Health of Antarctic birds: a review of their parasites, pathogens and diseases

Abstract

Antarctic birds are not beyond the effects of parasites or pathogens. However, potential ecological consequences of wide-spread infections for bird populations in Antarctica have received little attention. In this paper, we review the information published about disease and parasites, and their effects on Antarctic birds. The information on host species, parasites and pathogens, and geographic regions is incomplete and data on ecological effects on the populations, including how birds respond to pathogens and parasites, are almost inexistent. We conclude that more research is needed to establish general patterns of spatial and temporal variation in pathogens and parasites, and to determine how such patterns could influence hosts. This information is crucial to limit the spread of outbreaks and may aid in the decision-making process should they occur.

Introduction

Disease is one of the main agents of morbidity and mortality in living organisms (Haldane 1949). A single outbreak can decimate animal populations. Some examples include the death of 18,000 seals in Northern Europe from the Phocine Distemper Virus (Jensen et al. 2002), the loss of 40,000 Mallards due to the appearance of new diseases (Friend 2006), a decrease in the population of North American House Finch due to Mycoplasma conjunctivitis (Hochachka and Dhondt 2000) and the decline of several species of frogs in Australia from a virus infection (Laurance et al. 1996), among others. However, disease (including both effects of microbes and parasites) has only recently been recognized as an active player in ecosystems through its effects on host populations (Grenfell and Dobson 1995).

Infectious disease outbreaks can lead to catastrophic population reductions. However, pathogens and parasites can also cause variations in metabolic rate (e.g., Møller et al. 1994), and influence life history traits, such as the phenology of reproduction, clutch size, and brood size (see revision in Møller 1997), the expression of secondary sexual characters (Hillgarth and Wingfield 1997) as well as social status (Rau 1983).

Despite their geographical isolation, habitats such as the Antarctic ecosystems are not beyond the risk posed by pathogens and/or parasites. So far, only a few events of mass mortality have been reported (Kerry et al. 1999) and no major outbreaks of infectious diseases have been described in Antarctica (Weimerskirch 2004), although some were reported from remote islands in the Southern Ocean (Weimerskirch 2004).

However, increased warming across the continent (see Steig et al. 2009) may make the survival of pathogens and large-scale outbreaks more likely.

During the “Workshop on diseases in Antarctic Wildlife” held in Hobart in 1998 a number of recommendations were made for their monitoring and prevention of Antarctic Treaty Consultative Meeting (ACTM) (Kerry et al. 1999). One of the recommendations was to establish that “a structured research program is required to provide information about what is normal and what is aberrant in the health of Antarctic species” (Kerry et al. 1999). However, to date this has not yet been achieved. What is required is an in-depth review on the epidemiology of diseases and their status in any Antarctic birds. The only review currently available focuses solely on penguins (see Clarke and Kerry 2000). This information is important in terms of ecosystem health, as any variation in the prevalence of a disease in species may be a sign of “ecosystem distress syndrome” (Rapport 2007). Global change is one of the main factors affecting ecosystem health through the relationship between climate change and global human travel, and the increase of distribution ranges, abundance and/or virulence of parasites and pathogens (Daszak et al. 2000; Sutherst 2001, Harvell et al. 2002; Epstein et al. 2003). In Antarctica, especially the Antarctic Peninsula and West Antarctica, temperatures have risen (Turner et al. 2004; IPCC 2007; Steig et al. 2009). Furthermore, human activities, such as research stations, as well as increasing tourism activities can facilitate the spread of disease (Curry et al. 2002). Research activities tend to concentrate on relatively small areas or specific locations while tourists visit a great number of colonies in a short span of time. It is worth mentioning that tour companies that are members of the International Antarctic Tour Operator (IAATO) have a boot-cleaning policy which may reduce such risk, as long as it is carried out thoroughly. Companies that are not IAATO members and private vessels are more likely to contribute to the spread of disease. Finally, disease can also be spread by migratory species. These species are thought to be responsible for transmission of several viruses, such as influenza or New Castle disease, bacteria, such as Campylobacter jejuni, Pasteurella multocida, Clostridium botulinum and Mycobacterium avium, and protozoa, such as Cryptosporidium sp (Hubalek 2004). These agents are a recognized risk in Antarctica (Kerry et al. 1999).

The aim of this paper is to compile published information on the presence and the effects of disease, pathogens and parasites in Antarctic birds to provide a baseline for the evaluation of the health of the Antarctic ecosystem.

Materials and methods

The information was taken from papers referenced in the Zoological Record and PubMed database and from in-depth bibliographical research. Antarctic birds were those non-passerines included in the book, “A Complete Guide to Antarctic Wildlife” (Shirihai 2002) breeding and distributed in Antarctica and sub-Antarctic islands south of 45°S (see Frenot et al. 2005 for a similar consideration of Antarctic territory). We examined information for 46 bird species (Table 1). Data on whether microorganisms (virus and bacteria) were detected by means of serology or by isolation were given as well as information about geographical location.

Table 1 Microorganisms, diseases and parasites present in Antarctic birds

Results and discussion

We reviewed 101 published papers dealing with issues related to parasites, pathogens or diseases (Table 1), and found information on 38 out of 46 (82%) bird species searched. The number of publications per species was highly variable (Table 1). For example, Adelie (Pygoscelis adeliae), the Gentoo (Pygoscelis papua), and the Chinstrap (Pygoscelis antarctica), as well as kelp gulls (Larus dominicanus), were mentioned in more than 15 publications compared to only three dealing with Antarctic terns (Sterna vittata). With respect to disease agents (or antibodies) reportedly in Antarctic birds, bacteria were detected in 15 species (33%), viruses in 9 (20%), protozoa in 14 (30%), gastrointestinal parasites in 20 (44%), and ectoparasites in 37 species (80%) (Table 1). The species with the highest number of parasites or pathogens described are the three pygoscelid penguins, the giant petrels (Macronectes giganteus), sub-Antarctic skuas (Catharacta skua lonnbergi), sheathbills (Chionis alba), and kelp gulls (Larus dominicanus). However, this difference is probably more a reflection of the differences in research effort rather than based on biological reasons.

