literature for average mass of a species, the maximum mass was also checked for correlation. Flea species richness on individual mammals was regressed (MS Excel) against average body mass (n = 303) and mean population density (n = 281). In addition, average flea species richness (n = 50 for mass, and n = 47 for density) and overall flea species richness for the host species were regressed to see if other calculations of flea species richness would show relationships with body mass or population density. Though ideally this investigation should use the actual mass and population density of the individual mammals that were trapped for fleas, these data do not exist, necessitating the use of literature-derived estimates. Because Egoscue’s data do not include hosts without fleas, his original data could give misleading results for small, or less dense, species that the theory implies should show more individuals without fleas. “Negative data” (flea-free hosts) are important to record along with parasite-infested hosts in order to determine parasite distributions. To find if missing hosts without fleas could influence the regressions, I evaluated additional, hypothetical data sets. They were constructed by assuming that 10% of populations of small mammals (maximum mass equal or less than 31 g), or 10% of mammal populations with low density (less than 0.004 individuals/m2), were infested by fleas. RESULTS Neither regression, between flea species richness and mammal size nor between flea species richness and mammal population density, showed the predicted correlations, whether on individual mammals, average for the mammal species, or overall flea species richness for the mammal species (P>0.05). The artificial data sets showed that any absence of records of flea-free hosts in the data did not influence the regression results significantly. Indeed, there was an intermediate mass (31 g) and
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population density (0.004 hosts/m2) for maximum flea species richness on individual hosts: one Peromyscus truei (Shufeldt) was parasitized by eight species of fleas (Atyphloceras echis Jordan and Rothschild, Epitedia stanfordi Traub, Malareus euphorbi (Rothschild), Malareus telchinum (Rothschild), Megarthroglossus procus Jordan and Rothschild, Megarthroglossus smiti Mendez, Meringis hubbardi Kohls, and Rhadinopsylla sectilis (Jordan and Rothschild)). Larger mammals such as C. latrans and mammals with denser populations, such as C. longimembris, the montane vole Microtus montanus (Peale), M. pennsylvanicus, and the house mouse Mus musculus L., had lower flea species richness. In regards to prevalence, lower prevalence of fleas on small hosts was observed. Less than 10% of the individuals of the intermediate-sized (19 g) Great Basin pocket mouse Perognathus parvus (Peale) were infested by fleas such as Meringis hubbardi Kohls. Only 10 to 30% of populations of long-tailed pocket mice Chaetodipus formosus (Merriam) (21 g) were infested with fleas, including Carteretta carteri (C. Fox), and no fleas were recorded from an unspecified percentage of populations of little pocket mice Perognathus longimembris (Coues) (8 g), and dark kangaroo mice Microdipodops megacephalus Merriam (13 g) (Parker and Howell 1959). In contrast, fleas were prevalent on large mammals, with greater than 50% of host populations infested. These large hosts included coyote Canis latrans Say (18 kg) with fleas Cediopsylla inequalis (Baker) and Pulex irritans L., and American badger Taxidea taxus Schreber (11 kg) with P. irritans (Parker and Howell 1959, Bossard 2006). DISCUSSION Based on H. J. Egoscue’s collections in the Great Basin Desert, flea species richness was not correlated with host size or host population density, contrary to predictions of island biogeography theory. Large mammals had low flea species richness. Because Egoscue attempted to remove all fleas from the mammals trapped, insufficient sampling will not explain low numbers of flea species, especially on large mammals. Krasnov et al. (2004) hypothesized that host burrow size may better predict flea species richness than host size, but this hypothesis is untested. Large mammals in the Great Basin Desert often do not use burrows, or use shallow, exposed holes, which makes life difficult for immature fleas in the harsh desert conditions. Pulicid fleas, which specialize on large mammals, may have behaviors or physiologies which allow them to thrive with high prevalence on large mammals, but it is unclear what those traits may be (Bossard 2006). Density of host populations correlates with flea species richness when using local estimates of density but does not correlate when using density from the literature (Stanko et al. 2002). The current study used density from the literature and similarly found no correlation. However, the lack of correlation may not be simply an artifact of data sources. Many of the mammal populations with low flea species richness fluctuate cyclically; for instance, voles (Microtus spp.) This population variability makes them less favorable hosts for parasites (May and Anderson 1978, Stanko et al. 2006).
