Jane Merkel

Assessing the risks of introduced chickens and their pathogens to native birds in the Galápagos Archipelago

Abstract Poultry production is an important economic activity on inhabited islands of the Galápagos archipelago. There has been a recent surge in both small-scale backyard chickens and larger scale broiler production associated with growth in the human population and the tourist industry. With increased poultry production, concerns have been expressed about the increasing risk of transfer of disease from chickens to native Galápagos bird species that may have little resistance to introduced pathogens [Wikelski, M., Foufopoulos, J., Vargas, H., Snell, H., 2004. Galápagos birds and diseases: invasive pathogens as threats for island species. Ecology and Society 9(5). Available from: URL:http://www.ecologyandsociety.org/vol9/iss1/art5]. This study evaluates risks posed by chicken disease to endemic and native Galápagos bird species, based on empirical evidence of pathogens present in chickens on the islands and a literature review of effects of these pathogens in wild species. Pathogens identified in domestic chicken populations of immediate avian conservation concern are Newcastle disease, Mycoplasma gallisepticum, and the proventricular parasite Dispharynx sp. Newcastle disease (avian paramyxovirus-1) poses an imminent threat to Galápagos penguins (Spheniscus mendiculus), flightless cormorants (Phalacrocorax harrisi), and lava gulls (Larus fuliginosus), species with very small population sizes (less than 1500 animals each). Additionally, litter from broiler farms could affect ecological processes in local ecosystems. Improved poultry biosecurity measures are urgently needed on the Galápagos Islands for avian disease management, yet developing these strategies presents political, social, and economic challenges.

Hematology, serum chemistry, and serology of Galápagos penguins (Spheniscus Mendiculus) in the Galápagos Islands, Ecuador

The Galápagos penguin (Spheniscus mendiculus) is an endangered species endemic to the Galápagos Islands, Ecuador. In 2003 and 2004, 195 penguins from 13 colonies on the islands of Isabela and Fernandina in the Galápagos archipelago were examined. Genetic sexing of 157 penguins revealed 62 females and 95 males. Hematology consisted of packed cell volume (n=134), white blood cell differentials (n=83), and hemoparasite blood smear evaluation (n=114). Microfilariae were detected in 22% (25/114) of the blood smears. Female penguins had significantly higher eosinophil counts than males. Serum chemistry on 83 penguins revealed no significant differences between males and females. Birds were seronegative to avian paramyxovirus type 1–3, avian influenza virus, infectious bursal disease virus, Mareks disease virus (herpes), reovirus, avian encephalomyelitis virus, and avian adenovirus type 1 and 2 (n=75), as well as to West Nile virus (n=87), and Venezuelan, western and eastern equine encephalitis viruses (n=26). Seventy-five of 84 (89%) penguins had antibodies to Chlamydophila psittaci but chlamydial DNA was not detected via polymerase chain reaction in samples from 30 birds.

SURVEY FOR HAEMOPROTEUS SPP., TRICHOMONAS GALLINAE, CHLAMYDOPHILA PSITTACI, AND SALMONELLA SPP. IN GALAPAGOS ISLANDS COLUMBIFORMES

Abstract Endemic free-ranging Galapagos doves (Zenaida galapagoensis) and introduced rock doves (Columba livia) were surveyed in several islands of the Galapagos archipelago to establish sample prevalence of hemoparasites, Trichomonas gallinae, Chlamydophila psittaci, and Salmonella species. A Haemoproteus sp., the only hemoparasite identified, was found in 89% of the Galapagos doves sampled but not in the rock doves. Trichomonas gallinae was detected by polymerase chain reaction in 44% of rock doves from San Cristobal but in none of the Galapagos doves. Chlamydophila psittaci was detected from cloacal swabs in 6% of the Galapagos doves but in none of the rock doves sampled. All positive cases of C. psittaci occurred on Española, where the crude sample prevalence was 24%. A polymerase chain reaction–based Salmonella test failed to show evidence of this organism from any birds sampled.

Cryptic host specificity of an avian skin mite (Epidermoptidae) vectored by louseflies (Hippoboscidae) associated with two endemic Galapagos bird species

Host specificity of vectors is an important but understudied force shaping parasite evolution and the relationship between hosts and parasites. Low vector specificity may allow a vectored parasite to invade new host species, whereas high specificity of vectors may reduce the host range of the parasite and favor specialization. The ‘generalist’ and widely distributed avian skin mite Myialges caulotoon Speiser (Acari: Epidermoptidae) is unusual because females require an insect vector to complete their life cycle. Myialges caulotoon was previously reported from 2 lousefly (Diptera: Hippoboscidae) species, Olfersia sordida and Icosta nigra, parasitizing flightless cormorants (Phalacrocorax harrisi) and Galápagos hawks (Buteo galapagoensis), respectively, within the Galápagos Islands. This is a surprising distribution, given that the 2 lousefly species involved are relatively host-specific. Mitochondrial DNA sequences revealed 2 reciprocally monophyletic Myialges clades that sorted out perfectly with respect to their vector species, regardless of whether they were in allopatry or sympatry. One clade was restricted to flies of hawks and the other to flies of cormorants. Females of the 2 Myialges groups were also separated consistently by the shape of the sternal surface sclerotization. Mites of hawk flies were more abundant than those of cormorant flies. Within the Myialges clade associated with hawks, genetic differentiation between 2 island populations mirrored its hosts patterns of differentiation.