The distribution of parasites and pathogens in Antarctic birds shows that seven viruses are likely to be present, of which only paramyxovirus and poxvirus have been isolated (Table 1). The viruses responsible for infectious bursal disease, Newcastle disease and influenza have only been reported from serological studies and have never been isolated in Antarctica (Morgan et al. 1981; Morgan and Westbury 1981; Austin and Webster 1993; Gardner et al. 1997; Gauthier-Clerc et al. 2002; Baumeister et al. 2004; Wallensten et al. 2006; Miller et al. 2008). Moreover in the studies where isolation or direct detection (i.e., PCR methods) was carried out, results have been negative (Morgan and Westbury 1988; Wallensten et al. 2006). Thus, if the presence of viruses is implied and solely determined by serological techniques, caution, needs to be applied when interpreting the results and further studies applying direct detection or isolation should be carried out to confirm or reject the presence of a certain organism. Of the 42 bacteria reported in Antarctic birds, 37 were isolated, and seven were detected only by serological techniques. The main bacteria detected were Campylobacter lari, the common bacteria causing enteritis in birds and humans (Waldenstrom et al. 2002), and are transmitted by contaminated food or water; Pasteurella multocida, responsible for avian cholera, can be transmitted by aerosols (Simensen and Olson 1980) or by contaminated food or water (Botzler 1991); Escherichia coli, although generally part of the natural bacterial flora in birds, can become pathogenic in conjunction with other infections (Morishita et al. 1999); Chlamidya sp. which is responsible for psittacosis and is transmitted mainly by aerosols, contaminated water, and by blood-suckling ectoparasites (Harkinezhad et al. 2009). Finally, at least five species of Salmonella were detected (Table 1). Interestingly, Salmonella was not only found in scavenging species, such as skuas and giant petrels, but also in albatrosses and penguins. These bacteria are common inhabitants of the intestinal tract of birds, and are usually the cause of disease only under conditions of stress. Birds contract the bacteria either through direct contact with infected birds or through ingestion of contaminated food or water (Tizard 2004). It is also interesting to note that in some species (i.e., pygoscelis penguins) reported results have been negative not only for Campylobacter sp., Campylobacter jejuni, but also for C. lari and for Salmonella in some locations, while in others the bacteria have been detected. This suggests that the distribution of these bacteria could be restricted to specific locations such as the proximity of research stations (Bonnedahl et al. 2005) or that resistance of the host may differ among different populations of the same species. Protozoa detected in Antarctica belong to six genera (Table 1). Two are blood parasites present in sub-Antarctic islands, but absent in Antarctica. This mirrors the presence of suitable vectors for their transmission that are absent in Antarctica (Merino et al. 1997). However, other such as the role of immunocompetence in preventing infection by blood-parasites in marine birds cannot be excluded (Martinez-Abrain et al. 2004). The remaining four genera are coccidian found in the intestinal tract of birds. Note that only one species has been identified, while most could only be identified to genus level because of the failure of the oocysts to sporulate (Golemansky 2003). Antarctic birds host 39 species and four genera not identified as specific gastrointestinal parasites (Table 1). The most frequently recorded species are the cestodes Parorchites zederi and Tetrabothrius pauliani, the nematode Stegophorus macronectes, the acanthocephalan Corynosoma hamanni, and the trematoda Gymnophallus deliciosus. The cestodes and nematode mainly infect penguin species, as well as sheathbills (Chionis alba) and giant petrels (Macronectes giganteus). In contrast, acanthocephalan and trematoda mainly infect not only kelp gulls (Larus dominicanus) and skuas (Catharacta lonnbergi and C. maccormicki) but also sheathbills. Infestations by cestodes, nematodes, acanthocephalan, and trematoda are strongly influenced by the foraging habits of the hosts (Hoberg 1996). General foragers would be expected to be infested by more parasites than specialized species. For instance, the bird species infected by the most species of parasites are sheathbills (14 species) and Kelp gulls (12 species), both are generalists. In comparison, species highly specialized in krill (Euphausia spp.) like Chinstrap penguins are only infested by four species of gastrointestinal parasites. Corynosoma matures in the intestinal tract of mammals and birds; fish and aquatic invertebrates often serve this worm as intermediate hosts. However, since euphausiids are not part of the intermediate hosts of Corynosoma, infestation rates are low krill-dependent species like penguins (Muzaffar and Jones 2004).

The most numerous of parasites in Antarctic and sub-Antarctic birds are ectoparasites with 75 species (Table 1). Lice (Phthiraptera) are the most abundant with 66 species, and some very well-represented genera such as Austrogoniodes sp., Docophoroides sp., Naubates sp., Trabeculus sp. or Saemundssonia sp. Other ectoparasites include the feather mites Zachvatknia sp, Alloptes sp., and Scutomegninia sp., ticks, of the Ixodes genus and the endemic Antarctic flea Glacyopsillus antarcticus. Finally, only one fungus infection by Thelebolus microsporus was reported in skuas, and two by the pentastomid Reighardia sternae in skuas and Kelp gulls.

Antarctic and Sub-Antarctic birds host a total of 173 parasites or pathogenic organisms. The most diversified group in terms of number of species is ectoparasites, especially lice. Although most of them seem to be located in the sub-Antarctic region, birds living in continental Antarctica, such as Emperor (Aptenodytes forsteri) and Adelie penguins (Pygoscelis adeliae) are parasitized by some lice. This suggests that lice are not limited by the environmental conditions of polar environments. However, these harsh conditions seem to limit the diversity and abundance of parasitic protozoa, which are represented by only six genera, specifically blood parasites, as these organisms need an arthropod vector to infect the birds (see above). The second most abundant group is the bacteria, which is clearly correspond to this group’s enormous diversity elsewhere. However, little is known about the community of potential pathogenic bacteria present in Antarctic birds (Kerry et al. 1999). The presence of viruses is difficult to evaluate because no disease-causing virus has yet been isolated in Antarctica, although certain virus antibodies have been found (see above). Therefore, more attention must be given to the isolation of pathogenic viruses in Antarctica.

Geographical variation in the distribution of reported parasites, pathogens and diseases shows that 63 of these organisms (eight bacteria, six viruses, two protozoa, 18 gastrointestinal parasites and 29 ectoparasites) are present in sub-Antarctic islands. Sixty organisms (32 bacteria, two viruses, two protoza, 23 gastro-intestinal parasites and one ectoparasite) are present in the South Shetlands and 23 in the continental Antarctic Peninsula (10 bacteria, two virus, two protozoa and nine gastrointestinal parasites). In continental Antarctica, there are 19 parasites or pathogens (two bacteria, four viruses, one protozoon, four gastrointestinal parasites and eight ectoparasites) (Table 1). It is difficult to interpret these apparent differences in distribution from a biological point of view, because they probably reflect differences in research effort in the various Antarctic regions rather than any actual geographical variation. For instance, the largest number of organisms was found at the South Shetlands where also most of the relevant research has been done in Antarctica. However, ectoparasites seem to be more common in the sub-Antarctic islands, which is to be expected from their dependency on thermal conditions. On the other hand, more ectoparasite species have been found in continental Antarctica than in the South Shetlands or the Antarctic Peninsula, which is contrary to expectations from a biological point of view. These results probably reflect the differential attention paid to this group in these regions. The distribution of bacteria also supports this idea.

