The Auk A Quarterly Journal of Ornithology Vol. 123 No. 3 July 2006
The Auk 123(3):625–638, 2006 © The American Ornithologists’ Union, 2006. Printed in USA. PERSPECTIVES IN ORNITHOLOGY CONSERVATION MEDICINE ON THE GALÁPAGOS ISLANDS: PARTNERSHIPS AMONG BEHAVIORAL, POPULATION, AND VETERINARY SCIENTISTS
Pf w h f G. Pfwp w,1,2,3 N f K w W rf ,1 f i R. Ew h M qq w2 1Department of Biology and International Center for Tropical Ecology, University of Missouri at St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121, USA; and 2Saint Louis Zoo, 1 Government Drive, St. Louis, Missouri 63110, USA
T animals in nature is mediated systems play in populations, and that populations by behavior, through individuals’ relative eff ec- play in relation to species. As we approached the tiveness in securing food, shelter, and mates. problem of studying diseases among birds in the Especially in its ecological context, animal Galápagos Islands, we took the perspective of behavior is responsible for the movement of behavioral ecologists, curious about the variable genes among population units and contributes roles among individuals, populations, and spe- strongly to the relative success and failure of cies in the dynamics of disease transmission. particular lineages. Behavioral ecology, an evolu- Veterinary medicine, likewise, has evolved tionary approach to the study of animal behavior signifi cantly in the decades since the 1970s, that emerged as a discipline in the 1970s, has incorporating the latest developments from produced bodies of rigorous theory on reproduc- population biology, human medicine, and the tive and foraging strategies, social systems, and biology and control of pathogenic organisms. communication. These theories are increasingly Seeking to understand threats of disease on being evaluated within a phylogenetic context. the Galápagos Islands by joining these perspec- During the same decades, developing tives, we have embarked on studies that have population-genetics methods brought historical implications in both basic and applied realms. perspective with the phylogeographic approach, At the outset, we anticipated that understand- as well as current estimates of gene fl ow (even ing the population dynamics of Galápagos birds asymmetrical gene fl ow between population would help us interpret parasite and pathogen subunits), and accurate measures of individual distribution and host susceptibility, and that our reproductive success, each with resolution that clinical fi ndings in parasite and pathogen distri- was not possible through more traditional mea- bution would inform our behavioral ecological sures. These approaches mean that we can inter- studies of Galápagos bird populations. pret the behavior of animals in a richer context Historically, the eff ect of disease on wildlife than was possible before, accounting for the roles populations has been understudied, aside from that individuals play in social systems, that social a few cases of conservation interest. Parasite- induced diseases have been underestimated, partly from the erroneous view that parasites 3E-mail: [email protected] that coevolve with their hosts do not have severe
625 626 Perspectives in Ornithology [Auk, Vol. 123 negative eff ects on them and partly from logisti- Galápagos National Park and Marine Reserve cal diffi culties (Gulland 1995). Disease, however, since the 1950s. However, the resident human has been shown to aff ect survival, reproduction, population has grown rapidly and exotic and movement in host populations, and to aff ect species are continually being introduced despite community structure in turn (reviewed in Sco increasing eff orts to exclude them. The Charles 1988). At the same time, emergent diseases are Darwin Foundation and the Galápagos National more common because of an expanding human Park fear the introduction of avian diseases population, associated growth of domestic ani- that could result in extinctions of Galápagos mal populations, increased travel and commerce, avifauna, similar to what happened in Hawaii human alteration of habitats, and global climate (Warner 1968; van Riper et al. 1986, 2002; change (Daszak et al. 2000). Outbreaks of “mad Wikelski et al. 2004). The appearance of avian- cow disease” (bovine spongiform encephalopa- pox-like lesions in domestic chickens (Gallus thy; Brown et al. 2001), foot-and-mouth disease gallus) on the islands, and then in endemic birds, (Picornaviridae: Aphthovirus; Kitching 1999), heightened concerns regarding the possibility West Nile virus (Flavivirus; Lancio i et al. 1999), of disease transmission from introduced birds SARS (Coronavirus), monkeypox (Orthopoxvirus), to endemics. In fact, it was presumed that pox and avian infl uenza (Orthomyxoviridae) have was brought to the archipelago via chickens demonstrated the virulence of some pathogens in the 20th century (Grant et al. 2000). In the and their potential to cross over to new hosts, mid-1980s, the mosquito Culex quinquefasciatus, including humans. Thus, interest grows in a vector of avian malaria, was reported from the dynamics of infectious diseases in wildlife Galápagos, and its establishment has recently (Daszak et al. 2000, Friend et al. 2001), especially been confi rmed (Whiteman et al. 2005). To date, in threatened species, as we recognize the poten- however, the especially pathogenic strains of tial for disease to limit populations (Thorne and avian malaria of the genus Plasmodium have not Williams 1988, Deem et al. 2001). been found. We have undertaken a large project, Parasites can have especially severe eff ects in collaboration with the Galápagos National when they are transmi ed to novel environments, Park and the Charles Darwin Foundation, to where populations may lack natural resistance. monitor disease status of Galápagos avian Island populations may be at higher risk, because endemics and introduced birds. Partnering their parasite diversity is less than that of their with international experts on major taxonomic continental counterparts (Lewis 1968a, b; Dobson groups of parasites, we use morphological and 1988; Fromont et al. 2001; Goüy de Bellocq et al. molecular approaches to identify organisms. 