New Host-Parasite Relationships by Host-Switching
- 579 Downloads
Host-switching is a natural phenomenon that many parasite species undergo as part of their life cycle; some are highly specialized, but others can readily change hosts to what is available in the community. Rapid environmental changes can open opportunities for host-switches that sometimes turn into important human and wildlife diseases. Island ecosystems contain large numbers of immunologically naive endemic species. The Galápagos Islands still have all their avian endemics extant; however, the ongoing introduction of animals to the archipelago could prompt extinctions of some endemics. In our first example, we tell the story of avian haemosporidian research in the Galápagos, which started with a small number of species, including conservation efforts to safeguard the little known endemic Galápagos dove (Zenaida galapagoensis); the work has since expanded to include almost all Galapagos endemics. Our second example will focus on Galápagos penguins (Spheniscus mendiculus) and Flightless cormorants (Phalacrocorax harrisi) infected by microfilariae (larvae of nematode worms). These two seabird species live in small populations mainly on the rocky coasts of Fernandina and Isabela Islands; they can experience devastating losses during El Niño periods due to food shortages. Fortunately, our studies show that despite high prevalence rates of these parasites, little or no health effect has been detected to date in these three avian endemics. Further monitoring and pathogen research is necessary, however, to rule out conservation concerns related to health effects due to the arrival of additional pathogens, or outbreaks of existing pathogens brought on by environmental change.
KeywordsGalapagos endemic birds Haemosporida Nematoda Host-switching Hemoparasites Diptera
Parasitism is the most successful lifestyle on earth; it is estimated that 50% or more of the organisms on the planet are parasites (Poulin 2007). Effects of parasites on host populations and communities can be profound and unpredictable under dynamic circumstances (Hatcher and Dunn 2011). Rapid environmental changes brought about by current human activities are disrupting natural ecological dynamics of both wildlife and their parasites, with unforeseen consequences (Bradley and Altizer 2007; Plowright et al. 2012; Santiago-Alarcon et al. 2015). In particular, land use changes such as agricultural practices and urbanization are among the most worrisome threats to biodiversity conservation and both human and veterinary health (Alberti 2008; Shochat et al. 2010; Aguirre et al. 2012; Hernández-Lara et al. 2017). Most human diseases are zoonotic in origin (i.e., they are derived from domestic and/or wild animals), and many zoonotic diseases are currently emergent threats both locally and globally (Jones et al. 2008). Human encroachment on natural habitats and global trade is rapidly exposing populations of both humans and wild animals to novel parasites that can subsequently develop into pathogens (van Riper et al. 1986; Parker et al. 2006; Alexander et al. 2012; Smith et al. 2012; Suzán et al. 2012; Santiago-Alarcon et al. 2012a). Hence, it is necessary to understand parasite ecological dynamics under the varied array of current environmental changes, in order to be able to predict and prevent parasite host switches that can pose medical and veterinary threats. However, it must be clear that parasites do not only represent negative impacts for their hosts, but they are rather essential components of a healthy functional ecosystem (Hudson et al. 2006; Lafferty et al. 2006, 2008), and deserve to be studied and conserved for their own value (Whiteman and Parker 2005).
In general, host-switching is a natural phenomenon that many parasite species undergo as part of their normal life cycle (e.g., heteroxenous parasites that must pass through two often very different hosts), which has been fine-tuned through time by evolution (Poulin 2007). Many parasites are highly specialized and depend completely on the host species they infect (e.g., lice, Bush and Clayton 2006), but others are more flexible in their preferences and can readily change hosts to what is available in the community (e.g., avian malaria, Ricklefs et al. 2004, Santiago-Alarcon et al. 2014). Rapid environmental changes can open opportunities for host-switches that would otherwise not happen and that sometimes turn into important human and wildlife diseases (e.g., habitat fragmentation, Suzán et al. 2012; wildlife trade, Smith et al. 2012; urbanization, Kilpatrick et al. 2006). For the Galápagos Islands, the most important conservation challenges are posed by an increasing human population and transport (aerial and maritime); the latter is one of the most important reasons for the introduction of pathogens (e.g., avian malaria) into the Hawaiian Islands, which created severe conservation and health problems for the endemic birds (e.g., Drepanididae, van Riper et al. 1986, Atkinson et al. 2000). Nonetheless, host-switches do not necessarily imply disaster for host health and host populations, but rather they are also the way for the development of new associations through adaptive evolution (e.g., aggressive symbiosis hypothesis, Ryan 2009). For example, the endemic Hawaiian bird amakihi (Hemignathus virens) has recolonized the lowland areas of the Island of Hawaii, even though avian malaria (Plasmodium relictum) is highly prevalent and there is year-round transmission; amakihi individuals still get infected but they experience low-intensity chronic infections, suggesting that this host-parasite interaction has developed into a more benign association (Woodworth et al. 2005). Thus, the lesson is that host-switching events must be studied in a case-by-case scenario, because many host-parasite associations may not respond in an anticipated manner.