To determine the actual distribution of these organisms the absence of parasites or pathogens in Antarctica must be considered as well. However, only nine out of 98 studies reported negative findings (i.e., Merino et al. 1997, Bonnedahl et al. 2005). This kind of information is as important as positive findings as it may aid to establish the time they may have been present, to determine the causes of their presence and to evaluate their impact on Antarctic fauna. To obtain the required information sample sizes have to be sufficiently large for results to be reliable (Bonnedahl et al. 2005). The techniques used to detect the pathogens are also important, as in some cases the presence of these organisms is extrapolated from serological methods (i.e., Gardner et al. 1997). The presence of antibodies suggests the exposure to a pathogen, but does not necessarily indicate its presence in that particular place, because the contact may have occurred elsewhere or in a particular time because the organisms may not always be present. This is especially important in migratory species such as skuas, gulls or terns. Moreover, it may indicate only the presence of a serologically related nonpathogenic organism (Kerry et al. 1999). Even given how little is known about endemic pathogen it is possible that our available test react with similar but as yet unknown organisms. Therefore, the presence of pathogenic organisms inferred from antibodies in either species or location should be taken with caution, and studies addressing their isolation should be encouraged.

The effects of parasites in Antarctic birds have been studied little. Ixodes uriae has attracted more attention than any other parasite (Gauthier-Clerc et al. 1998; Bergstrom et al. 1999a, b; Mangin et al. 2003 among others). In general, ticks may be causing delayed growth (Moreby 1996) and mortality in chicks (Bergstrom et al. 1999a), affecting the host population dynamics (Boulinier and Danchin 1996). Other parasites have been given less attention, and studies dealing with the effects of parasites may be considered almost anecdotic (e.g., Quillfeldt et al. 2004 for effects of chewing lice on physiology). Therefore, because of the lack of studies, the probable effects of parasites on Antarctic avifauna must be extrapolated from information taken in other organisms or in other latitudes, reducing its reliability. Therefore, further studies are required to shed light on the situation.

Another gap in the information reviewed is that most of the publications only provide descriptive data about the presence of the parasites, pathogens or diseases, and only a few give information on the prevalence and/or intensity of parasitism. Only 16 out of 101 papers reviewed focused on physiology related to parasitism or diseases, and most of these were in penguins.

Thus, it may be concluded that the information published about diseases and parasites in Antarctic birds is scarce and fragmental. Moreover, some studies were undertaken at least 20 years ago and in others pathogens were detected through traditional techniques, which are less reliable than modern molecular methods. Overall little is known about which diseases are endemic or exotic. Knowledge about the presence of disease and parasites is crucial to understand how Antarctica is functioning in terms of ecosystem health. This information is important to the decision-making process in conservation management. The possibility that emergent infectious diseases could cause a catastrophic extinction of bird populations is a plausible scenario (Van Riper et al. 1986) although there is only one documented case of extinction by infection (Daszak and Cunningham 1999). Antarctica is not beyond this risk, animals affected by new pathogens or parasites can be severely affected due to their less effective immunological systems (Merino et al. 2001). Moreover, the presence of pollutants in the environment can depress the immune system, increasing the magnitude of such effects (Briggs et al. 1997). As infestation by a great number of parasites, like gastrointestinal parasites, is dependent on feeding habits (Hoberg 1996), changes in prey can play an important role in exposure to new parasites. Changes in diet may be a consequence of climate change (Emslie et al. 1998) or overexploitation of krill. We, therefore, need to improve our knowledge of physiological functions, such as the immune system, to understand the biological basis for disease and the effects of parasites.

Another point of critical importance concerning disease in Antarctica is related to public health. Most human emergent infectious diseases are acquired from exposure to pathogens transmitted naturally between animals and humans, that is, by zoonotic transmission and wildlife play a key role by providing reservoirs to unknown pathogens responsible for such diseases (Daszak et al. 2000). Although Antarctica can still be considered an isolated continent, the presence of thousands of people each austral summer could increase the risk of zoonosis, although only a small part of those people have close contact with Antarctic birds or mammals. Influenza, caused by a virus, and Lyme disease, caused by the bacteria Borrelia burgdorferi, are two examples of this kind of potential zoonotic disease.

Finally, Kerry et al. (1999) made several recommendations for reducing the risk of humans introducing disease in Antarctica. These included setting up a “central clearing-house for information on suspected disease occurrences” (Recommendation 4) and “establishment of serum banks” (Recommendation 19). However, 10 years after their presentation to the Antarctic Treaty, to our knowledge, such recommendations have not yet been implemented. Specifically, these two recommendations must be complied with to improve our knowledge about the health of bird and mammals populations in Antarctica to help prevent outbreaks or make decisions when they occur.

References

  1. Alexander DJ, Manvell RJ, Collins Ms, Brockman SJ, Westbury HA, Morgan I, Austin FJ (1989) Characterization of paramyxoviruses isolated from penguins in Antarctica and Sub-Antarctica during 1976–1979. Arch Virol 109:135–143. doi:10.1007/BF01310525

    PubMed  CAS  Article  Google Scholar 

  2. Andersen KI, Lysfjord S (1982) The functional morphology of the scolex of two Tetrabothrius Rudolphi 1819 species (Cestoda: Tetrabothriidae) from penguins. Parasitol Res 67:299–307

    Google Scholar 

  3. Austin FJ, Webster RG (1993) Evidence of ortho- and paramyxoviruses in fauna from Antarctica. J Wildl Dis 29:568–571

    PubMed  CAS  Google Scholar 

  4. Banks JC, Palma RL, Paterson AM (2006) Cophylogenetic relationships between penguins and their chewing lice. J Evol Biol 19:156–166. doi:10.1111/j.1420-9101.2005.00983.x

    PubMed  CAS  Article  Google Scholar 

  5. Baumeister E, Leotta G, Pontoriero A, Campos A, Montalti D, Vigo G, Pecoraro M, Savy V (2004) Serological evidences of influenza A virus infection in Antarctica migratory birds. Int Congr Ser 1263:737–740. doi:10.1016/j.ics.2004.02.099

    Article  Google Scholar 

  6. Bell PJ, Burton HR, van Franeker JA (1988) Aspects of the biology of Glaciopsyllus antarcticus (Siphonaptera: Ceratophyllidae) during the breeding season of a host (Fulmarus glacialoides). Polar Biol 8:403–410. doi:10.1007/BF00264716

    Article  Google Scholar 

  7. Bergstrom S, Haemig PD, Olsen B (1999a) Increase mortality of black-browed albatross chicks at a colony heavily-infested with the tick Ixodes uriae. Int J Parasitol 29:1359–1361. doi:10.1016/S0020-7519(99)00088-0

    PubMed  CAS  Article  Google Scholar 

  8. Bergstrom S, Haemig PD, Olsen B (1999b) Distribution and abundance of the tick Ixodes uriae in a diverse subantarctic community. J Parasitol 85:25–27. doi:10.2307/3285694