2002). Founders likely carry only a subset of the We pursue phylogeographic studies to parasites found in the donor population, and understand the history of the parasite lineages virulent pathogens that need large host popula- on the archipelago, and the relationships among tions may be lost quickly (Dobson and May 1986, parasite lineages and among parasites and host Dobson 1988). Paucity of parasites reduces selec- species. The result is a multilayered program tion for resistance and enhances host population examining the interplay between hosts and densities, both of which facilitate the transmis- parasites and the behavioral ecology of both sion of introduced parasites (Dobson 1988). hosts and pathogens, which provides valuable The Galápagos Islands are volcanic in origin information to the managers of this World (Christie et al. 1992, White et al. 1993) and are Heritage Site and adds new dimensions to the located on the equator, ∼1,000 km west of South study of evolutionary ecology of all Galápagos America. Their isolation and relative desolation organisms, regardless of their body size. delayed their permanent colonization by humans until the 1800s, and their biodiversity remains C fwfh w l Pfwf f i Pf l ∼ mostly intact, only 5% of species having Gfqufl I qf i been lost (Gibbs et al. 1999); 26 of 28 breeding landbird species are endemic, and there have In 2001 and 2002, animal health professionals from been no extinctions of bird species. Currently, the Saint Louis Zoo collaborated with biologists from humans occupy only 4 of the 11 main islands, the University of Missouri at St. Louis to off er Avian and most of those 4 islands and the remainder Health Workshops to personnel of the Charles Darwin of the archipelago have been protected as the Research Station, the Galápagos National Park, the July 2006] Perspectives in Ornithology 627 customs and immigration offi ce of Galápagos, and event of outbreaks and receives carcasses reported to local veterinary professionals. Lectures covered the the station, and is involved in a year-round training biology of avian pathogens and diagnostic symptoms program for Ecuadorian veterinarians and veterinary of major avian diseases; hands-on workshops trained pathologists on the islands. We broadened the fi eld participants in phlebotomy for disease testing, smears survey to include four seabird species on Genovesa for blood parasites, and necropsy protocol. Subjects and other island populations of landbirds. Upon cap- were domestic chickens from local farms and Rock ture, birds are handled briefl y while morphological Pigeons (Columba livia) from extermination programs, measures are made and ocular, choanal, and cloacal on the human-inhabited islands of Santa Cruz and swabs are taken. Blood samples (≤1% body weight) San Cristobal. In addition, we began the fi eld surveys are taken, and two smears are made on the spot. One of natural populations of endemic birds. During the drop of blood is preserved in lysis buff er for genetic fi rst two years, plasma and serum samples, blood analyses, whereas the remainder is spun in the fi eld smears, and cloacal swabs were sampled from Waved and plasma or serum frozen in liquid nitrogen. Later, Albatrosses (Phoebastria irrorata), endemic to the island samples and tissues are examined by serological tests, of Española (Padilla et al. 2003); Galápagos Hawks polymerase chain reaction (PCR), microscopy, and (Buteo galapagoensis) from eight islands; Galápagos histopathology (on chickens and Rock Pigeons eutha- Doves (Zenaida galapagoensis) from fi ve islands (three nized humanely as part of the extermination program, uninhabited by humans and two inhabited; Padilla et or on tissues from animals found dead) for complete al. 2004); and from Galápagos Penguins (Spheniscus blood counts, serum chemistry panel, and tests for mendiculus) and Galápagos Flightless Cormorants enteric pathogens (Salmonella, Shigella, Campylobacter (Phalacrocorax harrisi) across their narrow ranges within spp.), Chlamydophila, as well as for avian cholera, avian the archipelago (Travis et al. 2006a, b). Sampling was infl uenza, Newcastle disease, Paramyxovirus 2 and 3, later extended to other species (see below). These West Nile Virus, infectious bronchitis, avian adeno- endemic species were chosen because we were already virus, avian encephalomyelitis virus, avian reovirus, involved in studies of their population biology and Marek’s disease, and infectious bursal disease. Blood genetics. They represented two terrestrial species (one smears were examined for hemoparasites in all spe- of which is the apex predator on the islands) and three cies, and positives were further examined by PCR for marine species (one of which is pelagic and covers identifi cation (Escalante et al. 1998, Ricklefs and Fallon huge distances, the other two of which are fl ightless), 2002, Fallon et al. 2003). Introduced and endemic and so could be seen as sentinel species for a large pro- doves were tested for Trichomonas gallinae. portion of the ecological zones inhabited by birds in the Ectoparasites are collected using a modifi ed Galápagos Islands. In addition, all are relatively large- dust-ruffl ing technique (Walther and Clayton 1997; bodied, so suffi cient samples could be taken to test for Whiteman and Parker 2004a, b) or, in the case of several pathogens. These ongoing population studies fresh carcasses, are removed directly from the hosts. provided a background against which data on disease Although dust-ruffl ing does not remove all ectopara- could be interpreted more fully. For example, our sites (e.g., many mites), it is relatively noninvasive population-genetics studies show that the Galápagos and allows a good estimation of ectoparasite infection Hawk is the most recent arrival of the endemic ver- intensity and prevalence (Walther and Clayton 1997). tebrates on the archipelago (Bollmer et al. 2006), that Ectoparasites are placed in 95–100% ethanol and stored since its arrival it has diversifi ed rapidly among island at –20°C to ensure DNA preservation. DNA is extracted populations, and that individuals very rarely move from exemplars from each host species or population, among islands (Bollmer et al. 2005). By contrast, the depending on the particular requirements of the study. genes of Galápagos Doves move freely among the A voucher method, in which an exoskeleton is retained islands of the main archipelago (Santiago-Alarcón et al. as a voucher specimen, is used (Cruickshank et al. 2006). Similar studies are underway for the penguins 2001, Whiteman et al. 2004). In the case of hippoboscid and cormorants. These data contribute to understand- fl ies or other relatively large arthropods, a single leg ing the timing of arrival of hosts and their host-specifi c is removed. DNA is extracted and used as a source of pathogens, their historical interisland movements, and template DNA for PCRs. Arthropod-specifi c PCR prim- the current dynamics of transmission of pathogens ers are then used to amplify and sequence loci to be among islands and species. For example, comparison used in population or phylogenetic studies (e.g., the 5’ of hawks and doves suggests that the doves are far end of the cytochrome-c oxidase subunit I [COI] is used more likely to distribute pathogens among islands. as a DNA barcode; Hebert et al. 2003). Thus, identifi ca- tions of ectoparasites are made using a combination of V w fw~ f i E{ qz fw~ Auuw fh morphological and molecular characters. For many parasites and pathogens, DNA sequence Since 2002, the Saint Louis Zoo has funded a vet- data off er a larger set of characters than morphological erinary pathologist to reside on the islands as part of data alone, for identifi cation purposes. For example, our research program. This person is present in the with our collaborator, Kevin P. Johnson, we genotyped 628 Perspectives in Ornithology [Auk, Vol. 123