Island ecosystems contain large numbers of endemic species, often with small isolated populations, which are often immunologically naive to pathogens, putting them at greater risk than their mainland counterparts (Frankham 1996, 1997, 1998; Szabo et al. 2012). Parasites make their way around the world by natural means, such as with migratory animals, and Galapagos is no exception to this mode of arrival (e.g., Levin et al. 2013, 2016). But avian species in the Galapagos Islands face additional anthropogenic threats due to oil spills, tourism, human population growth, and global climate change (Matamoros et al. 2006). Furthermore, introduction of hemoparasites is a factor that can lead to island extinctions, such as those that have occurred in Hawaiian endemic birds (Warner 1968; van Riper et al. 1986) and endemic mammals on Christmas Island (Wyatt et al. 2008). The Galapagos Islands still have all their endemic avian species extant; however, increasing travel to the islands places endemic species at risk of introduced pathogens (Wikelski et al. 2004; Parker et al. 2006), which are more likely to arrive via non-native avian species such as chickens (Soos et al. 2008) and insect vectors (e.g., Culex quinquefasciatus, a competent vector of avian malaria, Whiteman et al. 2005). The ongoing introduction of plants and animals to the Galápagos archipelago must be carefully investigated; fortunately, efforts are being made to combat such problems (Cruz et al. 2005; Campbell et al. 2004; Parker et al. 2006).
Our collaborative multiyear project (16+ years) between the Galapagos National Park (GNP), University of Missouri-St. Louis (UMSL), Charles Darwin Foundation (CDF), and the Saint Louis Zoo (SLZ) works to identify and mitigate the impact of pathogens on Galápagos avian endemics. Prior to our work on the Galapagos Islands, only two other studies had examined parasite presence in Galapagos columbiform birds, where Trichomonas gallinae was found infecting non-native rock pigeons (Columba livia, Harmon et al. 1987) and a new coccidian parasite (Eimeria palumbi) was described from an infected adult of the endemic Galapagos dove (McQuistion 1991). Since the year 2001, we have found haemosporidian parasites in several endemic Galapagos birds (Santiago-Alarcon et al. 2010; Levin et al. 2009, 2011, 2013), trypanosomes in a Galapagos hawk (pers. obs. Merkel), and microfilariae in flightless cormorants and Galapagos penguins, which were originally reported by Harmon et al. (1985) (Merkel et al. 2007), as well as many other viruses, bacteria and ectoparasites in a number of endemic and introduced birds. In addition, we were able to add to the body of literature that refutes the paradigm of a paucity of hemoparasites in seabirds (Greiner et al. 1975; Quillfeldt et al. 2011), which states that blood parasites are rare in seabirds because insect vectors would not find suitable habitats in oceanic islands with little fresh water and high winds; however, our efforts to trap mosquitoes have yielded high numbers even in coastal areas that appeared inhospitable to mosquitoes (Merkel, pers. obs.). Thus, we have found Plasmodium parasite lineages in penguins (Levin et al. 2009, 2013), and Haemoproteus parasite lineages infecting red-footed boobies, Nazca boobies, swallow-tailed gulls, magnificent frigate birds, and great frigate birds (Padilla et al. 2006; Levin et al. 2011).
