WildCare Institute

St. Louis, United States

WildCare Institute

St. Louis, United States

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Levin I.I.,University of Missouri-St. Louis | Levin I.I.,WildCare Institute | Zwiers P.,University of Missouri-St. Louis | Zwiers P.,Francis Marion University | And 16 more authors.
Conservation Biology | Year: 2013

Haemosporidian parasites in the genus Plasmodium were recently detected through molecular screening in the Galapagos Penguin (Spheniscus mendiculus). We summarized results of an archipelago-wide screen of 3726 endemic birds representing 22 species for Plasmodium spp. through a combination of molecular and microscopy techniques. Three additional Plasmodium lineages were present in Galapagos. Lineage A-infected penguins, Yellow Warblers (Setophaga petechia aureola), and one Medium Ground Finch (Geospiza fortis) was detected at multiple sites in multiple years. The other 3 lineages were each detected at one site and at one time; apparently, they were transient infections of parasites not established on the archipelago. No gametocytes were found in blood smears of infected individuals; thus, endemic Galapagos birds may be dead-end hosts for these Plasmodium lineages. Determining when and how parasites and pathogens arrive in Galapagos is key to developing conservation strategies to prevent and mitigate the effects of introduced diseases. To assess the potential for Plasmodium parasites to arrive via migratory birds, we analyzed blood samples from 438 North American breeding Bobolinks (Dolichonyx oryzivorus), the only songbird that regularly migrates through Galapagos. Two of the ephemeral Plasmodium lineages (B and C) found in Galapagos birds matched parasite sequences from Bobolinks. Although this is not confirmation that Bobolinks are responsible for introducing these lineages, evidence points to higher potential arrival rates of avian pathogens than previously thought. © 2013 Society for Conservation Biology.


Levin I.I.,University of Missouri-St. Louis | Parker P.G.,University of Missouri-St. Louis | Parker P.G.,WildCare Institute
Molecular Ecology | Year: 2014

Haemosporidian parasites, which require both a vertebrate and invertebrate host, are most commonly studied in the life stages occurring in the vertebrate. However, aspects of the vector's behaviour and biology can have profound effects on parasite dynamics. We explored the effects of a haemosporidian parasite, Haemoproteus iwa, on a hippoboscid fly vector, Olfersia spinifera. Olfersia spinifera is an obligate ectoparasite of the great frigatebird, Fregata minor, living among bird feathers for all of its adult life. This study examined the movements of O. spinifera between great frigatebird hosts. Movement, or host switching, was inferred by identifying host (frigatebird) microsatellite genotypes from fly bloodmeals that did not match the host from which the fly was collected. Such host switches were analysed using a logistic regression model, and the best-fit model included the H. iwa infection status of the fly and the bird host sex. Uninfected flies were more likely to have a bird genotype in their bloodmeal that was different from their current host's genotype (i.e. to have switched hosts) than infected flies. Flies collected from female birds were more likely to have switched hosts than those collected on males. Reduced movement of infected flies suggests that there may be a cost of parasitism for the fly. The effect of host sex is probably driven by differences in the sex ratio of bird hosts available to moving flies. See also the Perspective by Waite © 2013 John Wiley & Sons Ltd.


Ettling J.A.,WildCare Institute | Ettling J.A.,University of Missouri-St. Louis | Aghasyan L.A.,Armenian National Academy of Sciences | Aghasyan A.L.,Armenian National Academy of Sciences | And 2 more authors.
Copeia | Year: 2013

Armenian vipers (Montivipera raddei) have a restricted and fragmented distribution throughout portions of Armenia, eastern Turkey, and northwestern Iran. Over the past 40 years their population numbers have dropped by nearly 88% due to a combination of over-collection for the pet trade, conversion of habitat to agriculture, and overgrazing by livestock. While a few studies have examined aspects of their reproductive biology, we know very little about the spatial ecology of this species. We used radiotelemetry to study the spatial ecology and habitat use of Armenian vipers inhabiting a landscape modified by human use in Kotayk Province, Armenia during the spring 2007-2009 (17 males, 11 females) and for complete active seasons 2008-2009 (8 males, 6 females). We found no significant difference between sexes for home range size, average movements, or movement rates through areas involving cropland versus strictly steppe. Home ranges were significantly larger for males whose spring core area included some cropland. Both sexes showed significant preference for mountain steppe over cropland. Despite these differences, the interspersing of cropland among steppe habitat does not appear to impede the snakes' movements and seasonal use of the available habitat. While conservation of intact mountain steppe habitat is the ultimate goal, providing corridors of habitat in areas of agricultural development should be considered a high priority for managing this viper population into the future. © 2013 by the American Society of Ichthyologists and Herpetologists.