Galápagos Dove lice (Columbicola macrourae and endemic to the Galápagos avifauna, which hopefully Physconelloides galapagensis) that moved horizontally to will encourage studies of other vertebrate groups Galápagos Hawks aV er the hawks fed upon the doves that harbor their own unique parasite lineages (e.g., and showed that the dove lice were indeed derived reptiles: Ayala and Hutchings 1974). from the local Galápagos Dove and were not a typical part of the hawk’s ectoparasite community (Whiteman Pw q r fw~ Szw{ ~ R zq et al. 2004). Genotyping was necessary because female lice of these species are indistinguishable from some D r h f i I w izh i B wi congeners. In the same study, we genotyped a louse nymph (Bovicola sp.) collected from a Galápagos Hawk that presumably moved from a goat carcass on which Domestic chickens were sampled on two the hawks were feeding. In addition to providing of the four human-inhabited islands; several additional characters for identifi cation, DNA sequence pathogens were detected by direct observa- data also allow estimation of relationships among tion, including nematodes (Dispharynx sp. and Galápagoan taxa and their mainland relatives and Capillaria spp.) and the prozotoan Toxoplasmosis estimation of gene fl ow of parasites among islands, a gondii (Go denker et al. 2005). Others were distinctly evolutionary approach that can build from detected by antibody presence (not necessarily and then inform the veterinary fi ndings. indicating active infection): avian adenovirus 1 Endoparasites are identifi ed using traditional (75%), infectious bronchitis CT (14%), infectious taxonomy from blood smears and formalin- bronchitis MA (20%), infectious bursal disease preserved specimens (when hosts are necropsied) and using PCR-based identifi cation (Padilla et al. (23%), avian encephalomyelitis (46%), and 2004). Moreover, microparasites (e.g., Haemoproteus, Marek’s disease (31%) (Go denker et al. 2005). microfi lariae, Trypanosoma, avipoxvirus) obtained Chickens interact closely with wild birds, and from avian blood, swabs, or biopsy are identifi ed these parasites infect wild relatives of Galápagos by extracting DNA (host and parasite) from host endemics elsewhere (Dubey 2002, Forrester and tissue samples (e.g., blood or skin biopsies) and PCR- Spalding 2003). Clearly, domestic chickens har- amplifying loci used to test for presence or absence bor pathogens, but the threat that these pose to (and then to calculate prevalence). Additionally, the the endemic avifauna is unclear. The population amplicons from a subset of positive samples from of introduced Rock Pigeons on the island of San each avian population are sequenced using standard Cristobal harbored Trichomonas (44%) in 2002 techniques (e.g., cytochrome-b oxidase mitochondrial DNA [mtDNA] for haemoproteids; Fallon et al. 2003). (Padilla et al. 2004). Chickens on Santa Cruz and Macroendoparasites are extracted using a method San Cristobal habor fowlpox virus identical to similar to the above when possible (preserving a part that from chickens elsewhere (Thiel et al. 2005). of the parasite as a voucher). All specimens are labeled fully and deposited in the appropriate institutions. E i r h Representatives of all lineages are deposited into the invertebrate collection at the Charles Darwin Research We have sampled >3,100 birds from 17 native Station aV er all data have been collected (e.g., DNA bird species from 13 islands (important fi ndings sequencing, morphometrics, photographs). summarized in Table 1). The 17 species have Public databases, such as GenBank, have proved highly useful for obtaining outgroups for phylo- been sampled in 36 island populations (see genetic analyses, and we have relied on the use of Table 1). Of these 36, 18 also have been sampled the BLAST search option on the National Center for ectoparasites. These 36 island populations, for Biotechnology Information (NCBI) server to for which at least 20 individuals have been sam- determine quickly and roughly the identities of the pled, represent 22.5% of the 160 island popula- parasite lineages recovered within Galápagos taxa tions of all seabirds and landbirds endemic at (e.g., trypanosomes, haemoproteids, avian skin the species or subspecies level. Other endemics mites, Phthiraptera). Eventually, our goal is to cre- are represented by single specimens on which ate a public database of all DNA sequences obtained necropsy results are reported (e.g., Blue-footed from exemplars of all parasite taxa studied within Booby [Sula nebouxii] and Brown Pelican the Galápagos Islands, with all available data on host, habitat, and collection information linked to [Pelecanus occidentalis]). In most species, previ- the sequences, which will allow rapid determina- ously undescribed or new host records of previ- tion of whether a given parasite has been recovered ously known parasites were recovered (Table 1); previously from a given host and locality. Thus, we in a few cases, results for particular focal species can quantify the large amount of parasite diversity revealed no remarkable fi ndings. For example, July 2006] Perspectives in Ornithology 629 ) ); ); d taxa sp. sp. sp.
e not been ) ) ); sp. aci aci aci ) Nematoda sp.; Trematoda Trematoda sp. ilariae ilariae sp. ( ) ); Und. ) sp. ( sp. ( Haemoproteus Trypanosoma Haemoproteus Haemoproteus Haemoproteus Haemoproteus microfl
Nematoda Haemoproteidae Haemoproteidae Nematoda Kinetoplastidae Haemoproteidae Nematoda Renicola Contracecum Renicola Und. microfl ( Haemoproteus Chlamydophila psi ( Und. ( Chlamydophila psi Chlamydophila psi Contracecum Und.
: ) );
)
,
—
( , Acari
).
Argasidae
Phthiraptera ( sp. Und.
sp. ( Epidermoptidae S. mendiculus
sp. ( sp.
) , Und. ). Microlynchia Olfersia sordida
Spheniscus demersus ) and may represent a ); ); ) Hippoboscidae ( Piagetiella Colpocephalum turbinatum Columbicola macrourae Pectinopygus Austrogoniodes demersus. Austrogoniodes
: : : : : Ornithodoros Myialges caulotoon
: : Phthiraptera Phthiraptera Phthiraptera Hippoboscidae Epidermoptidae Phthiraptera Insecta Insecta Degeeriella regalis Insecta Physconelloides galapagensis Acari Craspedorrhynchus Myiagles caulotoon Insecta Acari Insecta Icosta nigra Ectoparasites Endoparasites
Esp Fer Flo Gen Isa Mar Pta SCI SCz SFe Sgo SFe SCz Pta SCI Esp Fer Mar Isa Gen Flo ing for ectoparasites (see text).
cent Frigatebird B A A A A Frigatebird B cent Und. on 11 islands. This is not an exhaustive list of known parasites from these birds, but only those from our work. Many birds hav list of known parasites from these birds, but only those our work. on 11 islands. This is not an exhaustive sampled using dust-ruffl Booby Endemic subspecies Blue-footed (2005). A A A A A Magnifi al. Pelican et Brown Banks A A A A see A A ( ( Galápagos Penguin C C C C C C Penguin C Galápagos been has species this that from on Note reported species ( cryptic (
Landbirds: Endemic species Galápagos Hawk C C C C C C C ( ( ( ( Swallow-tailed Gull Gull A A A A Swallow-tailed A A B A A A A Und. Tfgq 1. Endemic Galápagos birds sampled and parasites recovered. We have sampled 9 endemic seabird taxa and 25 landbir have We 1. Endemic Galápagos birds sampled and parasites recovered. Tfgq Galápagos Dove ( C A A C A A A C C C C Waved Albatross Albatross Endemic seabirds C B C Waved Cormorant Flightless
Islands 630 Perspectives in Ornithology [Auk, Vol. 123 ) ); UnID Contracecum ; ; ; UnID
Nematoda Chlamydiaceae Avipoxvirus Avipoxvirus Avipoxvirus Avipoxvirus Avipoxvirus Avipoxvirus Avipoxvirus sp.
sp. Canarypox-like ). ( except for domestic birds and occasional migrants). s. C =same as B, plus ectoparasite collections.