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Large geographic ranges enable mammals to contact many habitats and hosts. Such mammals tend to pick up more fleas (Krasnov et al. 2004, Bossard 2006). The simplifying assumption that individual mammals act like geological islands among which flea species travel is not true in the Great Basin Desert. Individual mammals may be far from the equilibrium required by island biogeography theory (Combes 2000, Soliman et al. 2001, Krasnov et al. 2006, Monello and Gompper 2009), but non-equilibrium does not seem to explain low species richness on large mammals. Further, interactions of fleas with their hosts and other fleas are significant in affecting colonization and extinction of flea species on hosts (Marshall 1981). Bossard (2006) found, from H. J. Egoscue’s collections, that the richness of flea species on a mammal was determined, not by equilibrial immigration and extinction, but by the mammal’s social interactions, such as through shared nests, and predation. In contrast, the prevalence of a flea species on a host was determined by how closely related the host was to the the flea’s usual host. If the host was the usual one, or closely related to the usual host, then the flea species was prevalent. If the host was not usual but interacted with usual hosts, then the flea species was often a minor member of the flea community on the host. If the host was neither usual, nor interacting with the usual hosts, then the flea species was absent. Associations of flea vectors with mammals are vital for pathogen transmission (Friggens and Beier 2010). Since fleas vary in their types and loads of pathogens, as well as in their vectorial efficiency, increased flea species richness should increase the chances of a mammal being infected. Even if island biogeography theory does not explain flea species richness for all mammals overall, the theory might still be correct within habitat types or mammalian sub-groups, such as predators or rodents. We could consider host burrow size (Krasnov et al. 2004), but estimating effective burrow size is difficult, especially since mammals may den only part of the year. Future research could use complete data sets on all hosts in an area, their population density, their flea density on individual hosts, microbial infections of host and flea, and seasonal and spatial distributions. These data could be evaluated with epidemiology with a transmission rate and colonization success for each species (Arneberg 2002, Foley and Foley 2010). Another approach is metapopulation theory with spatially explicit, interconnected populations (Hanski 1998), of host, vector, and pathogen. Epidemiological or metapopulation theories are possible alternatives to island biogeography theory for describing species richness of parasites (Poulin 2007). Acknowledgments H. J. Egoscue’s collection records were invaluable for this research. I thank L. A. Durden, P. Foley, W. Wills, and anonymous reviewers for reviews. REFERENCES CITED Arneberg, P. 2002. Host population density and body mass as determinants of species richness in parasite communities:
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comparative analyses of directly transmitted nematodes of mammals. Ecography 25: 88-94. Bengtson, S.A., G. Brinck-Lindroth, L. Lundqvist, A. Nilsson, and S. Rundgren. 1986. Ectoparasites on small mammals in Iceland: Origin and population characteristics of a speciespoor insular community. Ecography 9: 143-148. Bossard, R.L. 2006. Mammal and flea relationships in the Great Basin Desert: From H. J. Egoscue’s collections. J. Parasitol. 92: 260-266. Brown, J.H. and M.V. Lomolino. 1989. Independent discovery of the equilibrium theory of island biogeography. Ecology 70: 1954-1957. Bryce, S.A., A.J. Woods, J.D. Morefield, J.M. Omernik, T.R. McKay, G.K. Brackley, R.K. Hall, D.K. Higgins, D.C. McMorran, K.E. Vargas, E.B. Petersen, D.C. Zamudio, and J.A. Comstock. 2003. Ecoregions of Nevada (color poster with map, descriptive text, summary tables, and photographs) (map scale 1:1,350,000). U.S. Geological Survey, Reston, VA. Choe, J.C. and K.C. Kim. 1987. Community structure of arthropod ectoparasites on Alaskan seabirds. Can. J. Zool. 65: 2998-3005. Combes, C. 2000. Introduction: Parasite, hosts, questions. In: R. Poulin, S. Morand, and A. Skouping (eds.). Evolutionary Biology of Host-parasite Relationships: Theory Meets Reality. pp. 1–8. Elsevier Science B.V., Amsterdam, The Netherlands. Dritschilo, W., H. Cornell, D. Nafus, and B. O’Connor. 