HEMATOLOGY, PLASMA CHEMISTRY, SEROLOGY, AND CHLAMYDOPHILA STATUS OF THE WAVED ALBATROSS (PHOEBASTRIA IRRORATA) ON THE GALAPAGOS ISLANDS

Abstract Venipuncture was performed on 50 adult, free-ranging waved albatrosses (Phoebastria irrorata) on Española, Galapagos Islands, Ecuador, to establish hematologic and plasma biochemistry reference ranges and to determine the prevalence of exposure to important domestic avian pathogens. Weights and plasma creatine phosphokinase activities differed significantly between males and females. Serum was tested for evidence of exposure to avian influenza, avian paramyxoviruses 1, 2, and 3, avian cholera, adenovirus groups 1 and 2, avian encephalomyelitis, Mareks disease, infectious bursal disease, and infectious bronchitis virus (Connecticut and Massachusetts strains). Of 44 birds, 29 (66%) seroreacted to adenovirus group 1, and four seroreacted to avian encephalomyelitis. Cloacal swabs were negative for Chlamydophila psittaci DNA.

Microfilariae in GaláPagos penguins (Spheniscus mendiculus) and flightless cormorants (Phalacrocorax harrisi): Genetics, morphology, and prevalence

Galápagos penguins (Spheniscus mendiculus) and flightless cormorants (Phalacrocorax harrisi) live in small, isolated populations on the westernmost islands of Isabela and Fernandina in the Galápagos Islands, Ecuador. Between August 2003 and February 2005, 4 field trips, 2 in the cool, dry season (August 2003 and August 2004) and 2 in the hot, rainy season (March 2004 and February 2005), were undertaken; 298 Galápagos penguins and 380 cormorants were sampled for prevalence and intensity of hemoparasites. Microfilariae were found in both the penguins and the cormorants. Blood smears were negative for the presence of other species of hemoparasites. Overall prevalence of microfilariae across seasons was 42.0% in cormorants and 13.8% in the penguins. Intensity of infection was generally low (mean = 3.2–31.7 in 25 fields across seasons and species) with the exception of a few individuals with markedly high intensities of parasites (>300 in 25 fields in 1 cormorant). Prevalence of microfilariae increased significantly over the 4 sampling periods for cormorants, but not for penguins. Prevalences were significantly higher in cormorants than in penguins for 3 of the 4 collecting trips. Male penguins had higher prevalences than females; however, there were no gender differences in cormorants. No relation was detected between body mass and either presence or intensity of parasitism. Morphological characteristics of the microfilariae are also described and specimens from each host species were similar in all characters measured. DNA sequence data from the mitochondrial cytochrome c oxidase subunit I gene were consistent with the morphological evidence and together demonstrate that the penguins and cormorants are likely to be infected with the same species of microfilariae.

HEMATOLOGY, PLASMA CHEMISTRY, AND SEROLOGY OF THE FLIGHTLESS CORMORANT (PHALACROCORAX HARRISI) IN THE GALAPAGOS ISLANDS, ECUADOR

The flightless cormorant (Phalacrocorax harrisi) is an endemic species of the Galápagos Islands, Ecuador. Health studies of the species have not previously been conducted. In August 2003, baseline samples were collected from flightless cormorant colonies on the islands of Isabela and Fernandina. Seventy-six birds, from nestlings to adults, were evaluated. Genetic sexing of 70 cormorants revealed 37 females and 33 males. Hematology assessment consisted of packed cell volume (n=19), leukograms (n=69), and blood smear evaluation (n=69). Microscopic evaluation of blood smears revealed microfilaria in 33% (23/69) of the cormorants. Plasma chemistries were performed on 46 cormorants. There was no significant difference in chemistry values or complete blood counts between male and female cormorants or between age groups. Based on a serologic survey to assess exposure to avian pathogens, birds (n=69) were seronegative for West Nile virus, avian paramyxovirus type 1 (Newcastle disease virus), avian paramyxovirus types 2 and 3, avian influenza, infectious bursal disease, infectious bronchitis, Mareks disease (herpes), reovirus, avian encephalomyelitis, and avian adenovirus type 2. Antibodies to avian adenovirus type 1 and Chlamydophila psittaci were found in 31% (21/68) and 11% (7/65) of flightless cormorants respectively. Chlamydophila psittaci was detected via polymerase chain reaction in 6% (2/33) of the cormorants. The overall negative serologic findings of this research suggest that the flightless cormorant is an immunologically naïve species, which may have a reduced capacity to cope with the introduction of novel pathogens.