n Cristobal, SCz = Santa Cruz, Sfe Fe, and Sgo Myrsidea Myrsidea
) Canarypox-like sp., sp., ) ) Acari Hippoboscidae (
) ed beyond family or genus). B = breeding population for which we have have family or genus). B = breeding population for which we ed beyond Brueelia Brueelia
: : : UnID feather mite Phthiraptera Phthiraptera Astigmata Insecta Insecta galapagensis Acari ( Ectoparasites Endoparasites ed (not identifi ) ) Esp Fer Flo Gen Isa Mar Pta SCI SCz SFe Sgo SFe SCz Pta SCI Esp Fer Mar Isa Gen Flo ) ) ) ) ) ) ) ) ) ) ) Camarhynchus crassirostris Camarhynchus G. fuliginosa G. fortis G. magnirostris G. conirostris continued Geospiza scandens Note: Only populations of endemic species or subspecies are included. This selection comprises most the land birds ( Isa = Isabela, Mar Marchena, Pta Pinta, SCI Sa Islands: Esp = Española, Fer Fernandina, Flo Floreana, Gen Genovesa, Abbreviations: A = breeding population; Und. undescribed (new species); UnID: Unidentifi A Abbreviations: ( sp. coccidian Endemic subspecies Warbler Yellow A B A A A A B A A A A ( Canarypox-like Mockingbird Hood B causing infection; protozoan coccidian systemic UnID ( Galápagos Mockingbird B B A B B B B A A B B B Mockingbird A B Galápagos ( Santiago. Tfgq 1. Continued. Tfgq Islands Vegetarian Finch A A A A B A UnID mites ( Finch mites Vegetarian UnID A A B A A A coccidian UnID Small Ground Finch Ground Small A A A A B A A A A A ( Canarypox-like Medium Ground Finch A A A B A A A A A Finch Ground Medium ( Canarypox-like Large Ground Finch ( A B A B A Canarypox-like Large Cactus Finch ( A A B Galápagos Dove Dove Galápagos ( Finch Cactus ( A A B A A A A A Canarypox-like information. in bold are either known to be endemic the archipelago or likely based on available Parasites swab sampled ≥20 individuals, taking blood samples, making smears, plasma or serum, and cloacal, choanal conjunctival July 2006] Perspectives in Ornithology 631 the single breeding population of Waved number of Galápagos Penguins and Flightless Albatross contained no remarkable fi ndings, Cormorants tested positive for apicomplexan which allows us to characterize normal ranges blood parasites by PCR, though none has been for plasma chemistry, serology, and hematology positively identifi ed on smears in either species. (Padilla et al. 2003). In other cases, we were bet- The genetic relationships among Apicomplexan ter able to characterize pathogens previously blood parasites are under study, assessing known to be present, such as Avipoxvirus (see whether there has been a radiation of blood below). Major pathogen fi ndings are summa- parasites on these isolated islands. rized briefl y here in broad categories. Kinetoplast blood parasites.—We recovered a species of Trypanosoma of unknown identity Bq i Pfwf in Galápagos Hawks of Santiago Island. We sequenced a small region of the small sub- Nematodes.—In collaboration with Hernan unit ribosomal DNA (ssu rDNA) gene from Vargas, 448 Flightless Cormorants and 330 bird-blood-derived DNA (Maslov et al. 1996), Galápagos Penguins were censused and sam- and a BLAST search on GenBank showed that pled on four trips over two years throughout this species is closely related to other raptor- the ranges of both species. Prevalences of what derived Trypanosoma species (J. Merkel and appears to be the same nematode microfi - N. K. Whiteman pers. comm.). We do not know larid (based on morphological evidence; H. I. its distribution or prevalence. Jones pers. comm.) were ∼0.50 for Flightless Other endoparasites and poxviruses.— Cormorant and lower, but still signifi cant, for Opportunistic necropsies of seabirds revealed Galápagos Penguin (J. Merkel pers. comm.; trematodes (Renicola), unidentifi ed coccidians, Travis et al. 2006a, b). We are pursuing genetic and in Galápagos Doves on one island, antibod- studies of these nematodes. Preliminary sequence ies of Chlamydophila psi aci (24% on Española, data from the COI locus, which has been shown 6% overall; Padilla et al. 2004). Chlamydophila to reliably diagnose nematode species (Blouin et psi aci antibodies were also detected at high al. 1998), revealed identical sequences between prevalence in Galápagos Penguin; lower preva- microfi larids obtained from blood samples of lences of C. psi aci in the sympatric Galápagos Galápagos Penguins and Flightless Cormorants, Cormorant may have refl ected the diff erent corroborating the morphological data. The results testing methodologies used. Chlamydophila of a BLAST search of the sequences were conclu- DNA was detected in several cormorants, sive. All the most similar sequences in GenBank but in no penguins (Travis et al. 2006a, b). to the two submi ed were fi larial nematode COI Histopathology of cutaneous lesions from sequences, although the two Galápagos-derived chickens, Yellow Warblers, and ground fi nches sequences were unique and diff ered from all (Geospiza spp.) revealed inclusion bodies diag- others in GenBank by ∼10% pairwise genetic nostic of Avipoxvirus spp. Our characterization distance. Nematodes of the genus Contracecum of the poxvirus in endemic passerine birds were also found in a Blue-footed Boobies, Brown revealed two variants very closely related to Pelicans, and Yellow Warblers (Dendroica pete- canarypox virus, whereas domestic chickens on chia) sampled opportunistically. the islands are infected with the distinct fowl- Apicomplexan blood parasites.—We observed pox virus (Thiel et al. 2005). This suggests that Haemoproteus in peripheral blood smears from the poxvirus did not “jump” from chickens to three of four species of Genovesa Island seabirds the endemic birds. Canarypox variants may also (two endemic), as well as in the sympatric and be endemic, perhaps arriving with avian colo- endemic Galápagos Dove. Prevalences were 7 of nists that gave rise to the endemic Galápagos 24 (29%) for Great Frigatebirds (Fregata minor), 2 avifauna, or transported by migrant passerines. of 23 (8.7%) for Red-footed Boobies (Sula sula), Recombination analyses, however, indicated and 3 of 19 (15.8%) for Swallow-Tailed Gulls ancient recombination among all strains exam- (Larus furcatus; Padilla et al. 2006). Almost all the ined, which suggests that recombination could 150 Galápagos Doves sampled on six islands had occur among sympatric Avipoxvirus strains in visible infections of a Haemoproteus-like parasite Galápagos Islands. Further phylogeographic (Padilla et al. 2004); prevalence in Galápagos studies of the virus in the endemic birds should Doves was 11 of 26 (42%) on Genovesa. A small clarify its closest relatives on the mainland. 632 Perspectives in Ornithology [Auk, Vol. 123