    PubMed  CAS  Article  Google Scholar 

  9. Bonnedahl J, Broman T, Waldenström J, Palmgren H, Niskanen T, Olsen B (2005) In search of human-associated bacterial pathogens in Antarctic wildlife: report from six penguin colonies regularly visited by tourists. Ambio 34:430–432

    PubMed  Google Scholar 

  10. Botzler RG (1991) Epizootiology of avian cholera in wild fowl. J Wildl Dis 27:367–395

    PubMed  CAS  Google Scholar 

  11. Boulinier T, Danchin E (1996) Population trends in kittiwake Rissa tridactyla colonies in relation to tick infestation. Ibis 138:326–334. doi:10.1111/j.1474-919X.1996.tb04345.x

    Article  Google Scholar 

  12. Briggs KT, Gershwin E, Anderson DW (1997) Consequences of petrochemical ingestion and stress on the immune system of seabirds. ICES J Mar Sci 54:718–725. doi:10.1006/jmsc.1997.0254

    Article  Google Scholar 

  13. Broman T, Bergstrom S, On SLW, Palmgren H, McCafferty DJ, Sellin M, Olsen B (2000) Isolation and characterization of Campylobacter jejuni subsp jejuni from macaroni penguins (Eudyptes chrysolophus) in the subantarctic region. Appl Environ Microbiol 66:449–452

    PubMed  CAS  Article  Google Scholar 

  14. Brown DA (1966) Breeding biology of the Snow Petrel Pagodroma nivea (Forster) ANARE (Aust Nat Antarct Res Exp). Sci Rep Ser B 89:1–63

    Google Scholar 

  15. Cameron AS (1968) The isolation of a psittacosis-lymphogranuloma venerium (PL) agent from an emperor penguin (Aptenodytes forsteri) chick. Aust J Exp Biol Med Sci 46:647–649. doi:10.1038/icb.1968.172

    PubMed  CAS  Article  Google Scholar 

  16. Chastel O, Beaucournu JC (1992) Notes sur la specificite et l’eco-ethologie des puces d’oiseaux aux Iles Kerguelen (Insecta; Siphonaptera). Ann Parasitol Hum Comp 67:213–220

    Google Scholar 

  17. Chastel C, Demazure M, Chastel O, Genevois F, Legrand MC, Gralet O, Odernatt M, Legoff F (1993) A rickettsia-like organism from Ixodes uriae ticks collected on the Kerguelen Islands (French sub-Antarctic territories). Acta Virol 37:11–20

    PubMed  CAS  Google Scholar 

  18. Cielecka D, Zdzitowiecki K (1981) The tapeworm Microsomacanthus shetlandicus sp. n. (Hymenolepididae) from the Dominican gull of King George Island (South Shetlands, Antarctic). Bull Acad Pol Sci Biol 29:173–180

    Google Scholar 

  19. Cielecka D, Wojciechowska A, Zdzitowiecki K (1992) Cestodes from penguins on King George Island (South Shetlands, Antarctic). Acta Parasitol 37:65–72

    Google Scholar 

  20. Clarke J, Kerry K (2000) Diseases and parasites of penguin. Penguin Conserv 13:5–24

    Google Scholar 

  21. Clay T, Moreby C (1970) Mallophaga and Anoplura of Subantarctic islands. Pac Insect Monogr 23:216–220

    Google Scholar 

  22. Curry CH, McCarthy JS, Darragh HM, Wake RA, Todhunter R, Terris J (2002) Could tourist boots act as vectors for disease transmission in Antarctica? J Travel Med 9:190–193

    PubMed  CAS  Google Scholar 

  23. Daszak P, Cunningham AA (1999) Extinction by infection. Trends Ecol Evol 14:279. doi:10.1016/S0169-5347(99)01665-1

    PubMed  Article  Google Scholar 

  24. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287:443–449. doi:10.1126/science.287.5452.443

    PubMed  CAS  Article  Google Scholar 

  25. De Meillon B (1952) The fleas of seabirds in the Southern Ocean. ANARE Report Series B, vol 1. Zoology

  26. Dimitrova ZM, Chipev NH, Georgiev BB (1996) Record of Corynosoma pseudohamanni Zdzitowiecki, 1984 (Acanthocephala, Polymorphidae) in birds at Livingston Island, South Shetlands, with a review of Antarctic avian acanthocephalans. Bulg Antarct Res Life Sci 1:102–110

    Google Scholar 

  27. Emslie S, Fraser W, Smith RC, Walder W (1998) Abandoned penguin colonies and environmental change in the Palmer Station area, Anvers Island, Antarctic Peninsula. Antarct Sci 10:257–268. doi:10.1017/S0954102098000352

    Article  Google Scholar 

  28. Epstein PR, Chivian E, Frith K (2003) Emerging diseases threaten conservation. Environ Health Perspect 111:A506–A507

    PubMed  Google Scholar 

  29. Feiler K (1986) Trematoden aus Chionis alba und Larus dominicanus von den Süd-Shetland-Inseln (Antarktis). Angew Parasitol 27:23–33

    Google Scholar 

  30. Fredes F, Raffo E, Muñoz P, Herrera M (2006) Fauna parasitaria gastrointestinal en polluelos de Pingüino papua (Pygoscelis papua) encontrados muertos en zona antártica especialmente protegida (ZAEP Nº 150). Parasitol Latinoam 61:179–182

    Article  Google Scholar 

  31. Fredes F, Raffo E, Muñoz P (2007a) First report of Cryptosporidium spp. Oocysts in stool of Adelie penguin from the Antarctic using acid-fast stain. Antarct Sci 19:437–438

    Google Scholar 

  32. Fredes F, Madariaga C, Raffo E, Valencia J, Herrera M, Godoy C, Alcaino H (2007b) Gastrointestinal parasite fauna of gentoo penguins (Pygoscelis papua) from the Peninsula Munita, Bahía Paraiso, Antarctica. Antarct Sci 19:93–94

    Google Scholar 

  33. Fredes F, Diaz A, Raffo E, Muñoz P (2008) Cryptosporidium spp. Oocysts detected using acid-fast stain in faeces of gentoo penguins (Pygoscelis papua) in Antarctica. Antarct Sci 20:495–496. doi:10.1017/S0954102008001296

    Article  Google Scholar 

  34. Frenot Y, de Oliveria E, Gauthier-Clerc M, Dennff J, Bellido A, Vernon P (2001) Life cycle of the tick Ixodes uriae in penguin colonies: relationships with host breeding activity. Int J Parasitol 31:1040–1047. doi:10.1016/S0020-7519(01)00232-6

    PubMed  CAS  Article  Google Scholar 

  35. Frenot Y, Chown SL, Whinam J, Selkirk PM, Convey P, Skotnicki M, Bergstrom DM (2005) Biological invasions in the Antarctic: extent, impacts and implications. Biol Rev Camb Philos Soc 80:45–72. doi:10.1017/S1464793104006542