1975. Insular biogeography: of mice and mites. Science 190: 467469. Durden, L.A. 1995. Fleas (Siphonaptera) of cotton mice on a Georgia barrier island: a depauperate fauna. J. Parasitol. 81: 526-529. Egoscue, H.J. 1957. The desert woodrat: a laboratory colony. J. Mamm. 38: 472-481. Egoscue, H.J. 1962. Ecology and life history of the kit fox in Tooele County, Utah. Ecology 43: 481-497. Egoscue, H.J. 1964. Ecological notes and laboratory life history of the canyon mouse. J. Mamm. 45: 387-396. Egoscue, H.J. 1976. Flea exchange between deer mice and some associated small mammals in western Utah. West. N. Am. Naturalist 36: 475-480. Egoscue, H.J. 1977. The sagebrush vole flea, Megabothris clantoni princei, in western Utah, with comments on the distribution of Megabothris in the Bonneville Basin. West. N. Am. Naturalist 37: 75-76. Egoscue, H.J. 1988. Noteworthy flea records from Utah, Nevada, and Oregon. West. N. Am. Naturalist 48: 530-532. Esch, G.W., A.O. Bush, and J.M. Aho. 1990. Parasite Communities: Patterns and Processes. Chapman and Hall, London, United Kingdom. Foley, P. and J. Foley. 2010. Modeling susceptible infective recovered dynamics and plague persistence in California rodent–flea communities. Vector Borne Zoonotic Dis. 10: 5967. Friggens, M.M. and P. Beier. 2010. Anthropogenic disturbance and the risk of flea-borne disease transmission. Oecologia 164: 809-820. Guegan, J.F. and C.R. Kennedy. 1993. Maximum local helminth parasite community richness in British freshwater fish: a test of the colonization time hypothesis. Parasitology 106: 91-100.
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Hanski, I. 1998. Metapopulation dynamics. Nature 396: 41-49. Holmes, J. C. and P. W. Price. 1986. Communities of parasites. In: D. J. Anderson and J. Kikkawa (eds.). Community Biology: Pattern and Processes. pp. 187–213. Blackwell, Oxford, United Kingdom. Kamiya, T., O’Dwyer, K., Nakagawa, S. and Poulin, R. 2014. What determines species richness of parasitic organisms? A metaanalysis across animal, plant and fungal hosts. Biological Reviews 89: 123–134. doi: 10.1111/brv.12046 Krasnov, B.R., G.I. Shenbrot, S.G. Medvedev, V.S. Vatschnok, and I.S. Khokhlova. 1997. Host–habitat relations as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitology 114: 159-173. Krasnov, B. R., G. I. Shenbrot, I. S. Khokhlova, and A. A. Degen. 2004. Flea species richness and parameters of host body, host geography and host ‘milieu’. J. Anim. Ecol. 73: 1121-1128. Krasnov, B.R., M. Stanko, and S. Morand. 2006. Age-dependent flea (Siphonaptera) parasitism in rodents: A host’s life history matters. J. Parasitol. 92: 242-248. Kuris, A.M., A.R. Blaustein, and J.J. Alio. 1980. Hosts as islands. Am. Nat. 116: 570-586. Laakkonen, J., R.N. Fisher, and T.J. Case. 2003. Microparasite assemblages of conspecific shrew populations in southern California. J. Parasitol. 89: 1153-1158. Lindenfors, P., C.L. Nunn, K.E. Jones, A.A. Cunningham, W. Sechrest, and J.L. Gittleman. 2007. Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density. Global Ecol. Biogeogr. 16: 496– 509. Luque, J.L., D. Mouillot, and R. Poulin. 2004. Parasite biodiversity and its determinants in coastal marine teleost fishes of Brazil. Parasitology 128: 671-682. MacArthur, R.H. and E.O. Wilson. 1967. The Theory of Island Biogeography. Princeton University Press, Princeton, NJ. Marshall, A.G. 1981. The Ecology of Ectoparasitic Insects. Academic Press, London. May, R.M. and R.M. Anderson. 1978. Regulation and stability of host–parasite population interactions II. Destabilizing processes. J. Anim. Ecol. 47: 249-267. Monello, R.J. and M.E. Gompper. 2009. Relative importance of demographics, locale, and seasonality underlying louse and flea parasitism of raccoons (Procyon lotor). J. Parasitol. 95: 5662. Morand S. and R. Poulin. 1998. Density, body mass and parasite species richness of terrestrial mammals. Evol. Ecol. 12: 717– 727. O’Connor, B.M., W. Dritschilo, D. Nafus, and H. Cornell. 1977. Ectoparasitic mites on rodents: application of the island biogeography theory? A reply to Kuris and Blaustein. Science 195: 596-598.