Ectoparasites.—Four endemic bird species et al. 2000, Marzal et al. 2005) and pathogenic- have been sampled for ectoparasites on 18 ity has been shown for certain hosts of certain island populations (C in Table 1). We have hemoparasite species (Garvin et al. 2003). The recovered Acari of families Epidermoptidae and pathogenicity of these parasites in the seabirds Argasidae, lice of genera Pectinopygus, Piagetiella, and doves sampled, or the eff ects on host fi t- Colpocephalum, Degeeriella, Craspedorhynchus, ness or reproductive success, are unknown. Columbicola, Physconelloides , and hippoboscid However, within Great Frigatebirds, birds fl ies (Olfersia, Icosta, and Microlynchia), as well infected with Haemoproteus-like parasites as undescribed lice and unidentifi ed mites exhibited signifi cantly higher heterophil-to- (Table 1). These parasites vary markedly in lymphocyte concentration ratios than unin- life history and host specifi city in ways that we fected birds (Padilla et al. 2006). In chickens, have investigated in our studies (see below). this ratio increased when birds were exposed Opportunistic samples from other species have to social stress or corticosterone in feed, and it recovered unidentifi ed mites and lice of genera is thus considered to be an indication of envi- Brueelia and Myrsidea. Other researchers have ronmental stress (Gross and Siegel 1983). In our reported ectoparasites from Galápagos birds studies, blood smears from each bird are used as well (e.g., Palma 1995, Madden and Harmon to identify circulating parasites and to conduct 1998, Mironov and Perez 2002, Price et al. 2003, complete cell counts (i.e., heterophils, lym- O’Connor et al. 2005). Extending this sampling phocytes, monocytes, eosinophils, basophils), eff ort to include all endemic bird taxa will and estimate concentrations of overall leuko- recover many new species and contribute to our cytes, each leukocyte type, and heterophil-to- understanding of the relationships among para- lymphocyte concentration ratios. Haptoglobin, site species as well as ecological relationships an acute phase protein found in birds and between parasites and their hosts. other taxa (Delers et al. 1988), will be quantifi ed using a serum assay available through Tri-Delta E h Pfwf f i O w Pf l Diagnostics (Morris Plains, New Jersey) that we E i r h B wi have used with success. Haptoglobin increases during infl ammatory responses to trauma or Pox-like symptoms have been described infection. Blood chemistries will be quantifi ed in several species and subspecies of endemic through commercial labs (Padilla et al. 2003, birds, including Galápagos Mockingbirds 2004, 2006; Travis et al. 2006a, b). We will com- (Nesomimus parvulus), Galápagos Doves, Yellow pare these measures of response in infected Warblers, and some Galápagos fi nches (Geospiza and noninfected hosts within each species, and spp., Camarhynchus spp.). Most data on the compare these diff erentials between “old” and eff ects of avian pox are from mockingbirds “recent” parasites, as identifi ed in our phylo- (Nesomimus spp.). During the 1982–1983 El geographic studies. For high-prevalence para- Niño event, 56% of Galápagos Mockingbirds sites in particular populations, we will return displaying lesions died on Genovesa, com- to estimate resighting rates of hosts between pared with 39% of asymptomatic individuals years to estimate parasite-related mortality. (Curry and Grant 1989). During the same El Eventually, we and our colleagues would like Niño event on Isla Santa Cruz, 28% of juvenile to experimentally treat nesting nonthreatened Galápagos Mockingbirds exhibited apparent birds (e.g., Great Frigatebirds) with antimalarial pox lesions; young birds without symptoms drugs to determine their ecological cost (e.g., had higher resighting frequencies (72%) than Merino et al. 2000, Marzal et al. 2005). We are those with lesions (0%), which suggested higher presently studying how removing lice from mortality for infected birds (Vargas 1987). Our banded Galápagos Hawks aff ects the hawks’ work has barely begun to consider the health long-term survivorship. consequences of parasites and pathogens on their hosts. Hemoparasites in Haemoproteus R q h B f{ wfq Eh q l~ have been traditionally considered incidental and relatively nonpathogenic parasites of birds We will also use these results to estimate and reptiles, though eff ects on host fi tness have consequences of parasite infection for other been demonstrated (Earlë et al. 1993, Merino components of fi tness in the endemic avifauna July 2006] Perspectives in Ornithology 633 of Galápagos. These studies will make connec- genetic diversity also have generally lower and tions back to our original interests in behavioral less variable natural antibody titres and higher characteristics of island fauna. We will ask, for ectoparasite loads than larger, more genetically example, whether parasite infection aff ects the variable island populations (Whiteman et al. red coloration of the Red-footed Booby’s (S. Sula) 2006). This reinforces the hypothesis that extinc- feet, and whether this, in turn, aff ects mating tion risk of island endemics is a ributable to success (P. Baiao pers. comm.). We know that the mechanisms associated with reduced genetic high prevalence of adenovirus seropositivity in diversity (Frankham 1996). Because of this the Waved Albatross is not related to their pair- fi nding, we recommended that the Galápagos ing or reproductive success (K. P. Huyvaert pers. National Park consider further restricting tourist comm.), but we are aware that some of these visitation to the more isolated smaller islands, disease organisms may have adverse fi tness given that Galápagos Hawks on those islands are consequences for their hosts in a manner that is likely more susceptible to invasive diseases that mediated through behavioral mechanisms such may enter the archipelago. as pairing success or foraging effi ciency, even Parasites that are not directly aff ected by when direct eff ects on morbidity are diffi cult to host immune function reveal other aspects of assess. For example, we have studied the ecto- the host–parasite interaction. Degeeriella regalis parasitic lice Degeeriella regalis and Colpocephalum is a feather louse that occurs, within the islands, turbinatum of the endemic Galápagos Hawk. only on Galápagos Hawks. On the mainland, it Number of lice per infected host correlates nega- occurs with regularity only on the Galápagos tively with body condition and predicts territory Hawk’s putative sister species, the Swainson’s status, such that nonterritorial birds carry higher Hawk (B. swainsoni; Riesing et al. 2003). This parasite loads and are in poorer condition than parasite is likely transmi ed vertically between territorial birds, even aV er controlling for age host individuals (Whiteman and Parker 2004a), (Whiteman and Parker 2004a). New data sug- transferring between parents and off spring gest that newcomers to polyandrous Galápagos during brooding. Comparative molecular data Hawk breeding groups on Santiago have signifi - (N. K. Whiteman et al. unpubl. data) suggest cantly more lice than birds that have resided in that the parasite’s mtDNA was diversifying the territories for at least one year, which is likely more quickly than the host’s under an island correlated with the newer birds’ recent status model of speciation (Hafner and Nadler 1990). as nonterritorial individuals (N. K. Whiteman We conservatively estimated that the Galápagos et al. unpubl. data). In addition, the intensity Hawk split from its common ancestor with of infection with the horizontally transmi ed the Swainson’s Hawk <200,000 years BP and louse, C. turbinatum, varied positively with size is, thus, the youngest known endemic bird of the infected Galápagos Hawk’s social group, lineage with the Galápagos Islands (Bollmer and intensity was signifi cantly more similar et al. 2006). The signature of a population within groups than between groups. This was bo leneck in the hawk lineage is seen at rap- not true for the vertically transmi ed D. regalis idly evolving nuclear minisatellite loci, which (Whiteman and Parker 2004b). Colpocephalum are nearly fi