Island and Taxon Effects in Parasitism and Resistance of Lesser Antillean Birds
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Ecology, 81(7), 2000, pp. 1959±1969 q 2000 by the Ecological Society of America ISLAND AND TAXON EFFECTS IN PARASITISM AND RESISTANCE OF LESSER ANTILLEAN BIRDS VICTOR APANIUS,1,3 NANCY YORINKS,1,4 ELDREDGE BERMINGHAM,2 AND ROBERT E. RICKLEFS1,2,5 1Department of Biology, Leidy Laboratories, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6018 USA 2Smithsonian Tropical Research Institute, Unit 0948, APO AA 34002-0948 USA, and Apto. Postal 2072, Balboa, Republica de Panama Abstract. Patterns of parasitism in insular avian communities can provide insight into processes that maintain host±parasite associations. On one hand, replicable relationships within evolutionarily independent communities of the same host and parasite taxa would indicate that these interactions are stable over time. On the other hand, unique ecological conditions on each island, sporadic colonizations and extinctions, plus new genetic variation would lead to island-speci®c host±parasite relationships. We examined the distribution of three parasitic taxa among avian host species on three islands in the Lesser Antilles: St. Lucia, Martinique, and Dominica. Blood protozoa of the genus Haemoproteus were found in 34% of host individuals examined. A signi®cant species effect, but no signi®cant island effect, was observed, suggesting an ecologically stable and replicable host±parasite asso- ciation. Cysts of the tissue-dwelling protozoan genus Sarcocystis were observed in 4% (9% on Dominica) of host individuals and were signi®cantly associated with ground foraging. Epithelial lesions characteristic of avian papilloma virus were recorded in 4% of host individuals on Martinique only. The pattern of infection with papilloma virus or Sarcocystis (signi®cant island effect) indicated that host species on a particular island are linked in transmission webs of these parasites. Such island-speci®c associations suggest a role for either history or unique local ecology in host±parasite associations. There was a statistically signi®cant interaction between island and species effects in the prevalence of Haemoproteus. This may stem from the independent evolution of host± parasite interactions in the different island populations. We were able to assess the extent of genetic divergence of the host species by analysis of mitochondrial ATPase 6,8 sequences. There was little genetic divergence between island populations of the host species. There- fore, the variation in Haemoproteus prevalence is not likely to be related to genetic dif- ferentiation of the host populations. Birds infected with Haemoproteus exhibited elevated leukocyte levels indicative of immunological control of the parasite. After statistically controlling for the intensity of Haemoproteus infection and host species, leukocyte levels varied signi®cantly among is- lands on which the host resided. This is consistent with the idea that insular avian com- munities are linked by transmission webs of parasites having broad host speci®city. Key words: blood parasites; Haemoproteus; hematozoans; host±parasite interactions; immune response; Lesser Antilles; leukocyte counts; papilloma virus; Sarcocystis. INTRODUCTION cluding the role of the immune response (Norman et al. 1994). Although empirical investigations have The dynamics and organization of communities of lagged, in part because of the complexity of natural parasites having many vertebrate hosts has proven to communities (e.g., Aho and Bush 1993), temporal and be a challenging problem for ecologists and evolution- spatial variation in parasite prevalence and infection ary biologists. Theoretical models have considered the by pathogens suggest complex, spatially heterogeneous population dynamics of such interactions (May and An- dynamics in host±parasite systems on ecological scales, derson 1979, Hudson et al. 1985, Crawley 1992), in- evolutionary scales, or both (van Riper et al. 1986, Prins and Weyerhaeuser 1987, Atkinson et al. 1988, Manuscript received 10 November 1997; revised 8 July 1998; Atkinson and Van Riper 1991, Yezerinac and Weath- accepted 21 October 1998; ®nal version received 17 May 1999. 