Exposure to Toxoplasma gondii in Galapagos Penguins (Spheniscus mendiculus) and Flightless Cormorants (Phalacrocorax harrisi ) in the Galapagos Islands, Ecuador

Toxoplasma gondii is one of the most common protozoan parasites of humans and warm-blooded animals. Members of the family Felidae are the only definitive hosts of this parasite and, thus, important in the epidemiology of the disease. Previous studies on Pacific islands have found T. gondii infections in a number of avian species where domestic cats (Felis catus) have been introduced. Little is known about T. gondii in the Galapagos Islands, although introduced domestic cats in the archipelago are known to be T. gondii antibody-positive. In this study, we quantified prevalence of antibody to T. gondii in two threatened avian marine species, Galapagos Penguins (Spheniscus mendiculus) and Flightless Cormorants (Phalacrocorax harrisi), and tested the hypothesis that this parasite is more prevalent on Isabela Island (with cats) than on Fernandina Island (without cats). Overall, antibody prevalence was 2.3% in both Galapagos Penguins and Flightless Cormorants from samples collected during 2003–2005, and in 2008. In Galapagos Penguins (n=298), a significantly higher antibody prevalence was found in penguins on Fernandina Island (free of cats) than on Isabela Island (with cats; Fishers exact test; P=0.02). In Flightless Cormorants (n=258), there was a higher antibody prevalence in cormorants living on Isabela than on Fernandina, although this difference was not statistically significant (Fishers; P=0.19). This study is the first to show exposure to T. gondii in endemic avian species in the Galapagos Islands, providing evidence for disease-related risks associated with the feral cat population in the archipelago. We provide possible explanations for these findings and recommendations for future studies towards a better understanding of the epidemiology of T. gondii in the Galapagos Islands.

COMPARISON OF BLOOD VALUES AND HEALTH STATUS OF FLOREANA MOCKINGBIRDS (MIMUS TRIFASCIATUS) ON THE ISLANDS OF CHAMPION AND GARDNER-BY-FLOREANA, GALÁPAGOS ISLANDS

The Floreana Mockingbird (Mimus trifasciatus) is one of the rarest bird species in the world, with an estimated 550 individuals remaining on two rocky islets off the coast of Floreana, Galápagos, Ecuador, from which the main population was extirpated more than 100 yr ago. Because they have been listed in critical danger of extinction, a plan to reintroduce this species to Floreana has been initiated. Determining the health status of the source mockingbird populations is a top priority within the reintroduction plan. We report the health status, over the course of 4 yr, of 75 Floreana Mockingbirds on Champion Island and 160 Floreana Mockingbirds on Gardner-by-Floreana, based on physical examinations, hematology, hemolysis–hemagglutination assay, exposure to selected infectious disease agents, and ecto- and endoparasite counts. Birds on Gardner-by-Floreana had higher body condition index scores, packed cell volumes, total solids, and lymphocyte counts. Additionally, Gardner-by-Floreana birds had lower heterophil counts, eosinophil counts, and heterophil:lymphocyte ratios. No Chlamydophila psittaci DNA or antibodies to paramyxovirus-I, adenovirus-II, or Mycoplasma gallisepticum were found in any of the mockingbirds tested. Ectoparasites were present on birds from both islands, although species varied between islands. A coccidian species was found in eight of the 45 fecal samples from birds on Gardner-by-Floreana, but none of 33 birds examined from Champion. Birds on Gardner-by-Floreana were classified as healthier than those on Champion based on clinical and laboratory findings. These health data will be analyzed in conjunction with genetics, population structure, and disease presence on Floreana for developing recommendations for the Floreana Mockingbird reintroduction plan.

ECOLOGICAL CORRELATES OF MICROFILARIAE PREVALENCE IN ENDANGERED GALAPAGOS BIRDS

Abstract This study assesses the ecological factors associated with microfilariae prevalence in wild populations of endangered flightless cormorants (Phalacrocorax harrisi) and Galápagos penguins (Spheniscus mendiculus). Prevalence values were tested for correlation with a large number of environmental variables, as modeled from weather station data and measured by satellite-borne sensors. Predictions were made based on the expected effects of climatic and landscape variables on sustained populations of arthropod vectors required for transmission of microfilariae. In general, findings were consistent with predictions in both cormorants and penguins; prevalence correlated positively with temperature, precipitation, and vegetation density, and negatively with measures of environmental variability. Resulting correlates were used to derive predictive distributions of prevalence values in cormorants throughout the archipelago. Evidence is presented implicating the mosquito Aedes taeniorhynchus as a likely vector. Knowledge of environmental variables that predict risk of disease transmission by arthropod vectors may be useful in control measures should novel pathogens be introduced to the ecosystem.