Our second example will focus on Galapagos penguins and flightless cormorants (Figs. 7.1b, c) living in small breeding colonies on the rocky coasts of the Galapagos, mainly on Fernandina and Isabela Islands. These species can experience devastating losses during periods of El Niño because the rich upsurging waters normally brought by the Humboldt Current come to a halt, making food scarce for sea birds in Galapagos during those periods (Valle 1995; Vargas et al. 2005). Both species of birds were discovered to harbor a microfilarial parasite, potentially from the genus Paronchocerca, which has been previously reported to infect a Galapagos penguin in captivity and Anhinga (Anhinga anhinga), this last species closely related to cormorants (Chabaud and Ball 1964). Paronchocerca spp. often infect species that inhabit the shoreline (Bartlett 2008). It is currently unclear whether this is a case of host-switching or just a parasite with a broad host distribution; however, known Paronchocerca spp . are confined within bird families and are not previously reported to switch between families (Bartlett 2008). Filarids have been found in many species of birds with a wide range of pathogenicity, ranging from non-pathogenic to fatal (Simpson et al. 1996). Studies have demonstrated that concurrent infection with more than one hemoparasite may increase the likelihood of pathogenic effects (Davidar and Morton 2006) and cause changes in life history patterns such as decreased parental investment and poor body condition (Merino et al. 2000). In the case of Galapagos penguins this is especially worrisome as this population is also infected with Plasmodium parasites. Penguins in captivity are known to be sensitive to avian malaria, often resulting in fatal cases (Graczyk et al. 1994). Hence, it is a conservation priority to determine if parasites are native or recent arrivals to island bird faunas (i.e., host switches) via non-native species.
7.2 Case Studies
7.2.1 The Galapagos Dove (Zenaida galapagoensis) and Haemoproteus parasites
We later sampled sea birds and realized that they were infected by Haemoproteus haplotypes that were closely related to the newly described dove parasite, but they were also infected by a unique clade of Haemoproteus parasites that was later re-described as H. iwa (Fig. 7.4b; Levin et al. 2011). Closely related lineages between endemic doves and different species of sea birds were suggestive of recent host-switches between those two groups of non-passerine birds. Host-switches in this parasite group must be mediated by competent dipteran vectors (Santiago-Alarcon et al. 2012b); in the present case, the putative vectors are three species of louse flies (Hippoboscidae: Olfersia spinifera and Olfersia aenescens parasitizing sea birds and Microlynchia galapagoensis parasitizing endemic doves), a group of blood-sucking flies that do not have specialized host preferences (e.g., Ibáñez-Bernal et al. 2016). Haemosporidian parasites found infecting doves and sea birds belong to the sub-genus Haemoproteus (Haemoproteus), which is a group that seems to be specialized on non-passerine birds, but that has parasites lineages/haplotypes that appear to readily switch among non-passerine hosts, even hosts that are not closely related (Santiago-Alarcon et al. 2014). For example, H. iwa and H. jenniae are closely related parasite species that infect birds from different families, Fregatidae and Laridae respectively. Furthermore, the dove parasite H. multipigmentatus , which only infects columbiforms, is closely related to lineages (NZB9, CY18, SGT14) that infect birds from different families (i.e., Sulidae, Laridae, Fregatidae) and orders (Suliformes and Charadriiformes) (Santiago-Alarcon et al. 2014). Hence, avian haemosporidians can host-switch across large taxonomic distances, making conservation efforts in the Galápagos and the study of disease ecology more challenging.
Fortunately, indirect evidence suggests that H. multipigmentatus do not have a strong negative effect on body condition of endemic doves (Santiago-Alarcon et al. 2012c). Nonetheless, we do not know the real impact of haemosporidians on Galapagos birds, which is a line of research that needs to be developed to gauge conservation efforts of native avifauna. Furthermore, the fact that endemic doves present high rates of gene flow across islands is suggestive of its high dispersal capacity (Santiago-Alarcon et al. 2006), which makes this species both susceptible to introduced pathogens and, if competent, a potential reservoir for moving pathogens across the archipelago that could switch to other endemic birds that are at higher risk due to factors such as small population sizes (e.g., Galapagos penguins; Levin et al. 2009).
Additionally to haemosporidian parasites, we also detected Trichomonas gallinae infecting non-native rock pigeons on San Cristóbal Island, but no infections with this parasite were detected in endemic doves from all the sampled islands (Padilla et al. 2004), which contrasts to some degree with the results found by Harmon et al. (1987), where they found infections with T. gallinae in three endemic doves from Santa Cruz Island, suggesting a host-switching event from non-native rock pigeons to endemic doves. Rock pigeons have been eradicated from the Galápagos archipelago and are no longer a threat to the endemic dove. We also detected Chlamidophila psittaci infecting endemic doves on Española Island, but no introduced rock pigeons, still present at that time, were infected by this parasite; no Salmonella sp. infections were detected in either of the two species of columbiform (Padilla et al. 2004).