Santiago-Alarcon D.,Institute Ecologia Ac | Santiago-Alarcon D.,University of Missouri-St. Louis | Rodriguez-Ferraro A.,Simon Bolivar University of Venezuela | Parker P.G.,University of Missouri-St. Louis | And 2 more authors.
Parasites and Vectors | Year: 2014

Background: Previous studies have shown that haemosporidian parasites (Haemoproteus (Parahaemoproteus) and Plasmodium) infecting passerine birds have an evolutionary history of host switching with little cospeciation, in particular at low taxonomic levels (e.g., below the family level), which is suggested as the main speciation mechanism of this group of parasites. Recent studies have characterized diverse clades of haemosporidian parasites (H. (Haemoproteus) and H. (Parahaemoproteus)) infecting non-passerine birds (e.g., Columbiformes, Pelecaniiformes). Here, we explore the cospeciation history of H. (Haemoproteus) and H. (Parahaemoproteus) parasites with their non-passerine hosts. Methods. We sequenced the mtDNA cyt b gene of both haemosporidian parasites and their avian non-passerine hosts. We built Bayesian phylogenetic hypotheses and created concensus phylograms that were subsequently used to conduct cospeciation analyses. We used both a global cospeciation test, PACo, and an event-cost algorithm implemented in CoRe-PA. Results: The global test suggests that H. (Haemoproteus) and H. (Parahaemoproteus) parasites have a diversification history dominated by cospeciation events particularly at the family level. Host-parasite links from the PACo analysis show that host switching events are common within families (i.e., among genera and among species within genera), and occasionally across different orders (e.g., Columbiformes to Pelecaniiformes). Event-cost analyses show that haemosporidian coevolutionary history is dominated by host switching and some codivergence, but with duplication events also present. Genetic lineages unique to raptor species (e.g., FALC11) commonly switch between Falconiformes and Strigiformes. Conclusions: Our results corroborate previous findings that have detected a global cospeciation signal at the family taxonomic level, and they also support a history of frequent switching closer to the tips of the host phylogeny, which seems to be the main diversification mechanism of haemosporidians. Such dynamic host-parasite associations are relevant to the epidemiology of emerging diseases because low parasite host specificity is a prerequisite for the emergence of novel diseases. The evidence on host distributions suggests that haemosporidian parasites have the potential to rapidly develop novel host-associations. This pattern has also been recorded in fish-monogenean interactions, suggesting a general diversification mechanism for parasites when host choice is not restricted by ecological barriers. © 2014 Santiago-Alarcon et al.; licensee BioMed Central Ltd.


Levin I.I.,University of Missouri-St. Louis | Valkinas G.,Institute of Ecology | Iezhova T.A.,Institute of Ecology | O'Brien S.L.,WildCare Institute | And 3 more authors.
Journal of Parasitology | Year: 2012

Haemoproteus (Haemoproteus) jenniae n. sp. (Haemosporida: Haemoproteidae) is described from a Galapagos bird, the swallow-tailed gull Creagrus furcatus (Charadriiformes, Laridae), based on the morphology of its blood stages and segments of the mitochondrial cytochrome b (cyt b) gene. The most distinctive features of H. jenniae development are the circumnuclear gametocytes occupying all cytoplasmic space in infected erythrocytes and the presence of advanced, growing gametocytes in which the pellicle is closely appressed to the erythrocyte envelope but does not extend to the erythrocyte nucleus. This parasite is distinguishable from Haemoproteus larae, which produces similar gametocytes and parasitizes closely related species of Laridae. Haemoproteus jenniae can be distinguished from H. larae primarily due to (1) the predominantly amoeboid outline of young gametocytes, (2) diffuse macrogametocyte nuclei which do not possess distinguishable nucleoli, (3) the consistent size and shape of pigment granules, and (4) the absence of rod-like pigment granules from gametocytes. Additionally, fully-grown gametocytes of H. jenniae cause both the marked hypertrophy of infected erythrocytes in width and the rounding up of the host cells, which is not the case in H. larae. Phylogenetic analyses identified the DNA lineages that are associated with H. jenniae and showed that this parasite is more closely related to the hippoboscid-transmitted (Hippoboscidae) species than to the Culicoides spp.-transmitted (Ceratopogonidae) species of avian hemoproteids. Genetic divergence between morphologically well-differentiated H. jenniae and the hippoboscid-transmitted Haemoproteus iwa, the closely related parasite of frigatebirds (Fregatidae, Pelecaniformes), is only 0.6; cyt b sequences of these parasites differ only by 1 base pair. This is the first example of such a small genetic difference in the cyt b gene between species of the subgenus Haemoproteus. In a segment of caseinolytic protease C gene (ClpC), genetic divergence is 4 between H. jenniae and H. iwa. This study corroborates the conclusion that hippoboscid-transmitted Haemoproteus parasites infect not only Columbiformes birds but also infect marine birds belonging to Pelecaniformes and Charadriiformes. We conclude that the vertebrate host range should be used cautiously in identification of subgenera of avian Haemoproteus species and that the phylogenies based on the cyt b gene provide evidence for determining the subgeneric position of avian hemoproteids. © 2012 American Society of Parasitologists.