xed within and diff erent between turbinatum is the same louse that is useful for island populations of the Galápagos Hawk indicating relative immune function of diff erent (Bollmer et al. 2005) and in the mtDNA haplo- populations, because it encounters the immune type network, which shows very li le polymor- system when it feeds on skin and growing feath- phism, yet high structure (Bollmer et al. 2006). ers. We asked whether genetic diversity, parasite However, the parasite mtDNA network shows load, and immune function were related across much more structure between and variability all the breeding populations of the Galápagos within island populations (N. K. Whiteman et Hawk, employing our quantitative sampling al. unpubl. data). Because it is vertically trans- of C. turbinatum, estimates of island-population mi ed and highly host-specifi c, such parasites genetic diversity (Bollmer et al. 2005), and tests act as rapidly evolving “markers” that provide of natural constitutive antibodies (Matson et al. more insight into host history than we can get 2005) run on banked serum samples from the from the hosts themselves. The parasite net- same individuals. We found that island popula- work reveals aspects of host history (which tions of Galápagos Hawks with extremely li le haplotypes are derived from which ancestral 634 Perspectives in Ornithology [Auk, Vol. 123 haplotype), and we used this logic as a new and Galápagos Hawks diff ered signifi cantly rationale for parasite conservation (Whiteman genetically even in areas where those two and Parker 2005). species co-occurred (e.g., Isla Fernandina). Surprisingly, our parasite surveys are among Our collaborator and expert on the Acari, H. the fi rst to examine parasite diversifi cation Klompen, found consistent morphological within the Galápagos Islands, and the data diff erences between the series from each host, gathered by our biotic inventory will be of use demonstrating the reciprocal illumination with to scientists for decades. Our ongoing work morphological and molecular data to uncover will continue to uncover parasite lineages new new parasite lineages. to science. For example, there are no published Disease epidemics have been implicated in reports of Phthiraptera from the following the local and global extinctions of endangered endemic birds, though each is a likely host to at species (van Riper et al. 1986, Thorne and least one species (Price et al. 2003): Lava Gull (L. Williams 1988, Laurance et al. 1996). Island fuliginosus), Galápagos Rail (Laterallus spilono- populations may be particularly infl uenced tus), eight species of Darwin’s fi nches (Geospiza by introduced pathogens because of their spp.), three mockingbird species (Nesomimus evolution in isolation, low levels of genetic spp.), Galápagos Martin (Progne modesta), heterogeneity, and increased population densi- Galápagos subspecies of the Short-eared Owl ties, all of which increase their susceptibility to (Asio fl ammeus), and others. Although two new diseases and disease transmission among species of lice were reported previously from individuals. Also, island populations naturally the Galápagos Hawk (de Vries 1973), our tend to be small, making them more vulner- sampling (aV er receiving a tip from R. Palma) able to extinction. In addition, the parasites revealed that a previously undetected head themselves are of extreme intrinsic value and louse, Craspedorrhynchus sp. (all in this genus interest. This partnership is describing the are specifi c to raptors), which occurred in all prevalence of parasites in terrestrial bird spe- island populations sampled, likely represents cies and seabirds on the Galápagos Islands, an endemic lineage. The detection of cryptic assessing the history and origin of those para- diversifi cation within the Galápagos Islands, in site lineages, and beginning to assess the rela- addition to new species or new records, is cer- tive eff ects of recent and historical parasites on tain. For example, an epidermoptid skin mite (a their hosts. In addition, we can use the empiri- member of a family in which no DNA sequence cal clinical data on health of individuals to data existed before our preliminary study), inform our behavioral-ecology studies of mate Myialges caulotoon, was previously reported choice, territory acquisition, reproductive suc- from Flightless Cormorants and Galápagos cess, and pa erns of movement. These results Hawks, both Galápagos endemics (Madden may contribute importantly to other conser- and Harmon 1998). These mites have caused vation eff orts in other parts of the world. The signifi cant mortality in wild birds elsewhere, results will also contribute a new dimension including an island endemic (Gilardi et al. to the role that the Galápagos archipelago has 2001). Previously, however, only one specimen served as evolution’s laboratory by revealing was collected from a Flightless Cormorant, the diversity of parasites that have evolved and only morphological characters were used there, and are enabling us to begin quantify- to identify these mites (Madden and Harmon ing the eff ects of both endemic and introduced 1998). Female mites of the genus Myialges are parasites and pathogens. obligately vectored by hippoboscid fl ies or On a fi nal, personal note, it is clear to each large chewing louse species (Fain 1965) and participant in this program that the combined oviposit only on the insects. However, diff erent perspectives of population biology, behavioral species of fl ies infest Flightless Cormorants and ecology, and veterinary science have greatly Galápagos Hawks (Maa 1963, N. K. Whiteman enhanced the rigor and reach of our research, et al. unpubl. data). Thus, we hypothesized and have made each of us a be er scientist. that gene fl ow of the mites between avian The authors of this paper include a behavioral– hosts was limited given the host-specifi city molecular ecologist (P.G.P.), an entomologist of their fl y vectors. We showed that individu- turned population biologist (N.K.W.), and a als of Myialges from Flightless Cormorants veterinarian and zoo administrator (R.E.M.). July 2006] Perspectives in Ornithology 635
In coming to understand one another, we have B qqr w, J. L., R. T. K rgfqq, N. K. W rf , each grown immeasurably, and we will forever J. H. Sfwf qf, f i P. G. Pfwp w. 2006. see our work, however it develops, in a much Phylogeography of the Galápagos Hawk: broader way. A recent arrival to the Galápagos Islands. Molecular Phylogenetics and Evolution 39: Ahp |q ilr 237–247. B qqr w, J. L., N. K. W rf , M. D. Cf , This work was supported by the National J. C. B i fw, T. i Vw , f i P. G. Pfwp w. Science Foundation, National Geographic 2005. Population genetics of the Galápagos Society, Saint Louis Zoo’s WildCare Institute Hawk (Buteo galapagoensis): Genetic mono- and Field Research for Conservation Programs, morphism within isolated populations. Auk Des Lee Zoological Collaborative, Oklahoma 122:1210–1224. City Zoo, Sigma Xi, and the International Bw | , P., R. G. W qq, R. Bwfiq ~, D. M. A w, Center for Tropical Ecology at the University f i L. D | q w. 2001. Bovine spongiform of Missouri-St. Louis (UMSL). Our partners encephalopathy and variant Creutzfeldt- in the fi eld are the Charles Darwin Research Jakob disease: Background, evolution, and Station and the Galápagos National Park. We current concerns. Emerging Infectious thank S. Goodman, V. Cedeno, and M. Cruz Diseases 7:16–17. of the Galapagos Genetics, Epidemiology, and C w , D. M., R. A. Dz hf , A. R. MhB w ~, Pathology Laboratory for their participation M. A. R h fwi , W. M. W , K. S. Hfwuu, f i and the use of laboratory facilities. We espe- C. G. F }. 