    PubMed  Article  Google Scholar 

  36. Friend M (2006) Evolving changes in diseases of waterbirds. In: Boere GC, Galbraith CA, Stroud DA (eds) Waterbirds around the world. The Stationery Office, Edinburgh, pp 412–417

    Google Scholar 

  37. Gardner H, Kerry K, Riddle M, Brouwer S, Gleeson L (1997) Poultry virus infection in Antarctic penguins. Nature 387:245. doi:10.1038/387245a0

    PubMed  CAS  Article  Google Scholar 

  38. Gauthier-Clerc M, Clerguin Y, Handrich Y (1998) Hyperinfestation by ticks Ixodes uriae: a possible cause of death in adult king penguins, a long-lived seabird. Colon Waterbirds 21:229–233. doi:10.2307/1521910

    Article  Google Scholar 

  39. Gauthier-Clerc M, Jaulhac B, Frenot Y, Bachelard C, Monteil H, Le Maho Y, Handrich Y (1999) Prevalence of Borrelia burgdorferi (the Lyme disease angent) antibodies in king penguin Aptenodytes patagonicus in Crozet Archipielago. Polar Biol 22:141–143. doi:10.1007/s003000050402

    Article  Google Scholar 

  40. Gauthier-Clerc M, Eterradossi N, Toquin D, Guittet M, Kuntz G, Le Maho Y (2002) Serological survey of the king penguin Aptenodytes patagonicus, in Crozet archipielago for antibodies to infectious bursal disease influenza A and Newcastle disease virus. Polar Biol 25:316–319

    Google Scholar 

  41. Georgiev BB, Vasileva GP, Chipev NH, Dimitrova ZM (1996) Cestodes of seabirds at Livingston Island, South Shetlands. Bulg Antarct Res Life Sci 1:111–127

    Google Scholar 

  42. Golemansky V (2003) Eimeria pygosceli n. sp. (Coccidia: Eimeriidae) from the penguins (Pygoscelidae) of the Livingston Island (the Antarctic). Acta Zool Bulg 55:3–8

    Google Scholar 

  43. Graczyk TK, Cranfield MR, Brossy JJ, Cockrem JF, Jouventin P, Seddon PJ (1995) Detection of avian malaria infections in wild and captive penguins. J Helmitol Soc Wash 62:135–141

    Google Scholar 

  44. Grenfell BT, Dobson AP (1995) Ecology of infection diseases in natural populations. Cambridge University Press, Cambridge

    Google Scholar 

  45. Haldane JBS (1949) Disease and evolution. Ric Sci Suppl A 19:68–76

    Google Scholar 

  46. Harkinezhad T, Geens T, Vanrompay D (2009) Chlamydophila psittaci infections in birds: a review with emphasis on zoonotic consequences. Vet Microbiol 135:68–77. doi:10.1016/j.vetmic.2008.09.046

    PubMed  Article  Google Scholar 

  47. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2163. doi:10.1126/science.1063699

    PubMed  CAS  Article  Google Scholar 

  48. Herrmann B, Rahman R, Bergstrom S, Bonnedahl J, Olsen B (2000) Chlamydophila abortus in a Brown Skua (Catharacta antarctica lonnbergi) from a subantarctic island. Appl Environ Microbiol 66:3654–3656. doi:10.1128/AEM.66.8.3654-3656.2000

    PubMed  CAS  Article  Google Scholar 

  49. Hillgarth N, Wingfield JC (1997) Parasite-mediated sexual selection: endocrine aspects. In: Clayton DH, Moore J (eds) Host-parasite evolution. General principles and avian models. Oxford University Press, Oxford, pp 78–104

    Google Scholar 

  50. Hoberg EP (1984) Trematode parasites of marine birds in Antarctica: the distribution of Gymnophallus deliciosus (Olsson 1893). Antarct J US 19:159–160

    Google Scholar 

  51. Hoberg EP (1986a) Aspects of ecology and biogeography of Acantocephala in Antarctic seabirds. Ann Parasitol Hum Comp 61:199–214

    Google Scholar 

  52. Hoberg EP (1986b) Eulindana rauschorum n. sp. a filarioid nematode (Lemdaninae) from Larus dominicanus in Antarctica with comments on evolution and biogeography. J Parasitol 72:755–761. doi:10.2307/3281469

    PubMed  CAS  Article  Google Scholar 

  53. Hoberg EP (1987a) Tetrabothrius shinni sp. nov. (Eucestoda) from Phalacrocorax atriceps bransfieldensis (Pelecaniformes) in Antarctica with comments on morphological variation host-parasite biogeography and evolution. Can J Zool 65:2969–2975. doi:10.1139/z87-450

    Article  Google Scholar 

  54. Hoberg EP (1987b) Reighardia sternae (Diesing, 1864) from seabirds in Antarctica. Can J Zool 65:1289–1291. doi:10.1139/z87-203

    Article  Google Scholar 

  55. Hoberg EP (1996) Faunal diversity among avian parasite assemblages: the interaction of history, ecology and biogeography in marine systems. Bull Scand Soc Parasitol 6:65–89

    Google Scholar 

  56. Hochachka WM, Dhondt AA (2000) Density-dependent decline of host abundance resulting from a new infectious disease. Proc Natl Acad USA 97:5303–5306. doi:10.1073/pnas.080551197

    CAS  Article  Google Scholar 

  57. Horne PA, Rounsevell D (1982) A Collection of feather mites (Acari: Astigmata) from Greater (Eastern) Antarctica. Pac Insects 24:196–197

    Google Scholar 

  58. Howie CA, Jones NV, Williams IC (1968) A report on the death of sheathbills Chionis alba (Gmelin) at Signy Island, South Orkney Islands during the winter of 1965. Br Antarct Surv Bull 18:79–83

    Google Scholar 

  59. Hubalek Z (2004) An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis 40:639–659

    PubMed  Google Scholar 

  60. Ikonicoff S, Zunino CH, Castrelos OD, Margni RA (1981) Microbiología antártica: nuevos estudios efectuados en Bahía Esperanza. Contrib Cient Inst Antart Argent 362:1–19

    Google Scholar 

  61. IPCC (2007) Climate Change 2007: The physical science basis. Contribution of working group I to the fourth assessment report of the IPCC. In: Solomon S, Qin D, Manning M, Chen Z, Marguis M, Averyt K, Tignor MMB, Miler Jr HL (eds) Cambridge University Press for the Intergovernmental Pannel of Climate Change, Cambridge

  62. Ippen R, Henne D (1989) Weitere Sarcocystisbefunde bei Vogeln und Saugetieren der Antarktis. Erkrg Zootiere 31:371–376

    Google Scholar 

  63. Ippen R, Odening K, Henne D (1981) Cestode Parorchites zederi and sarcosporidian Sarcocystis spp. Infections in penguins of the South Shetland Islands. Erkrg Zootiere 22:203–210