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Parker, D.D. and J.F. Howell. 1959. Host-flea relationships in the Great Salt Lake Desert. J. Parasitol. 45: 597-604. Poulin, R. 1997. Species richness of parasite assemblages: evolution and patterns. Annu. Rev. Ecol. Syst. 28: 341-358. Poulin, R. 2004. Macroecological patterns of species richness in parasite assemblages. Basic Appl. Ecol. 5: 423-434. Poulin, R. 2007. Are there general laws in parasite ecology? Parasitology 134: 763-776. Price, P.W. 1980. Evolutionary Biology of Parasites. Princeton University Press, Princeton, NJ. Reperant, L.A. 2010. Applying the theory of island biogeography to emerging pathogens: toward predicting the sources of future emerging zoonotic and vector-borne diseases. Vectorborne Zoonot. Dis. 10: 105-110. Ròzsa, L. 1993. Speciation patterns of ectoparasites and “straggling lice”. Int. J. Parasitol. 23: 859-864. Sánchez, S., E. Serrano, M. Gómez, C. Feliu, and S. Morand. 2013. Positive co-occurrence of flea infestation at a low biological cost in two rodent hosts in the Canary archipelago. Parasitology 21: 1-11. doi: 10.1017/S0031182013001753. Scharf, W.C. 1991. Geographic distribution of Siphonaptera collected from small mammals on Lake Michigan islands. Great Lakes Entomol. 24: 39-43. Soliman, S., A.S. Marzouk, A.J. Main, and A.A. Montasser. 2001. Effect of sex, size, and age of commensal rat hosts on the infestation parameters of their ectoparasites in a rural area of Egypt. J. Parasitol. 87: 1308-1316. Stanko, M., B.R. Krasnov, and S. Morand. 2006. Relationship between host abundance and parasite distribution: inferring regulating mechanisms from census data. J. Anim. Ecol. 75: 575–583. Stanko, M., D. Miklisová, J. Goüy de Bellocq, and S. Morand. 2002. Mammal density and patterns of ectoparasite species richness and abundance. Oecologia 131: 289–295. Tallamy, D.W. 1983. Equilibrium biogeography and its application to insect host-parasite systems. Am. Nat. 121: 244-254. Trimble, S. 1989. The sagebrush ocean: Natural history of the Great Basin Desert. University of Nevada Press, Reno, NV. Wilkinson, D.M. 1993. Equilibrium island biogeography: Its independent invention and the marketing of scientific theories. Global Ecol. Biogeogr. 3: 65-66. Wilson, N. and L.A. Durden 2003. Ectoparasites of terrestrial vertebrates inhabiting the Georgia Barrier Islands, USA: an inventory and preliminary biogeographical analysis. J. Biogeogr. 30: 1207-1220. Zander, C.D. 2005. Four-year monitoring of parasite communities in gobiid fishes of the southwest Baltic - III. Parasite species diversity and applicability of monitoring. Parasitol. Res. 95: 136-144.