1992. Drowned islands downstream cially appreciate the collaboration of H. Vargas, from the Galapagos hotspot imply extended T. de Vries, V. Cedeno, M. Cruz, D. Cruz, and G. speciation times. Nature 355:246–248. Jimenez on the Galápagos, and of C. Soos, N. Cwz hp f p, R. H., K. P. J , V. S. Sr , Go denker, T. Walsh, E. Travis, L. Padilla, M. R. J. Aifr , D. H. Cqf~ , f i R. D. Duncan, and J. Merkel at the Saint Louis Zoo. Pfl . 2001. Phylogenetic analysis of par- At UMSL, we thank collaborators J. Bollmer, tial sequences of elongation factor 1 alpha D. Santiago-Alarcόn, P. Baiao, I. Levin, K. identifi es major groups of lice (Insecta: Huyvaert, K. Matson, T. Thiel, and R. Ricklefs. Phthiraptera). Molecular Phylogenetics and Field help was provided by J. Rabenold, S. Bahr, Evolution 19:202–215. G. Buitron, P. Sanchez, A. Iglesias, J. Carlos Czww~, R. L., f i P. R. Gwf . 1989. Demography Valarezo, R. Wright, B. Allen, C. McWilliams, of the cooperatively breeding Galapagos B. Nims, R. Campbell, and V. Dosanjh. Experts Mockingbird, Nesomimus parvulus, in a cli- who have contributed importantly include B. matically variable environment. Journal of Sinclair, H. Klompen, G. Valkiunas, H. Jones, R. Animal Ecology 58:441–463. Sehgal, and E. Greiner. Df fp, P., A. A. Cz l fr, f i A. D. H~f . 2000. Emerging infectious diseases L wf zw C i of wildlife—Threats to biodiversity and human health. Science 287:443–449. A~fqf, S. C., f i R. Hz h l . 1974. D r, S. L., W. B. Kfw , f i W. W rf . Hemogregarines (Protozoa: Sporozoa) 2001. Pu ing theory into practice: Wildlife as zoogeographical tracers of Galapagos health in conservation. Conservation Biology Island lava lizards and marine iguanas. 15:1224–1233. Herpetologica 30:128–132. D q w , F., G. S w hp w, f i R. E lq w. 1988. Bf p , J. C., R. L. Pfqrf, f i A. M. Pf w . Glycosylation of chicken haptoglobin: Isola- 2006. Cophylogenetic relationship between tion and characterization of three molecular penguins and their chewing lice. Journal of variants and studies of their distribution Evolutionary Biology 19:156–166. in hen plasma before and aV er turpentine- Bq z , M. S., C. H. Y | qq, C. H. C zw ~, induced infl ammation. Biochemistry and f i J. B. Dfr . 1998. Substitution bias, Cell Biology 66:208–217. rapid saturation, and the use of mtDNA for i Vw , T. 1973. The Galápagos Hawk: An eco- nematode systematics. Molecular Biology geographical study with special reference to and Evolution 15:1719–1727. its systematic position. Ph.D. dissertation, 636 Perspectives in Ornithology [Auk, Vol. 123
Vrij e Universiteit te Amsterdam, Amsterdam, Gfw{ , M. C., B. L. H r w, f i E. C. Gw w. The Netherlands. 2003. Pathogenicity of Haemoproteus D g , A. P. 1988. Restoring island ecosys- danielewskyi, Kruse, 1890, in Blue Jays tems: The potential of parasites to control (Cyanoci a cristata). Journal of Wildlife introduced mammals. Conservation Biology Diseases 39:161–169. 2:31–39. G gg , J. P., H. L. S qq, f i C. E. Cfz . 1999. D g , A. P., f i R. M. Mf~. 1986. Pa erns of Eff ective monitoring for adaptive wildlife invasions by pathogens and parasites. Pages management: Lessons from the Galápagos 58–76 in Ecology of Biological Invasions of Islands. Journal of Wildlife Management 63: North America and Hawaii (H. A. Mooney 1055–1065. and J. A. Drake, Eds.). Springer-Verlag, New G qfwi , K. V. K., J. D. G qfwi , A. Fwf p, M. L. York. G , f i W. M. B ~h . 2001. Epidermoptid Dzg ~, J. P. 2002. A review of toxoplasmosis mange in Laysan Albatross fl edglings in in wild birds. Veterinary Parasitology 106: Hawaii. Journal of Wildlife Diseases 37: 121–153. 185–188. Efwq, R. A., S. S. Bf f qq , G. F. B , G i p w, N., T. Wfq , H. Vfwlf , M. f i R. C. Kw h p. 1993. Histopathology Dz hf , J. M wp q, G. J r , R. E. M qq w, and morphology of the tissue stages of M. Df q ~, f i P. G. Pfwp w. 2005. Assessing Haemoproteus columbae causing mortality in the risks of introduced chickens and their Columbiformes. Avian Pathology 22:67–80. pathogens to native birds in the Galápagos E hfqf , A. A., D. E. Fw qf i, W. E. Archipelago. Biological Conservation 126: C qq , f i A. A. Lfq. 1998. The evolution 429–439. of primate malaria parasites based on the G ×~ i B qq hv, J., S. M wf i, f i C. F q z. gene encoding cytochrome b from the lin- 2002. Pa erns of parasite species richness of ear mitochondrial genome. Proceedings of Western Palaearctic micro-mammals: Island the National Academy of Sciences USA 95: eff ects. Ecography 25:173–183. 8124–8129. Gwf , P. R., R. L. Czww~, f i B. R. Gwf . Ff , A. 1965. A review of the family 2000. A remnant population of the Floreana Epidermoptidae Trouessart parasitic on Mockingbird on Champion Islands, the skin of birds (Acarina: Sarcoptiformes). Galápagos. Biological Conservation 92: Verhandelingen van de Koninklij ke Vlaamse 285–290. Academie voor Wetenschappen, Li eren Gw , W. B., f i H. S. S l q. 1983. Evaluation en Schone Kunsten van Belgie. Klasse der of the heterophil/lymphocyte ratio as a mea- Wetenschappen, no. 84, 27. sure of stress in chickens. Avian Diseases 27: Ffqq , S. M., E. B wr l fr, f i R. E. 972–979. R hpq . 2003. Island and taxon eff ects in Gzqqf i, F. M. D. 1995. Impact of infectious dis- parasitism revisited: Avian malaria in the eases on wild animal populations: A review. Lesser Antilles. Evolution 57:606–615. Pages 20–51 in Ecology of Infectious Diseases F ww w, D. J., f i M. G. Sufqi l. 2003. in Natural Populations (B. T. Grenfell and Parasites and Diseases of Wild Birds A. P. Dobson, Eds.). Cambridge University in Florida. University of Florida Press, Press, Cambridge, United Kingdom. Gainesville. Hf w, M. S., f i S. A. Nfiq w. 1990. Fwf p fr, R. 1996. Relationship of genetic Cospeciation in host–parasite assemblages: variation to population size in wildlife. Comparative analysis of rates of evolu- Conservation Biology 10:1500–1508. tion and timing of cospeciation events. Fw i, M., R. G. MhL f , f i F. J. D . 2001. Systematic Zoology 39:192–204. Disease emergence in birds: Challenges for H g w , P. D., N. A. C~| pf, S. L. Bfqq, f i the twenty-fi rst century. Auk 118:290–303. J. R. i Wffwi. 2003. Biological identifi ca- Fw r , E., L. M w{ qq w , M. Aw , f i tions through DNA barcodes. Proceedings D. P w. 2001. Parasite richness and of the Royal Society of London, Series B 270: abundance in insular and mainland feral 313–322. cats: Insularity or density? Parasitology 123: K h l, R. P. 1999. Foot-and-mouth disease: Cur- 143–151. rent world situation. Vaccine 17:1772–1774. July 2006] Perspectives in Ornithology 637