    Google Scholar 

  64. Jarecka L, Ostas J (1984) Hymenolepis arctowskii sp. n. (Cestoda, Hymenolepididae) from Larus dominicanus Licht. of the Antarctic. Acta Parasitol Pol 29:189–196

    Google Scholar 

  65. Jensen T, Van de Bildt M, Dietz HH, Andersen TH, Hammer AS, Kuiken T, Osterhaus A (2002) Another phocine distemper outbreak in Europe. Science 297:209. doi:10.1126/science.1075343

    PubMed  CAS  Article  Google Scholar 

  66. Jones NV (1963) The sheathbill Chionis alba (Gmelin) at Signy Island, South Orkney Islands. Br Antarct Surv Bull 2:53–71

    CAS  Google Scholar 

  67. Jones HI (1988) Notes on parasites in penguins (Spheniscidae) and petrels (Procellariidae) in the Antarctic and sub-Antarctic. J Wildl Dis 24:166–167

    PubMed  CAS  Google Scholar 

  68. Jones NV, Williams IC (1967) The cestode parasites of the sheathbill Chionis alba (Gmelin) from Signy Island, South Orkney Islands. J Helminthol 41:151–160

    Article  Google Scholar 

  69. Jones NV, Williams IC (1968) The trematode parasites of the sheathbill Chionis alba (Gmelin) from Signy Island, South Orkney Islands. J Helminthol 42:65–80

    Article  Google Scholar 

  70. Jones NV, Williams IC (1969a) The nematode and acanthocephalan parasites of sheathbill, Chionis alba (Gmelin) at Signy Island, South Orkney Islands and a summary of host parasite relationships in the sheathbill. J Helminthol 43:59–67

    PubMed  CAS  Article  Google Scholar 

  71. Jones NV, Williams IC (1969b) Paramonostomum signiensis n. sp. (Trematoda: Notocotylidae) from the sheathbill Chionis alba. J Helminthol 43:53–57

    PubMed  CAS  Article  Google Scholar 

  72. Jones HI, Gallagher JM, Miller GD (2002) Survey of South Polar Skuas (Catharacta maccormicki) for blood parasites in the Vestfold Hills region of Antarctica. J Wildl Dis 38:213–215

    PubMed  Google Scholar 

  73. Jorge MC, Najle R, Montalti D (2002) Cloacal bacterial flora on Antarctic birds. Riv Ital Orn 71:163–169

    Google Scholar 

  74. Kerry K, Riddle M, Clarke K (1999) Diseases of Antarctic wildlife. A report for SCAR and COMNAP. SCAR

  75. Laurance WF, McDonald KR, Speare R (1996) Epidemic disease and the catastrophic decline of Australian rain forest frogs. Conserv Biol 10:406–413. doi:10.1046/j.1523-1739.1996.10020406.x

    Article  Google Scholar 

  76. Leotta GA, Cerda R, Coria NR, Montalti D (2001) Preliminary studies on some avian diseases in Antarctic birds. Pol Polar Res 22:227–231

    Google Scholar 

  77. Leotta GA, Pare JA, Sigler L, Montalti D, Vigo G, Petruccelli M, Reinoso EH (2002) Thelebolus microsporus mycelial mats in the trachea of wild brown skua (Catharacta antarctica lonnbergi) and south polar skua (C. maccormicki) carcasses. J Wildl Dis 38:443–447

    PubMed  Google Scholar 

  78. Leotta GA, Rivas M, Chinen I, Vigo GB, Moredo FA, Coria N, Wolcott MJ (2003) Avian cholera in a southern giant petrel (Macronectes giganteus) from Antarctica. J Wildl Dis 39:732–735

    PubMed  CAS  Google Scholar 

  79. Leotta GA, Vigo GB, Giacoboni G (2006a) Isolation of Campylobacter lari from seabirds in Hope Bay, Antarctica. Pol Polar Res 27:303–308

    Google Scholar 

  80. Leotta GA, Chinen I, Vigo GB, Pecoraro M, Rivas M (2006b) Outbreaks of avian cholera in Hope Bay, Antarctica. J Wildl Dis 42:259–270

    PubMed  CAS  Google Scholar 

  81. MacCormack WP, Vazquez SC, Montalti D (1998) Studies on the bacterial flora associated to the brown skua (Catharacta antarctica lonnbergi). Ber z. Polarforschung 299:182–185

    Google Scholar 

  82. MacDonald DM, Conroy JWH (1971) Virus disease resembling puffinosis in the gentoo penguin (Pygoscelis papua). Br Antarct Surv Bull 60:80–83

    Google Scholar 

  83. Mangin S, Gauthier-Clerc M, Frenot Y, Gendner JP, Le Maho Y (2003) Ticks Ixodes uriae and the breeding performance of a colonial seabird, King penguin Aptenodytes patagonicus. J Avian Biol 34:30–34. doi:10.1034/j.1600-048X.2003.02916.x

    Article  Google Scholar 

  84. Margni RA, Castrelos OD, Herrera ME (1967) Estudios bacteriológicos del contenido gastrointestinal y cloacal de pingüinos antárticos. Contrib Cient Inst Antart Argent 102:1–19

    Google Scholar 

  85. Martinez-Abrain A, Esparza B, Oro D (2004) Lack of blood parasites in bird species: absence of blood parasite vector explain it all? Ardeola 51:225–232

    Google Scholar 

  86. Mawson PM (1953) Parasitic nematoda collected by the Australian National Antarctic Research Expedition: Heard Island and Macquarie Island 1948–1951. Parasitology 43:291–297

    PubMed  CAS  Article  Google Scholar 

  87. Merino S, Barbosa A, Moreno J, Potti J (1997) Absence of haematozoa in a wild chinstrap penguin Pygoscelis antarctica population. Polar Biol 18:227–228. doi:10.1007/s003000050181

    Article  Google Scholar 

  88. Merino S, Martinez J, Møller AP, Barbosa A, de Lope F, Rodriguez-Caabeiro F (2001) Physiological and hematological consequences of a novel parasite on the red-rumped swallow Hirundo rustica. Int J Parasitol 31:1187–1193. doi:10.1016/S0020-7519(01)00243-0

    PubMed  CAS  Article  Google Scholar 

  89. Miller GD, Couch L, Duszynski DW (1993) Preliminary survey for coccidian parasites in the birds of Cape Bird, Ross Island. Antarct J US 28:148

    Google Scholar 

  90. Miller GD, Watts JM, Shellam GR (2008) Viral antibodies in South Polar Skuas around Davis Station, Antarctica. Antarct Sci 20:455–461. doi:10.1017/S0954102008001259

    Article  Google Scholar 

  91. Mironov SV (1991) Two new species of the feather mites superfamily Analgoidea from the Antarctic birds. Inf Byull Sov Antarkt Eksped 116:69–75