Ettling J.A.,WildCare Institute | Aghasyan A.L.,Armenian National Academy of Sciences | Aghasyan L.A.,Armenian National Academy of Sciences
International Zoo Yearbook | Year: 2015

The Caucasus is classified as one of the world's 35 'Biodiversity Hotspots', owing to the high level of endemism. Armenia is situated in the middle of the Caucasus hotspot and its reptilian fauna is considered to be one of the most interesting in the region. There are four species of viper occurring in Armenia: Blunt-nosed viper Macrovipera lebetina obtusa, Armenian viper Montivipera raddei, Darevsky's viper Pelias darevskii and Armenian Steppe viper Pelias eriwanensis. The latter three species are classified by the International Union for Conservation of Nature Red List as Near Threatened, Critically Endangered and Vulnerable, respectively. This paper provides insight into the factors that are threatening the existence of these vipers and describes what has been learned about their biology, and outlines the conservation actions that are being taken to secure their future. © 2014 The Zoological Society of London.


Chaves J.A.,University of California at Los Angeles | Parker P.G.,University of Missouri-St. Louis | Parker P.G.,WildCare Institute | Parker P.G.,Charles Darwin Foundation | Smith T.B.,University of California at Los Angeles
Journal of Evolutionary Biology | Year: 2012

The faunas associated with oceanic islands provide exceptional examples with which to examine the dispersal abilities of different taxa and test the relative contribution of selective and neutral processes in evolution. We examine the patterns of recent differentiation and the relative roles of gene flow and selection in genetic and morphological variation in the yellow warbler (Dendroica petechia aureola) from the Galápagos and Cocos Islands. Our analyses suggest aureola diverged from Central American lineages colonizing the Galápagos and Cocos Islands recently, likely less than 300000years ago. Within the Galápagos, patterns of genetic variation in microsatellite and mitochondrial markers suggest early stages of diversification. No intra-island patterns of morphological variation were found, even across steep ecological gradients, suggesting that either (i) high levels of gene flow may be homogenizing the effects of selection, (ii) populations may not have had enough time to accumulate the differences in morphological traits, or (iii) yellow warblers show lower levels of 'evolvability' than some other Galápagos species. By examining genetic data and morphological variation, our results provide new insight into the microevolutionary processes driving the patterns of variation. © 2012 The Authors. Journal of Evolutionary Biology © 2012 European Society For Evolutionary Biology.


Levin I.I.,University of Missouri-St. Louis | Valkiu-nas G.,Institute of Ecology | Santiago-Alarcon D.,University of Missouri-St. Louis | Cruz L.L.,University of Leeds | And 9 more authors.
International Journal for Parasitology | Year: 2011

Haemosporidian parasites are widely distributed and common parasites of birds, and the application of molecular techniques has revealed remarkable diversity among their lineages. Four haemosporidian genera infect avian hosts (Plasmodium, Haemoproteus, Leucocytozoon and Fallisia), and Haemoproteus is split into two sub-genera based on morphological evidence and phylogenetic support for two divergent sister clades. One clade (Haemoproteus (Parahaemoproteus)) contains parasites developing in birds belonging to several different orders, except pigeons and doves (Columbiformes), while the other (Haemoproteus (Haemoproteus)) has previously been shown to only infect dove hosts. Here we provide molecular and morphological identification of Haemoproteus parasites from several seabird species that are closely related to those found in dove hosts. We also document a deeply divergent clade with two haemosporidian lineages recovered primarily from frigatebirds (Fregatidae, Pelecaniformes) that is sister to the hippoboscid-(Hippoboscidae) transmitted dove parasites. One of the lineages in this new clade of parasites belongs to Haemoproteus iwa and is distributed in two species of frigatebird (Fregata) hosts from Hawaii, the Galapagos Islands, the eastern Pacific and throughout the Caribbean Basin. Haemosporidian parasites are often considered rare in seabirds due in part to the lack or low activity of some dipteran vectors (e.g., mosquitos, biting midges) in marine and coastal environments; however, we show that H. iwa is prevalent and is very likely vectored among frigatebirds by hippoboscid flies which are abundant on frigatebirds and other seabirds. This study supports the existence of two sister clades of avian Haemoproteus in accord with the subgeneric classification of avian hemoproteids. Description of H. iwa from Galapagos Fregata minor is given based on morphology of blood stages and segments of the mitochondrial cytochrome b gene, which can be used for identification. This study shows that hippoboscid flies warrant more attention as vectors of avian Haemoproteus spp., particularly in marine and coastal environments. © 2011 Australian Society for Parasitology Inc.