Finally, we detected high infection prevalence (≥80%) in endemic doves by two lice species native to the Galápagos , Columbicola macrourae and Physconelloides galapagoensis , which to our knowledge pose no health threat to this bird given that they feed on feathers and feather debris (Santiago-Alarcon et al. 2008). Feather-feeding lice are known to create health problems to their hosts when parasite load is high, producing high levels of plumage damage that can leave birds unable to thermoregulate (Booth et al. 1993). Even in the case of these mostly benign ectoparasites, we have recorded that predator-prey interactions can open the door to host-switching events. We have retrieved the two above-mentioned lice species from endemic Galapagos hawks (Buteo galapagoensis), which are known to readily feed on endemic doves, and we know that the only typical bird host of those lice species on the Galápagos is the endemic dove (Whiteman et al. 2004). Hence, different ecological interactions such as competition (e.g., space for nesting on beaches) and predation are likely routes for parasite exchange among birds in the archipelago.
7.2.2 Filarial Parasites of the Flightless Cormorant (Phalacrocorax harrisi) and the Galapagos Penguin (Spheniscus mendiculus)
Measurements (μm) of microfilariae from peripheral blood of Flightless cormorants ( Phalacrocorax harrisi ) (N = 3 birds) and Galapagos Penguins ( Spheniscus mendiculus ) (N = 3 birds) (Reproduced from Merkel et al. 2007)
Flightless cormorants (N: 30)
Galapagos penguins (N:21)
G 1 cella
Sixteen genera of filarial parasites are known to infect many taxa of avian hosts (Bartlett 2008). Avian filarial parasites can be found in the brain, heart, lungs, spleen, kidney, eyes, subcutaneous tissues, and within the synovial fluid of joints (Bartlett 2008). In many cases no overt signs of disease are present; however, mechanical irritation, dyspnea, anorexia, pneumonia, and lethargy have been reported (Irwin 1975; Bartlett and Anderson 1981; Law et al. 1993; Simpson et al. 1996; Samour and Naldo 2001; Tarello 2006; Larrat et al. 2012). Subtle health compromise in wild birds can be difficult to assess. If the filarial parasite that infects the penguins and cormorants resides in a vital organ, such as the brain or heart, slight health effects could be missed with a single examination. Furthermore, concurrent infection with more than one parasite can have an additive deleterious effect. Mixed infections of an unidentified filarial parasite with Haemoproteus prognei, a Haemosporida, have been shown to cause a 90% mortality rate in wild Purple martins (Progne subis) (Davidar and Morton 2006). A combination of avian pox and Plasmodium parasites, also Haemosporida, had devastating effects on Hawaiian native birds (Warner 1968; van Riper et al. 1986; Atkinson et al. 1995). A Plasmodium parasite in the Galapagos penguins, not present in cormorants, was recently detected (Levin et al. 2009; Levin et al. 2013). Serious illness and fatalities have been reported in penguins infected with Plasmodium spp. (Fix et al. 1988; Grim et al. 2003; Bueno et al. 2010). Thus, Galapagos penguins concurrently infected with Plasmodium spp. and the filarial parasite may be more at risk of morbidity and mortality, but we have no direct evidence of this during the seasons of our sampling.