    Google Scholar 

  92. Mironov SV (2000) A review of the feather mite genus Scutomegninia Dubinin, 1951 (Acarina: Analgoidea: Avenzoariidae). Acarina 8:9–58

    Google Scholar 

  93. Møller AP (1997) Parasitism and the evolution of host life history. In: Clayton DH, Moore J (eds) Host-parasite evolution. General principles and avian models. Oxford University Press, Oxford, pp 105–127

    Google Scholar 

  94. Møller AP, De Lope F, Moreno J, Gonzalez G, Perez JJ (1994) Ectoparasites and host energetics: house martin bugs and house martin nestlings. Oecologia 98:263–268. doi:10.1007/BF00324213

    Article  Google Scholar 

  95. Moore BW, Cameron AS (1969) Chlamydia antibodies in Antarctic fauna. Avian Dis 13:681–684. doi:10.2307/1588545

    PubMed  CAS  Article  Google Scholar 

  96. Moreby YE (1996) The abundance and effects of ticks (Ixodes uriae) on nestling Cassin’s auklets (Ptychorramphus aleuticus) at Triangle island, British Columbia. Can J Zool 74:1585–1589. doi:10.1139/z96-172

    Article  Google Scholar 

  97. Morgan IR, Westbury HA (1981) Virological studies of Adelie penguin (Pygoscelis adeliae) in Antarctica. Avian Dis 25:1019–1026. doi:10.2307/1590077

    PubMed  CAS  Article  Google Scholar 

  98. Morgan IR, Westbury AS (1988) Studies of viruses in penguins in the Vestfold Hills. Hydrobiologia 165:263–269. doi:10.1007/BF00025595

    Article  Google Scholar 

  99. Morgan IR, Westbury HA, Caple IW, Campbell J (1981) A survey of virus infection in sub-Antarctic penguins on Macquarie Island, Southern Ocean. Aust Vet J 57:333–335. doi:10.1111/j.1751-0813.1981.tb05839.x

    PubMed  CAS  Article  Google Scholar 

  100. Morishita TY, Aye PP, Ley EC, Harr BC (1999) Survey of pathogens and blood parasites in free-living passerines. Avian Dis 43:549–552. doi:10.2307/1592655

    PubMed  CAS  Article  Google Scholar 

  101. Munyer PD, Holloway HL Jr (1990) Renicola williamsi n. sp. (Trematoda: Digenea: Renicolidae) from the south Polar skua, Catharacta maccormiki. Trans Am Microsc Soc 109:98–102. doi:10.2307/3226600

    Article  Google Scholar 

  102. Murray MD, Vestjens WJM (1967) Studies on the ectoparasites of seals and penguins. Aust J Zool 15:715–725. doi:10.1071/ZO9670715

    Article  Google Scholar 

  103. Murray MD, Orton MN, Cameron AS (1967) The Antarctic Flea Glaciopsyllus antarctica Smit and Dunnet. Antarct Res Ser 10:393–395

    Google Scholar 

  104. Murray MD, Palma RL, Pilgrim RLC (1991) Ectoparasites of Australian, New Zealand and Antarctic birds. Appendix I. In: Marchant S, Higgins PJ (eds) Handbook of Australian, New Zealand and Antarctic birds, vol I. Part A. Oxford University Press, Melbourne

    Google Scholar 

  105. Muzaffar SB, Jones IL (2004) Parasites and diseases of the auks (alcidae) of the world and their ecology—a review. Mar Ornithol 32:121–146

    Google Scholar 

  106. Nievas VF, Leotta GA, Vigo GB (2007) Subcutaneous clostridial infection in Adelie penguins in Hope Bay, Antarctica. Polar Biol 30:249–252. doi:10.1007/s00300-006-0179-5

    Article  Google Scholar 

  107. Odening K (1982a) Cestoden aus Flugvogeln der Sudshetlands (Antarktis) und der Falklandinseln (Malwinen). Angew Parasitol 23:202–223

    PubMed  CAS  Google Scholar 

  108. Odening K (1982b) Paramonostomum antarcticum (Trematoda, Nocotylidae) in Larus dominicanus der Südshetlands (Antarktis). Angew Parasitol 23:137–143

    PubMed  CAS  Google Scholar 

  109. Oelke H, Steiniger F (1973) Salmonella in adelie penguins (Pygoscelis adeliae) and south polar skuas (Catharacta maccormicki) on Ross Island, Antarctica. Avian Dis 17:568–573. doi:10.2307/1589155

    PubMed  CAS  Article  Google Scholar 

  110. Olsen B, Bergstrom S, McCafferty DJ, Sellin M, Wistrom J (1996) Salmonella enteriditis in Antarctica: zoonosis in man or humanosis in penguins. Lancet 348:1319–1320. doi:10.1016/S0140-6736(05)65807-2

    PubMed  CAS  Article  Google Scholar 

  111. Palma RL, Horning DS (2002) The lice (Insecta: Phtiraptera) from Macquaire Island. ANARE Res Notes 148:1–36

    Google Scholar 

  112. Palmgrem H, McCafferty D, Aspan A, Broman T, Sellin M, Wollin R, Bergstrom S, Olsen B (2000) Salmonella in sub-Antarctica: low heterogeneity in Salmonella serotypes in South Georgia seals and birds. Epidemiol Infect 125:262–275

    Google Scholar 

  113. Parmelee DF, Maxson SJ, Berstein NP (1979) Fowl cholera outbreak among brown skuas at Palmer Station. Antarct J US 14:168–169

    Google Scholar 

  114. Peirce MA, Prince PA (1980) Hepatozoon albatrossi sp nov. (Eucoccida: Hepatozidae) from Diomedea spp in the Antarctic. J Nat Hist 14:447–452. doi:10.1080/00222938000770381

    Article  Google Scholar 

  115. Pilgrim RLC (1998) Larvae of the genus Notiopsylla (Siphonaptera: Pygiopsyllidae) with a key to their identification. J Med Entomol 35:362–376

    PubMed  CAS  Google Scholar 

  116. Prudhoe S (1969) Cestodes from fish, birds and whales. BANZARE Rep Ser B VIII(Part 9)

  117. Quillfeldt P, Masello JF, Moestl E (2004) Blood chemistry in relation to nutrition and ectoparasite load in Wilson’s stormpetrels Oceanites oceanicus. Polar Biol 27:168–176. doi:10.1007/s00300-003-0572-2

    Article  Google Scholar 

  118. Rapport DJ (2007) Sustainability science: an ecohealth perspective. Sustain Sci 2:77–84. doi:10.1007/s11625-006-0016-3

    Article  Google Scholar 

  119. Rau ME (1983) Establishment and maintenance of behavioural dominance in male mice infected with Trichinella spiralis. Parasitology 86:319–322