Lf h , R. S., J. T. R w l, V. D zg q, J. O’C w, B. M., J. F z u zq , D. L u , Sr , M. Pfwp w, K. S q , B. Cw , K. E. f i K. L i w¾r. 2005. Mites associated V qu , M. B. Cwfg w , J. H. Sh ww , f i with the small ground fi nch, Geospiza fuligi- w . 1999. Origin of the West Nile virus nosa (Passeriformes: Emberizidae), from the responsible for an outbreak of encephalitis Galapagos Islands. Journal of Parasitology in the northeastern United States. Science 91:1304–1313. 286:2333–2337. Pfi qqf, L. R., K. P. Hz~{f w , J. F. M wp q, R. E. Lfzwf h , W. F., K. R. MhD fqi, f i R. M qq w, f i P. G. Pfwp w. 2003. Hema- Su fw . 1996. Epidemic disease and the tology, plasma chemistry, serology, and catastrophic decline of Australian rain forest Chlamydophila status of free ranging adult frogs. Conservation Biology 10:406–413. waved albatrosses (Phoebastria irrorata) on L | , J. W. 1968a. Studies on the helminth Española, Galápagos Islands. Journal of Zoo parasites of the long-tailed fi eld mouse, and Wildlife Medicine 34:278–283. Apodemus sylvaticus sylvaticus from Wales. Pfi qqf, L. R., D. Sf fl , J. F. M wp q, R. E. Journal of Zoology (London) 154:287–312. M qq w, f i P. G. Pfwp w. 2004. Survey for L | , J. W. 1968b. Studies on the helminth Trichomonas gallinae, Chlamydophila psitacci, parasites of voles and shrews from Wales. Salmonella spp. and Haemoproteus organisms Journal of Zoology (London) 154:313–331. in Columbiformes from the Galápagos Mff, T. C. 1963. Genera and species of Islands. Journal of Zoo and Wildlife Hippoboscidae (Diptera): Types, synonomy, Medicine 35:60–64. habitats and natural groupings. Pacifi c Pfi qqf, L. R., N. K. W rf , J. M wp q, K. D. Insects Monographs 6:1–186. Hz~{f w , f i P. G. Pfwp w. 2006. Health Mfii , D., f i W. M. Hfwr . 1998. First assessment of seabirds on Isla Genovesa, record and morphology of Myialges caulotoon Galápagos. Pages 86–97 in Current Topics (Acari: Epidermoptidae) from Galápagos in Avian Disease Research: Understanding hosts. Journal of Parasitology 84:186–189. Endemic and Invasive Diseases (R. K. Barra- Mfwfq, A., F. i L u , C. Nf{fww , f i A. P. clough, Ed.). Ornithological Monographs, MÃqq w. 2005. Malarial parasites decrease no 60. reproductive success: An experimental study Pfqrf, R. L. 1995. A new synonymy and new in a passerine bird. Oecologia 142:541–545. records of Quadraceps (Insecta: Phthiraptera: Mf q {, D. A., J. Lzp , M. J wpz, f i L. Philopteridae) from the Galapagos Islands. S ru . 1996. Phyologeny of trypanosomes New Zealand Journal of Zoology 22:217–222. as inferred from the small and large subunit Pw h , P. W., R. A. H qq fq, f i R. L. Pfqrf. rRNAs: Implications for the evolution of 2003. The chewing lice: World checklist parasitism in the trypanosomatid protozoa. and biological overview. Pages 1–448 in Molecular and Biochemical Parasitology 75: World Checklist of Chewing Lice with 197–205 Host Associations and Keys to Families and Mf , K. D., R. E. R hpq , f i K. C. Kqf l. Genera (R. D. Price, R. A. Hellenthal, R. L. 2005. A hemolysis-hemagglutination assay Palma, K. P. Johnson, and D. H. Clayton, for characterizing constitutive innate Eds.). Illinois Natural History Survey humoral immunity in wild and domestic Special Publication, no. 24. birds. Developmental and Comparative R hpq , R. E., f i S. M. Ffqq . 2002. Immunology 29:275–286. Diversifi cation and host switching in avian M w , S., J. M w , J. J. Sf , f i E. Aww w . malaria parasites. Proceedings of the Royal 2000. Are avian blood parasites pathogenic Society of London, Series B 269:885–892. in the wild? A medication experiment in R l, M. J., L. Kwzhp fz w, A. Gfrfz , Blue Tits (Parus caeruleus). Proceedings of f i E. Hfw l. 2003. Molecular phylog- the Royal Society of London, Series B 267: eny of the genus Buteo (Aves: Accipitridae) 2507–2510. based on mitochondrial marker sequences. M w {, S. V., f i T. M. P w . 2002. Two new Molecular Phylogenetics and Evolution 27: feather mites (Astigmata, Analgoidea) from 328–342. ground fi nches of the genus (Geospiza). Acta Sf fl -Aqfwhό , D., S. M. Tf p q ~, f i P. G. Parasitologica 47:228–234. Pfwp w. 2006. Morphological variation and 638 Perspectives in Ornithology [Auk, Vol. 123
genetic structure of Galápagos Dove (Zenaida Wfq w, B. A., f i D. H. Cqf~ . 1997. Dust- galapagoensis) populations: Issues in conser- ruffl ing: A simple method for quantifying vation for the Galápagos bird fauna. Wilson ectoparasite loads of live birds. Journal of Journal of Ornithology 118: in press. Field Ornithology 68:509–518. Sh , M. E. 1988. The impact of infection and Wfw w, R. E. 1968. The role of introduced disease on animal populations: Implications diseases in the extinction of the endemic for conservation biology. Conservation Hawaiian avifauna. Condor 70:101–120. Biology 2:40–56. W , W. M., A. R. MhB w ~, f i R. A. T q, T., N. K. W rf , A. T wfu , M. I. Dz hf . 1993. Petrology and geochemistry Mfvz w , V. C i , T. Wfq , G. J r , of the Galápagos Islands: Portrait of a patho- f i P. G. Pfwp w. 2005. Characterization of logical mantle plume. Journal of Geophyical canarypox-like viruses infecting endemic Research 98:19533–19563. birds in the Galápagos Islands. Journal of W rf , N. K., S. J. G irf , B. J. S hqf w, Wildlife Diseases 41:342–353. T. Wfq , A. A. Cz l fr, L. D. Kwfr w, T w , E. T., f i E. S. W qq fr . 1988. Disease f i P. G. Pfwp w. 2005. Establishment of and endangered species: The black-footed the avian disease vector Culex quinquefas- ferret as a recent example. Conservation ciatus Say, 1823 (Diptera: Culicidae) on Biology 2:66–74. the Galápagos Islands, Ecuador. Ibis 147: Twf{ , E. K., F. H. Vfwlf , J. M wp q, N. 844–847. G i p w, R. E. M qq w, f i P. G. Pfwp w. W rf , N. K., K. D. Mf , J. L. B qqr w, 2006a. Hematology, serum chemistry, and f i P. G. Pfwp w. 2006. Disease ecology in serology of the Galápagos Penguin in the the Galápagos Hawk (Buteo galapagoensis): Galápagos Islands, Ecuador. Journal of Host genetic diversity, parasites, and natural Wildlife Diseases. In press. antibodies. Proceedings of the Royal Society Twf{ , E. K., F. H. Vfwlf , J. M wp q, N. of London, Series B 273:797–804. G i p w, R. E. M qq w, f i P. G. Pfwp w. W rf , N. K., f i P. G. Pfwp w. 2004a. Body 2006b. Hematology, plasma chemistry, condition and parasite load predict territory and serology of the Flightless Cormorant ownership in the Galápagos Hawk. Condor (Phalacrocorax harrisi) in the Galápagos 106:915–921. Islands, Ecuador. Journal of Wildlife W rf , N. K., f i P. G. Pfwp w. 2004b. Diseases 42:133–141. Eff ects of host sociality on ectoparasite {f R u w, C., III, f i J. M. Sh . 2001. population biology. Journal of Parasitology Limiting factors aff ecting Hawaiian 90:939–947. native birds. Pages 221–233 in Evolution, W rf , N. K., f i P. G. Pfwp w. 2005. Using Ecology, Conservation, and Management parasites to infer host population history: of Hawaiian Birds: A Vanishing Avifauna A new rationale for parasite conservation. (J. M. Sco , S. Conant, and C. van Riper III, Animal Conservation 8:175–181. Eds.). Studies in Avian Biology, no. 22. W rf , N. K., D. Sf fl -Aqfwhό , K. P. {f R u w, C., III, S. G. {f R u w, M. L. G , f i J , f i P. G. Pfwp w. 2004. Diff erences M. Lf wi. 1986. The epizootiology and eco- in straggling rates between two genera logical signifi cance of malaria in Hawaiian of dove lice reinforce population genetic land birds. Ecological Monographs 56: and cophylogenetic pa erns (Insecta: 327–344. Phthiraptera). International Journal for {f R u w, C., III, S. G. {f R u w, f i W. R. Parasitology 34:1113–1119. Hf . 2002. Epizootiology and eff ect of W p q p , M., J. F z u zq , H. Vfwlf , f i H. avian pox on Hawaiian forest birds. Auk S qq. 2004. Galápagos birds and diseases: 119:929–942. Invasive pathogens as threats for island Vfwlf , H. 1987. Frequency and eff ect of pox- species. Ecology and Society 9 [online]. like lesions in Galapagos mockingbirds. Available at www.ecologyandsociety.org/ Journal of Field Ornithology 58:101–102. vol9/iss1/art5.