Filarial parasites have been reported previously in the Galapagos Islands. Dirofilaria immitis, a filarial parasite commonly known as canine heartworm, has been found on the island of Floreana (Barnett 1985). Dogs and sea lions were found with circulating microfilariae indicating a patent infection (an infection in which the parasite can complete the lifecycle), while humans and cats demonstrated circulating antibodies (exposure to the parasite but possibly not patent) (Barnett 1985). A subsequent study on Isabela Island, which is inhabited by penguins and cormorants, found that 34% of dogs were infected with canine heartworm. However, it was demonstrated that the filarial parasites infecting penguins and cormorants are unique and only distantly related to D. immitis (Levy et al. 2008). Filarial parasites are extremely rare in wild penguins (Jones and Shellam 1999). Our findings of the microfilariae in the Galapagos penguin may be the first in a non-captive penguin species (Merkel et al. 2007). D. immitis was found in the heart of a captive Humboldt penguin (Spheniscus humboldti), a close relative of the Galápagos penguin (Sano et al. 2005), which was believed to be the cause of death. A different filarioid parasite, Paronchocera straeleni , was found in the heart of a Galapagos penguin in captivity; this penguin had been captured in the wild and it was hypothesized that this infection was acquired prior to capture (Chabaud and Ball 1964). Reports of adult filarial parasites in cormorants or closely related birds include Chandlerella shaldybini, from a red-faced cormorant (Phalacrocorax urile), and an anhinga (Anhinga anhinga) infected with Paronchocerca helicina (Sonin 1963; Gubanov 1954). The genus Paronchocera has 17 identified species known to infect avian hosts (Bartlett 2008). Unlike other genera of filarial parasites which tend to have low host specificity, Paronchocera spp. are believed to be host specific within families of birds (Bartlett 2008). Our studies, the life history traits of Paronchocerca spp., and the description of P. straeleni from a Galapagos penguin has led us to suggest Paronchocera as the possible genus infecting both cormorants and penguins. Pending taxonomic validation, this would represent the first report of a Paronchocerca species switching between families of birds, Phalacrocracidae (cormorants) and Spheniscidae (penguins). If this is the case and the parasite has switched between families, it is likely that the cormorant is the preferred host. Our reasoning is that (a) cormorants had a higher prevalence of this parasite than the penguins and (b) worldwide, more cormorants are infected with filarids than penguins.
In the case of a parasite with an indirect life cycle it is important to consider possible vectors. All five groups of invertebrates capable of transmitting filarial and haemosporidian parasites to avian species occur in the Galapagos Islands: Phthiraptera (lice), Simuliidae (black flies), Culicidae (mosquitoes), Ceratopogonidae (biting midges), and Hippoboscidae (louse flies). Lice have been documented on both penguins and cormorants: Austrogoniodes demersus on Galapagos penguins and Pectinopygus nannopteri on flightless cormorants (Palma and Peck 2013; Banks and Palma 2003). Eleven species of ceratopogonid midges occur in the Galapagos Islands (Borkent 1991). Simuliidae are present in the Galapagos; however, due to the lack of fresh water required for breeding, it is unclear whether they inhabit the same coastal habitat as penguins and cormorants (Causton et al. 2006; Peck et al. 1998). There is one native mosquito species on the islands, the brackish-water breeding Aedes taeniorhynchus, and two non-native mosquitoes, Culex quinquefasciatus (Whiteman et al. 2005) and Aedes aegypti (Causton et al. 2006). Larvae of the worm D. immitis have been found infecting both A. taeniorhynchus and C. quinquefasciatus (Barnett 1985). Two different studies have demonstrated that A. taeniorhynchus feeds on cormorants (Bataille et al. 2012, Siers et al. 2010) and both have found a DNA sequence of a filarial nematode that was 100% identical to the filarial parasite infecting penguins and cormorants (Siers et al. 2010; Bataille et al. 2012). Siers et al. (2010) found a positive correlation between environmental factors (temperature, vegetation density, moisture) and prevalence. Higher temperatures, precipitation, and ground cover would increase the habitat quality for Aedes taeniorhynchus , the putative vector, thereby increasing the likelihood of transmission to the host. Although positive correlations between local environmental conditions and prevalence were found for both species, the correlations were stronger at the cormorant nesting sites (Siers et al. 2010). Lower prevalence in the penguins, despite similar microclimatic conditions for vectors, may point again to the cormorant being the preferred host (Siers et al. 2010). Although C. quinquefasciatus can breed in water with up to 40% salinity and is found on Isabela Island, it is improbable that this species is the vector as it is only found in areas close to human habitations or in the highlands far from the penguins and cormorants (Mosha and Subra 1983; Siers et al. 2010).
