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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.
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.
The information was taken from papers referenced in the Zoological Record and PubMed database and from indepth 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.
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 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 Austrogoniodes mawsoni
Tetrabothrius wrighti
Austrogoniodes mawsoni
Parorchites zederi
Pygoscelis papua
Docophoroides brevis
Naubates fuliginosus
Naubates fuliginosus
Pseudonirmus gurlti
Trabeculus hexacon
Docophoroides brevis
Harrisoniella hopkinsi
Harrisoniella hopkinsi
Paraclisis hyalina
Paraclisis hyalina
Naubates pterodromi
Austromenopon affine
Perineus concinnoides
Episbates pederiformis
Thalassarche melanophrys Halipeurus procellariae
Halipeurus procellariae
Naubates pterodromi
Naubates heteroproctus
Naubates heteroproctus
Saemundssonia sp 1 (14) Trabeculus schillingi
Trabeculus schillingi
Pterodroma mollis Ancistrona sp 1 (98) Longimenopon galeatum
Longimenopon galeatum
Naubates prioni
Naubates prioni
Naubates clypeatus
Halipeurus diversus
Halipeurus turtur
Trabeculus sp 1 (14) Pachyptilla turtur
Naubates prioni 1 (98)
Ixodes kerguelensis
Zachvatkinia robusta
Docophoroides brevis
Naubates fuliginosus
Naubates fuliginosus
Pseudonirmus gurlti
Trabeculus hexacon
Trabeculus hexacon
Procellaria cinerea
Naubates fuliginosus
Trabeculus hexacon
Halipeurus procellariae
Halipeurus diversus
Puffinus griseus
Halipeurus diversus
Trabeculus hexacon
Trabeculus hexacon
Naubates prioni
Notiopsylla kerguelensis
Paramonostomum signiensis
Paramonostomum signiensis
Lateriporus australis
Lateriporus australis
Lateriporus australis
Nototaenia fileri
Nototaenia fileri 1 (78) Gymnophallus deliciosus
Quadraceps ornatus
Diplostomum minutum
Quadraceps ornatus
Diplostomum antarcticum
Saemundssonia lari
Diplostomum dominicanum
Saemundssonia lari
Hymenolepis arctowski
Naubates prioni
Anomotaenia dominicana
Reighardia sternae
Paramonostomum antarcticum 2 (64) Paramonostomum antarcticum 2 (79) Corynosoma shackletoni
Corynosoma shackletoni
Corynosoma hamanni
Gymnophallus deliciosus
Eulimdana rauschorum
Sterna vittata
Quadraceps houri
Saemundssonia lockleyi
Saemundssonia lockleyi 1 (98) A Antibodies, I Zlotorzycka and Modrzejewska (1992) , (56) Bergstrom et al. (1999a) , (57) Weimerskirch (2004), (58) Wilson (1970) , (59) Leotta et al. (2003) , (60) , (61) Bell et al. (1988) , (62) Rounsevell and Horne (1986) , (63) Horne and Rounsevell (1982) , (64) Odening (1982b) , (65) Brown (1966) , (66) Pilgrim (1998) , (67) Chastel and Beaucournu (1992) , (68) Mironov ( 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 clearinghouse 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.
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