Parker P.G.,University of Missouri-St. Louis | Parker P.G.,WildCare Institute | Buckles E.L.,Cornell University | Farrington H.,University of Cincinnati | And 7 more authors.
PLoS ONE | Year: 2011

The role of disease in regulating populations is controversial, partly owing to the absence of good disease records in historic wildlife populations. We examined birds collected in the Galapagos Islands between 1891 and 1906 that are currently held at the California Academy of Sciences and the Zoologisches Staatssammlung Muenchen, including 3973 specimensrepresenting species from two well-studied families of endemic passerine birds: finches and mockingbirds. Beginning with samples collected in 1899, we observed cutaneous lesions consistent with Avipoxvirus on 226 (6.3%) specimens. Histopathology and viral genotyping of 59 candidate tissue samples from six islands showed that 21 (35.6%) were positive for Avipoxvirus, while alternative diagnoses for some of those testing negative by both methods were feather follicle cysts, non-specific dermatitis, or post mortem fungal colonization. Positive specimens were significantly nonrandomly distributed among islands both for mockingbirds (San Cristobal vs. Espanola, Santa Fe and Santa Cruz) and for finches (San Cristobal and Isabela vs. Santa Cruz and Floreana), and overall highly significantly distributed toward islands that were inhabited by humans (San Cristobal, Isabela, Floreana) vs. uninhabited at the time of collection (Santa Cruz, Santa Fe, Espanola), with only one positive individual on an uninhabited island. Eleven of the positive specimens sequenced successfully were identical at four diagnostic sites to the two canarypox variants previously described in contemporary Galapagos passerines. We conclude that this virus was introduced late in 18909s and was dispersed among islands by a variety of mechanisms, including regular human movements among colonized islands. At present, this disease represents an ongoing threat to the birds on the Galapagos Islands. © 2011 Parker et al.


Yackulic C.B.,Columbia University | Yackulic C.B.,Princeton University | Blake S.,Wildlife Conservation Society | Blake S.,Max Planck Institute for Ornithology (Radolfzell) | And 5 more authors.
Journal of Animal Ecology | Year: 2011

Large data sets containing precise movement data from free-roaming animals are now becoming commonplace. One means of analysing individual movement data is through discrete, random walk-based models. Random walk models are easily modified to incorporate common features of animal movement, and the ways that these modifications affect the scaling of net displacement are well studied. Recently, ecologists have begun to explore more complex statistical models with multiple latent states, each of which are characterized by a distribution of step lengths and have their own unimodal distribution of turning angles centred on one type of turn (e.g. reversals). Here, we introduce the compound wrapped Cauchy distribution, which allows for multimodal distributions of turning angles within a single state. When used as a single state model, the parameters provide a straightforward summary of the relative contributions of different turn types. The compound wrapped Cauchy distribution can also be used to build multiple state models. We hypothesize that a multiple state model with unimodal distributions of turning angles will best describe movement at finer resolutions, while a multiple state model using our multimodal distribution will better describe movement at intermediate temporal resolutions. At coarser temporal resolutions, a single state model using our multimodal distribution should be sufficient. We parameterize and compare the performance of these models at four different temporal resolutions (1, 4, 12 and 24h) using data from eight individuals of Loxodonta cyclotis and find support for our hypotheses. We assess the efficacy of the different models in extrapolating to coarser temporal resolution by comparing properties of data simulated from the different models to the properties of the observed data. At coarser resolutions, simulated data sets recreate many aspects of the observed data; however, only one of the models accurately predicts step length, and all models underestimate the frequency of reversals. The single state model we introduce may be adequate to describe movement data at many resolutions and can be interpreted easily. Multiscalar analyses of movement such as the ones presented here are a useful means of identifying inconsistencies in our understanding of movement. © 2011 The Authors. Journal of Animal Ecology © 2011 British Ecological Society.

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