    PubMed  Article  Google Scholar 

  120. Rounsevell DE, Horne PA (1986) Terrestrial, parasitic and introduced invertebrates of the Vestfold Hills. In: Pickard J (ed) Antarctic oasis, terrestrial environments and history of the Vestfold Hills. Academic Press, New York, pp 309–331

    Google Scholar 

  121. Shearn-Boschler V, Green DE, Converse KA, Docherty DE, Thiel T, Geisz HN, Fraser WR, Patterson-Fraser DP (2008) Cutaneous and diphtheritic avian poxvirus infection in a nestling Southern Giant Petrel (Macronectes giganteus) from Antarctica. Polar Biol 31:569–573. doi:10.1007/s00300-007-0390-z

    Article  Google Scholar 

  122. Shirihai H (2002) A complete guide to Antarctic wildlife. The birds and marine mammals of the Antarctic Continent and Southern Ocean. Alula Press Oy, Finland

    Google Scholar 

  123. Simensen E, Olson LD (1980) Aerosol transmission of Pasteurella multocida in turkeys. Avian Dis 24:1007–1010. doi:10.2307/1589975

    PubMed  CAS  Article  Google Scholar 

  124. Steele WK, Pilgrim RLC, Palma RL (1997) Ocurrence of the flea Glacypsillus antarcticus and avian lice in central Droming Maud Land. Polar Biol 18:292–294. doi:10.1007/s003000050190

    Article  Google Scholar 

  125. Steig EJ, Schneider DP, Rutherford RD, Mann ME, Comisso JC, Shindell DT (2009) Warming of the Antarctic ice-sheet surface since the 1957 International Geophysical Year. Nature 457:459–463. doi:10.1038/nature07669

    PubMed  CAS  Article  Google Scholar 

  126. Sutherst RW (2001) The vulnerability of animal and human health to parasites under global change. Int J Parasitol 31:933–948. doi:10.1016/S0020-7519(01)00203-X

    PubMed  CAS  Article  Google Scholar 

  127. Tizard I (2004) Salmonellosis in wild birds. Semin Avian Exotic Pet Med 13:50–66. doi:10.1053/j.saep.2004.01.008

    Article  Google Scholar 

  128. Turner J, Sr Colwell, Marshall GJ, Lachlan-Cope TA, Carleton AM, Jones PD, Lagun V, Reid PA, Iagovkina S (2004) The SCAR READER project: toward a high-quality database of mean Antarctic meteorological observations. J Clim 17:2890–2898. doi:10.1175/1520-0442(2004)017<2890:TSRPTA>2.0.CO;2

    Article  Google Scholar 

  129. Van Riper CI, Goff ML, Laird M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr 56:327–344. doi:10.2307/1942550

    Article  Google Scholar 

  130. Waldenstrom J, Broman T, Carlsson I, Hasselquist D, Achterberg RP, Wanegaar JA, Olse B (2002) Prevalence of Campylobacter jejuni, Campylobacter lari and Campylobacter coli in different ecological guilds and taxa of migrating birds. Appl Environ Microbiol 68:5911–5917. doi:10.1128/AEM.68.12.5911-5917.2002

    PubMed  CAS  Article  Google Scholar 

  131. Wallensten A, Munster VJ, Osterhaus ADME, Waldenstrom J, Bonnedahl J, Broman T, Fouchier RAM, Olsen B (2006) Mounting evidence for the presence of influenza A virus in the avifauna of the Antarctic region. Antarct Sci 18:353–356. doi:10.1017/S095410200600040X

    Article  Google Scholar 

  132. Weimerskirch H (2004) Diseases threaten Southern Ocean albatrosses. Polar Biol 27:374–379. doi:10.1007/s00300-004-0600-x

    Article  Google Scholar 

  133. Whitehead MD, Burton HR, Bell PJ, Arnould JPY, Rounsevell DE (1991) A further contribution on the biology of the Antarctic flea, Glaciopsyllus antarcticus (Siphonaptera: Cerataophyllidae). Polar Biol 11:379–383. doi:10.1007/BF00239690

    Article  Google Scholar 

  134. Williams IC, Jones NV, Payne MJ, Ellis C (1974) The helminth parasites of the sheathbill, Chionis alba and the diving petrels, Pelecanoid georgicus and P. urinatrix at Bird Island, South Georgia. J Helminthol 48:195–197

    PubMed  CAS  Article  Google Scholar 

  135. Wilson N (1970) Acarina: Mesostigmata: Halarachnidae, Rhinonyssidae of South Georgia, Heard and Kerguelen. Pac Insects Monogr 23:71–77

    Google Scholar 

  136. Zdzitowiecki K (1978) Corynosoma shackletoni sp. n. from hosts in South Shetlands and South Georgia (Antarctic). Bull Acad Pol Sci Biol 26:629–634

    Google Scholar 

  137. Zdzitowiecki K (1985) Acanthocephalans of birds from South Shetlands (Antarctic). Acta Parasitol Pol 30:11–24

    Google Scholar 

  138. Zdzitowiecki K, Drozdz J (1980) Redescription of Stegophorus macronectes (Johnston et Mawson, 1942) and description of Stegophorus arctowskii sp. n. (Nematoda, Spirurida) from birds of South Shetlands (the Antarctic). Acta Parasitol Pol 27:205–212

    Google Scholar 

  139. Zdzitowiecki K, Szelenbaum-Cielecka D (1984) Anomotaenia dominicana (Railliet et Henry, 1912) (Cestoda, Dilepididae) from the Dominican gull Larus dominicanus Licht. of the Antarctic. Acta Parasitol Pol 29:49–58

    Google Scholar 

  140. Zdzitowiecki K, Niewiadomska K, Drozdz J (1989) Trematodes of birds and mammals in the environs of H. Arctowski Station (South Shetlands, Antarctic). Acta Parasitol Pol 34:243–257

    Google Scholar 

  141. Zlotorzycka J, Modrzejewska M (1992) Contribution to the knowledge of lice Mallophaga from the Antarctic. Pol Polar Res 13:59–63

    Google Scholar 

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Acknowledgments

This review was done under International Polar Year Project number 172 Birdhealth. This study was supported by Projects CGL2004-01348 and POL2006-05175 funded by the Spanish Ministry of Science and Innovation and by the European Regional Development Fund. MJP was supported by a Ph.D. grant from the Spanish Ministry of Science and Innovation (BES-2005-8465). We specially thank Barbara Wienecke and two anonymous referees for helpful suggestions on an early version of this manuscript. Deborah Faldauer corrected the language.

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Barbosa, A., Palacios, M.J. Health of Antarctic birds: a review of their parasites, pathogens and diseases. Polar Biol 32, 1095 (2009). https://doi.org/10.1007/s00300-009-0640-3

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Keywords

  • Antarctic birds
  • Bacteria
  • Disease
  • Health
  • Parasite
  • Virus