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Flea (Siphonaptera) species richness in the Great Basin Desert and island biogeography theory Robert L. Bossard Westminster College, Salt Lake City, UT 84105, U.S.A., [email protected] Received 12 December 2014; Accepted 11 February 2014 ABSTRACT: Numbers of flea (Siphonaptera) species (flea species richness) on individual mammals should be higher on large mammals, mammals with dense populations, and mammals with large geographic ranges, if mammals are islands for fleas. I tested the first two predictions with regressions of H. J. Egoscue’s trapping data on flea species richness collected from individual mammals against mammal size and population density from the literature. Mammal size and population density did not correlate with flea species richness. Mammal geographic range did, in earlier studies. The intermediate-sized (31 g), moderately dense (0.004 individuals/m2) Peromyscus truei (Shufeldt) had the highest richness with eight flea species on one individual. Overall, island biogeography theory does not describe the distribution of flea species on mammals in the Great Basin Desert, based on H. J. Egoscue’s collections. Alternatively, epidemiological or metapopulation theories may explain flea species richness. Journal of Vector Ecology 39 (1): 164-167. 2014. Keyword Index: host size, host density, host range, fleas, species richness, island biogeography theory.
INTRODUCTION Island biogeography theory is a simple, influential model of species richness reflecting an equilibrium between species immigration and extinction. The theory predicts that species richness will be less on small or distant islands (MacArthur and Wilson 1967, Brown and Lomolino 1989, Wilkinson 1993). Islands are depauperate of fleas (Siphonaptera) (Bengtson et al. 1986, Durden 1995, Wilson and Durden 2003, Sánchez et al. 2013), but Scharf (1991) found no effect in Lake Michigan of island size or distance on species richness of fleas. An interesting extension of the original island biogeography theory is to assume that, like geological islands, hosts themselves are islands for parasites. Island size and distance are a function of the “host size, host population size, or magnitude of host geographic range” (Price 1980)(Kuris et al. 1980, Tallamy 1983, Holmes and Price 1986, Esch et al. 1990, Morand and Poulin 1998, Combes 2000, Luque et al. 2004, Poulin 2004, Zander 2005, Reperant 2010). Results of testing island biogeography theory with parasites have been mixed (Choe and Kim 1987, Ròzsa 1993, Poulin 1997, 2007). For example, species richness of ectoparasitic mites on some rodents is correlated with host range (Dritschilo et al. 1975, O’Connor et al. 1977), and parasite species richness of fissiped carnivores is correlated with host body mass, host population density, and host geographic range (Lindenfors et al. 2007). However, parasite species richness of freshwater fish is not correlated with host range (Guegan and Kennedy 1993), for shrews is not correlated with population density (Laakkonen et al. 2003), and for bats is not correlated with host body size, but is with population density. Poulin (2007) wrote that with “every positive relationship between a host trait and parasite species richness currently published, one can find a negative relationship and some nonsignificant relationships.” Remarkably, Kamiya et al. (2014)
claimed that all three variables were “universal predictors of parasite richness across host species, namely host body size, geographical range size and population density, applicable regardless of the taxa considered.” For fleas, “hosts can be considered as biological islands... and so the parasite communities should conform to principles of classical insular biogeography” (Krasnov et al. 1997). Because mammals are small patches of favorable habitat for fleas, supplying food, shelter, and mates in an expanse of unfavorable habitat, the situation resembles that for terrestrial animals and plants on geological islands in an expanse of water. However, flea species richness is not correlated with host species body size (Stanko et al. 2002, Krasnov et al. 2004), but it is correlated with host species geographic range (Krasnov et al. 2004, Bossard 2006), and host population density (Stanko et al. 2002). Mammals infested with many species of flea could be important in epidemics, if any fleas were vectoring pathogens, but to measure flea species richness on mammals requires extensive data on flea occurrence on mammals. H. J. Egoscue trapped mammals in the Great Basin Desert and recorded their fleas from 1950 to 2002 in a variety of life zones throughout the seasons. He studied flea taxonomy and distribution, and host ecology and behavior, especially for the kit fox (Vulpes macrotis Merriam), deer mouse (Peromyscus maniculatus (Wagner)), and woodrat (Neotoma spp.), but did not analyze his data for species richness (Egoscue 1957, 1962, 1964, 1976, 1977, 1988, etc.). In preliminary analyses of Egoscue’s data, Bossard (2006) clustered mammals and their fleas using multivariate statistics. The data for the current analysis are primarily from Egoscue’s specimens of fleas and associated field data. The fleas are slidemounted and identified to species with their host and locality and, along with his laboratory and field records for fleas and mammals, are deposited in the H. J. Egoscue collections (University of Utah, Salt Lake City). In this paper, I evaluate the correlation of flea species richness