Despite more than 16 years of avian parasite research on the Galápagos archipelago, we are barely starting to understand parasite exchange among different host species. There is still taxonomic and systematic work to determine parasite species, their origins, and their health effects on avian endemics. We also need more studies on the ecology and phylogeography of parasites to understand their dynamics, movements, and origins. It is a priority to continue monitoring efforts for parasites across the archipelago, but with particular emphasis on those areas inhabited by humans and visited by tourists. Entry ports, either aerial or maritime, are hotspots for the arrival of non-native species. Hence, if funding for a monitoring program covering major islands is not feasible, then efforts should be made to secure funding for continuously monitoring ports and urban areas. In the case of birds with high dispersal capacity, such as doves, we recommend a continuous monitoring of their populations because they can serve as reservoirs and dispersing agents of non-native pathogens (e.g., avian haemosporidians). In the case of cormorants and penguins, we need to locate recently deceased penguins and cormorants, so we can determine the location of the adult filarial parasite in internal organs, which will allow definitive taxonomic identification. Flightless cormorants and Galapagos penguins are both endangered species (IUCN 2015), and live in restricted parts of a fragile habitat. Hence, we should not assume that these filarial parasites are non-pathogenic, which they may appear to be during benign environmental conditions, especially in the case of immunologically naive island species.
We thank all the people involved in the different parts of field work, in particular A. Iglesias, G. Buitron, J. Rabenold, J. Bollmer, I. Levin, J. Higashiguchi, and S. O’Brien. We also thank people involved in microscopy work, B. Murray, M. Rosenthal, J. Allen, G. Valkiūnas, and B. Sinclair (vector identification) and A. Sandoval-Comte for preparing Figs. 7.2 and 7.5. The University of Missouri-St. Louis Animal Care and Use Committee and the Galapagos National Park Service, Ecuador approved all animal handling and sampling protocols. We thank the Charles Darwin Foundation for logistical support during our work in Galapagos. This work was supported by grants from the Whitney R. Harris World Ecology Center, Idea Wild, The Frank M. Chapman Memorial Fund of the American Museum of Natural History, The Field Research for Conservation program of the Saint Louis Zoo (FRC 05–2 and FRC 08–2), The Organization for Tropical Studies, and by The Des Lee Collaborative Vision in Zoological Studies from the University of Missouri-St. Louis.
- Aguirre AA, Ostfeld RS, Daszak P (2012) New directions in conservation medicine: applied cases of ecological health. Oxford University Press, New York, NY, p 639Google Scholar
- Alexander AM, Finnoff DC, Shogren JF (2012) Human migration, border controls, and infectious disease emergence. In: Aguirre AA, Ostfeld RS, Daszak P (eds) New directions in conservation medicine: applied cases of ecological health. Oxford University Press, New York, NY, pp 179–191Google Scholar
- Baptista LF, Trail PW, Horblit HM (1997) Family Columbidae (pigeons and doves). In: del Hoyo J, Elliot A, Sargatal J (eds) Handbook of the birds of the world, Sandgrouse to cuckoos, vol 4. Lynx Edicions, Barcelona, pp 60–243Google Scholar
- Barnett BD (1985) Dogs of the Galapagos Islands: evolution, ecology, impact, and control. Dissertation, University of California–DavisGoogle Scholar
- Bartlett CM (2008) Filarioid nematodes. In: Atkinson CT, Thomas NJ, Hunter DB (eds) Parasitic diseases of wild birds. Wiley–Blackwell, Ames, IA, pp 439–462Google Scholar
- Gifford EW (1913) Expedition of the California Academy of Sciences to the Galápagos Islands, 1905–1906. Proc Calif Acad Sci 2:1–132Google Scholar
- Gubanov NM (1954) The helminth fauna of animals of economic importance from the Sea of Okhotsk and the Pacific Ocean. Akad Nauk SSSR 7:380–381Google Scholar
- Harmon WA, Harbecker A, Clark WA (1985) Parasite studies in the Galapagos. Report to the Charles Darwin Research Station. Charles Darwin Research Station, Puerto Ayora, Santa Cruz, Galapagos, pp 35–39Google Scholar