3 Present address: Department of Biological Sciences, erhead 1995). Florida International University, University Park, Miami, Empirical studies of temporal and spatial heteroge- Florida 33199 USA. E-mail: apanius@®u.edu neity in parasite±host interactions are most informative 4 Present address: School of Veterinary Medicine, 2015 when comparisons are made among discrete popula- Linden Drive West, University of Wisconsin, Madison, Wis- tions. Longitudinal studies of geographically circum- consin 53706 USA. 5 Present address: Department of Biology, University of scribed host populations can provide insight into the Missouri, 8001 Natural Bridge Road, St. Louis, Missouri ecological and evolutionary dynamics of multiple host± 63121-4499 USA. parasite relationships (Forbes et al. 1994, Bennett et 1959 1960 VICTOR APANIUS ET AL. Ecology, Vol. 81, No. 7 al. 1995, MerilaÈ et al. 1995), but inferences may be turnover of the avifaunas between islands preclude the obscured by temporal or spatial variation in the data. estimation of island 3 host interactions in these data. The roles of ecological and evolutionary factors in In this study, we present data on haematozoan par- the outcome of host±parasite interactions can be teased asite prevalence and white blood cell counts for six apart statistically by examining a set of species over species of passerine bird on three adjacent islands in several discrete localities, such as isolated islands. In the Lesser Antilles. The host species were the Bana- this case, island effects represent unique attributes of naquit (Coereba flaveola), Antillean Elaenia (Elaenia individual islands, which may include the array of hab- martinica), Lesser Antillean Bull®nch (Loxigilla noc- itats on each island, composition of the host commu- tis), Streaked Saltator (Saltator albicollis), Black-faced nity, and presence of suitable vectors and reservoirs Grassquit (Tiaris bicolor), and the Black-whiskered for parasites. To the extent that an island effect may Vireo (Vireo altiloquus). Data were collected during a result from community composition, it may also, in single, brief period in 1991. Our sampling design al- part, re¯ect stochasticity of colonization and extinction lowed us to estimate island and host effects as well as independent of an island's ecology. Host-speci®c ef- host 3 island interactions. Signi®cant host effects in fects may arise because of unique genetic or ecological the prevalence of the protozoan parasite Haemoproteus attributes of each type of host. From the standpoint of spp. demonstrated that the sampling program was large host±parasite evolution, the most revealing source of enough to discern statistically signi®cant host±parasite variation is the host 3 island interaction, which indi- combinations. Moreover, blood leukocyte counts, which cates the extent of unique outcomes of host±parasite indicate an individual host's response to its parasite relationship in a particular host across a set of ecolog- load (Fallis et al. 1951, Desser et al. 1968), show that ically de®ned locations. Such statistical interactions both deterministic and historical factors shape host± could result from island-speci®c genetic factors in the parasite associations. Finally, we suggest a framework host resulting from founder events and mutation. Host± for gauging the relative importance of these factors parasite coevolution, i.e., reciprocal genetic changes in based on island biogeographic analysis. host and parasite populations, would also have to be considered as a possibility. STUDY AREA AND METHODS Several studies have addressed the distribution of This study was conducted on St. Lucia, Martinique, parasites across island populations, but these have and Dominica, Lesser Antilles, between 20 July and lacked suitable sampling to detect host 3 island inter- 10 August 1991. These islands are similar in size (616± actions. An analysis of the gut helminth parasites of 1100 km2) and reach elevations (960±1450 m) that cre- Anolis lizards in the Lesser Antilles related variation ate a variety of habitats ranging from montane forest in parasitism to the distribution of hosts among habitats to dry lowland scrub (Beard 1949, Lack 1976). We within islands rather than to ecological differences be- sampled both wet and dry habitats in different parts of tween islands associated with area or altitude (Dobson each island to obtain a representative sample of each and Pacala 1992). Repeatable associations between island's avifauna. To some extent, the sample sizes (9± parasites and hosts thus appear to follow upon envi- 37 individuals per island population) re¯ect the relative ronmental factors. However, disjunct distributions of abundances of the host species on each island. Birds many parasites suggested that historical factors, such were captured with mist nets at the following locations as colonization and extinction, may have in¯uenced the (and dates): on St. Lucia, Edmond Forest Preserve (20± particular assemblage of parasite species within each 22 July), and Anse La Sorciere (23±25 July); on Dom- host population (Dobson and Pacala 1992). Because inica, Spring®eld Plantation-Mt. Joy Estate (27±29 Anolis comprises only one or two morphologically dis- July), Syndicate Estate (30±31 July), Ponte Casse (1 tinct species on most islands, it is dif®cult to resolve August), and Glanvillia Quarry (2 August); on Mar- whether the observed patterns represent