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on individual hosts and host species with host body size and population density using H. J. Egoscue’s trapping data in the Great Basin Desert. MATERIALS AND METHODS The Great Basin Desert is a mountainous desert in the western U.S. and consists of a variety of life zones, including salt deserts, grass and shrublands, wetlands, and high altitude forests (Trimble 1989, Bryce et al. 2003). Fleas and mammals examined in this study were recorded from Egoscue’s data and from Parker and Howell (1959) (Bossard 2006). In addition, the current study considers the following hosts: Microtus pennsylvanicus (Ord) (meadow vole), Mustela frenata Lichtenstein (long-tailed weasel), Mustela erminea L. (short-tailed weasel), Tamias umbrinus (Allen) (Uinta chipmunk), Ursus americanus (Pallas) (American black bear), and Vulpes vulpes (L.) (red fox), and does not include the mountain cottontail (Sylvilagus nuttallii (Bachman)) due to insufficient samples. For species with a large number of trapping records, such as P. maniculatus, only a portion of the data were used. For each mammal species, body mass (average, in g), and population density (mean number of individuals/m2) were estimated from the literature for the species throughout their ranges, including the Great Basin Desert. Because there was variation in the literature for average mass of a species, the maximum mass was also checked for correlation. Flea species richness on individual mammals was regressed (MS Excel) against average body mass (n = 303) and mean population density (n = 281). In addition, average flea species richness (n = 50 for mass, and n = 47 for density) and overall flea species richness for the host species were regressed to see if other calculations of flea species richness would show relationships with body mass or population density. Though ideally this investigation should use the actual mass and population density of the individual mammals that were trapped for fleas, these data do not exist, necessitating the use of literature-derived estimates. Because Egoscue’s data do not include hosts without fleas, his original data could give misleading results for small, or less dense, species that the theory implies should show more individuals without fleas. “Negative data” (flea-free hosts) are important to record along with parasite-infested hosts in order to determine parasite distributions. To find if missing hosts without fleas could influence the regressions, I evaluated additional, hypothetical data sets. They were constructed by assuming that 10% of populations of small mammals (maximum mass equal or less than 31 g), or 10% of mammal populations with low density (less than 0.004 individuals/m2), were infested by fleas. RESULTS Neither regression, between flea species richness and mammal size nor between flea species richness and mammal population density, showed the predicted correlations, whether on individual mammals, average for the mammal species, or overall flea species richness for the mammal species (P>0.05). The artificial data sets showed that any absence of records of flea-free hosts in the data did not influence the regression results significantly. Indeed, there was an intermediate mass (31 g) and
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population density (0.004 hosts/m2) for maximum flea species richness on individual hosts: one Peromyscus truei (Shufeldt) was parasitized by eight species of fleas (Atyphloceras echis Jordan and Rothschild, Epitedia stanfordi Traub, Malareus euphorbi (Rothschild), Malareus telchinum (Rothschild), Megarthroglossus procus Jordan and Rothschild, Megarthroglossus smiti Mendez, Meringis hubbardi Kohls, and Rhadinopsylla sectilis (Jordan and Rothschild)). Larger mammals such as C. latrans and mammals with denser populations, such as C. longimembris, the montane vole Microtus montanus (Peale), M. pennsylvanicus, and the house mouse Mus musculus L., had lower flea species richness. In regards to prevalence, lower prevalence of fleas on small hosts was observed. Less than 10% of the individuals of the intermediate-sized (19 g) Great Basin pocket mouse Perognathus parvus (Peale) were infested by fleas such as Meringis hubbardi Kohls. Only 10 to 30% of populations of long-tailed pocket mice Chaetodipus formosus (Merriam) (21 g) were infested with fleas, including Carteretta carteri (C. Fox), and no fleas were recorded from an unspecified percentage of populations of little pocket mice Perognathus longimembris (Coues) (8 g), and dark kangaroo mice Microdipodops megacephalus Merriam (13 g) (Parker and Howell 