- Ibáñez-Bernal S, González-García F, Santiago-Alarcon D (2016) New bird host records for Ornithoctona fusciventris (diptera: hippoboscidae) in Mexico. S W Natural 60:377–381Google Scholar
- IUCN red list (2015) Red list. http://www.iucnredlist.org. Accessed Apr 2 2016
- Jones HI, Shellam GR (1999) Blood parasites in penguins, and their potential impact on conservation. Marine Ornithol 27:181–184Google Scholar
- Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546PubMedPubMedCentralCrossRefGoogle Scholar
- Levin II, Valkiūnas G, Santiago-Alarcon D, Cruz LL, Iezhova TA, O’Brien SL, Ricklefs RE (2011) Hippoboscid-transmitted Haemoproteus parasites (Haemosporida) infect Galapagos Pelecaniform birds: evidence from molecular and morphological studies, with a description of Haemoproteus iwa. Int J Parasitol 41(10):1019–1027PubMedCrossRefGoogle Scholar
- Levin I, Zwiers P, Deem SL, Geest EA, Higashiguchi JM, Iezhova TA, Jimenez-Uzcategui G, Kim DH, Morton JP, Perlut NG, Renfrew RB, Sari EHR, Valkiūnas G, Parker PG (2013) Multiple lineages of avian malaria parasites (Plasmodium) in the Galapagos Islands and evidence for arrival via migratory birds. Conserv Biol 27:1366–1377PubMedCrossRefGoogle Scholar
- Matamoros Y, Vargas H, Byers O, and Lacy R (2006) Taller de Análisis de Viabilidad de la Población y el Hábitat del Pingüino de Galápagos (Spheniscus mendiculus) 8–11 de Febrero, 2005. Puerto Ayora, Galápagos, Ecuador. IUCN/SSC Conservation Breeding Specialist Group, Apple Valley, Minnesota, pp 1–167Google Scholar
- Mosha FW, Subra R (1983) Salinity and breeding of Culex quinquefasciatus Say, Anopheles funestus Giles and Anopheles gambiae Giles sensu stricto (Diptera: Culicidae) on the Kenya Coast. Entomol Méd Parasitol 21(3):135–138Google Scholar
- Plowright RK, Cross PC, Tabor GM, Almberg E, Bienen L, Hudson PJ (2012) Climate change and infectious disease dynamics. In: Aguirre AA, Ostfeld RS, Daszak P (eds) New directions in conservation medicine: applied cases of ecological health. Oxford University Press, New York, NY, pp 111–121Google Scholar
- Poulin R (2007) Evolutionary ecology of parasites, 2nd edn. Princeton University Press, Princeton, NJ, p 332Google Scholar
- Prestwich AA (1959) The Galapagos Dove in freedom and captivity. Avic Mag 65:66–76Google Scholar
- Ryan F (2009) Virolution. Harper Collins Publishers, LondonGoogle Scholar
- Santiago-Alarcon D, Ricklefs RE, Parker PG (2012c) Parasitism in the endemic Galápagos Dove (Zenaida galapagoensis) and its relation to host genetic diversity and immune response. In: Paul E (ed) Emerging avian disease. Studies in avian biology, vol 42. University of California Press, Berkeley, CA, pp 31–42CrossRefGoogle Scholar
- Smith KF, Schloegel LM, Rosen GE (2012) Wildlife trade and the spread of disease. In: Aguirre AA, Ostfeld RS, Daszak P (eds) New directions in conservation medicine: applied cases of ecological health. Oxford University Press, New York, NY, pp 151–163Google Scholar
- Sonin MD (1963) Filariata of birds in the Soviet Far East [Filyariiptits Sovetskogo Dal’nego Vostoka]. Trudy GELAN 13:227–249Google Scholar
- Suzán G, Esponda F, Carrasco-Hernández R, Aguirre AA (2012) Habitat fragmentation and infectious disease ecology. In: Aguirre AA, Ostfeld RS, Daszak P (eds) New directions in conservation medicine: applied cases of ecological health. Oxford University Press, New York, NY, pp 135–150Google Scholar
- Swarth HS (1931) The avifauna of the Galapagos Islands. Occas Pap Calif Acad Sci 18:5Google Scholar
- Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton, FLGoogle Scholar
- Valkiūnas G, Santiago-Alarcon D, Levin II, Iezhova TA, Parker PG (2010) A new Haemoproteus species (Haemosporidia: Haemoproteidae) from the endemic galapagos dove Zenaida galapagoensis, with remarks on the parasite distribution, vectors, and molecular diagnostics. J Parasitol 96(4):783–792PubMedCrossRefGoogle Scholar
- Woodworth BL, Atkinson CT, LaPointe DA, Hart PJ, Spiegel CS, Tweed EJ, Henneman C, LeBrun J, Denette T, DeMots R, Kozar KL, Triglia D, Lease D, Gregor A, Smith T, Duffy D (2005) Host population persistence in the face of introduced vector-borne diseases: Hawaii amakihi and avian malaria. Proc Natl Acad Sci U S A 102:1531–1536PubMedPubMedCentralCrossRefGoogle Scholar