1959). In contrast, fleas were prevalent on large mammals, with greater than 50% of host populations infested. These large hosts included coyote Canis latrans Say (18 kg) with fleas Cediopsylla inequalis (Baker) and Pulex irritans L., and American badger Taxidea taxus Schreber (11 kg) with P. irritans (Parker and Howell 1959, Bossard 2006). DISCUSSION Based on H. J. Egoscue’s collections in the Great Basin Desert, flea species richness was not correlated with host size or host population density, contrary to predictions of island biogeography theory. Large mammals had low flea species richness. Because Egoscue attempted to remove all fleas from the mammals trapped, insufficient sampling will not explain low numbers of flea species, especially on large mammals. Krasnov et al. (2004) hypothesized that host burrow size may better predict flea species richness than host size, but this hypothesis is untested. Large mammals in the Great Basin Desert often do not use burrows, or use shallow, exposed holes, which makes life difficult for immature fleas in the harsh desert conditions. Pulicid fleas, which specialize on large mammals, may have behaviors or physiologies which allow them to thrive with high prevalence on large mammals, but it is unclear what those traits may be (Bossard 2006). Density of host populations correlates with flea species richness when using local estimates of density but does not correlate when using density from the literature (Stanko et al. 2002). The current study used density from the literature and similarly found no correlation. However, the lack of correlation may not be simply an artifact of data sources. Many of the mammal populations with low flea species richness fluctuate cyclically; for instance, voles (Microtus spp.) This population variability makes them less favorable hosts for parasites (May and Anderson 1978, Stanko et al. 2006).
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Large geographic ranges enable mammals to contact many habitats and hosts. Such mammals tend to pick up more fleas (Krasnov et al. 2004, Bossard 2006). The simplifying assumption that individual mammals act like geological islands among which flea species travel is not true in the Great Basin Desert. Individual mammals may be far from the equilibrium required by island biogeography theory (Combes 2000, Soliman et al. 2001, Krasnov et al. 2006, Monello and Gompper 2009), but non-equilibrium does not seem to explain low species richness on large mammals. Further, interactions of fleas with their hosts and other fleas are significant in affecting colonization and extinction of flea species on hosts (Marshall 1981). Bossard (2006) found, from H. J. Egoscue’s collections, that the richness of flea species on a mammal was determined, not by equilibrial immigration and extinction, but by the mammal’s social interactions, such as through shared nests, and predation. In contrast, the prevalence of a flea species on a host was determined by how closely related the host was to the the flea’s usual host. If the host was the usual one, or closely related to the usual host, then the flea species was prevalent. If the host was not usual but interacted with usual hosts, then the flea species was often a minor member of the flea community on the host. If the host was neither usual, nor interacting with the usual hosts, then the flea species was absent. Associations of flea vectors with mammals are vital for pathogen transmission (Friggens and Beier 2010). Since fleas vary in their types and loads of pathogens, as well as in their vectorial efficiency, increased flea species richness should increase the chances of a mammal being infected. Even if island biogeography theory does not explain flea species richness for all mammals overall, the theory might still be correct within habitat types or mammalian sub-groups, such as predators or rodents. We could consider host burrow size (Krasnov et al. 2004), but estimating effective burrow size is difficult, especially since mammals may den only part of the year. Future research could use complete data sets on all hosts in an area, their population density, their flea density on individual hosts, microbial infections of host and flea, and seasonal and spatial distributions. These data could be evaluated with epidemiology with a transmission rate and colonization success for each species (Arneberg 2002, Foley and Foley 2010). Another approach is metapopulation theory with spatially explicit, interconnected populations (Hanski 1998), of host, vector, and pathogen. Epidemiological or metapopulation theories are possible alternatives to island biogeography theory for describing species richness of parasites (Poulin 2007). Acknowledgments H. J. Egoscue’s collection records were invaluable for this research. I thank L. A. Durden, P. Foley, W. Wills, and anonymous reviewers for reviews. REFERENCES CITED Arneberg, P. 2002. Host population density and body mass as determinants of species richness in parasite communities:
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