Author/s Andres Barbosa* (1#), Erli Schneider Costa (2#), Meagan Dewar (3#), Daniel González-Acuña (4#), Rachael Gray (5#), Michelle Power (6#), Ralph Eric Thijl Vanstreels (7) (1) Museo Nacional de Ciencias Naturales, CSIC, Spain (2) Universidade Estadual do Rio Grande do Sul and APECS-Brazil, Brazil (3) Deakin University, APECS-Oceania, IPECS (International Penguin Early Career Scientists), Australia (4) Universidad de Concepción, Chile (5) The University of Sydney, Australia (6) Macquarie University, Australia (7) Universidade de São Paulo, Brazil # Working Group of Health Monitoring of Antarctic Bird and Marine Mammals (EGBAMM-SCAR) Brief Overview There have been relatively few wildlife mass mortality events reported in Antarctica that can be conclusively attributed to infectious disease. Climate change and increasing human activity in the region may increase both the risk of pathogen transmission and the frequency of mortality events. Information on the presence of pathogens and diseases in birds and marine mammals is limited and fragmented, being based on relatively few species and locations. Despite concerns about the introduction of non-endemic pathogens, structured Antarctic wildlife health surveillance programs have not been established, making it difficult to assess the implications of disease for conservation actions. To achieve a sound health surveillance program, long-term investigations are essential to identify both host species and monitoring locations to detect emergent pathogens, as well as to better characterise the viral, microbial and parasitic communities, both native and introduced, in Antarctica and their effects on host physiology, fitness and survival. Detailed Overview Infectious disease is one of the main causes of mortality in wild animals worldwide. Moreover, pathogens and parasites can cause sub-lethal effects to hosts, such as the reduction in reproductive output by physiological changes, which can in turn contribute to population decline. Infections can also interact with toxins (such as persistent organic pollutants) (1) increasing the host vulnerability to secondary infections from other pathogens and parasites, or reduce the ability of animals to accommodate to extreme environmental changes. Emerging infectious disease also presents a significant threat to populations, particularly when a species is unable to mount an effective immune response to novel pathogens with which it did not co-evolve. Antarctica is relatively isolated from other regions of the world, and communities of microorganisms there may differ from those of other regions of the planet. As a result, vertebrate species that inhabit the Antarctic environment may not have been exposed for long periods to many microorganisms (including pathogens) and, having not co-evolved with them, may now fail to produce an effective immune response if exposed. Another factor increasing the risk of a disease outbreak in Antarctic wildlife is that many bird and mammals live in dense aggregations which increase the probability of infectious disease transmission. However, the environmental conditions, particularly in terms of temperature and humidity, may render it very difficult for introduced microorganisms (or their invertebrate vectors/hosts) to thrive in this region. As a result, many pathogens, particularly those transmitted by vectors and those that have temperature/moisture thresholds for effective transmission, could have limited capability to disperse and cause disease outbreaks. Investigation of the health of Antarctic wildlife is therefore crucial to assessing the risk of disease outbreaks and pathogen introduction. Information relating to disease in Antarctic species, including causative agents, pathogenicity, prevalence and geographic range, is both limited and fragmented (2, 3, 4). Data from zoo animals, especially penguins, has, however, established their susceptibility to a wide range of diseases (2). Moreover, climate change is predicted to shift the global distribution of some pathogens and parasites (5). Climate change has already affected the distribution of some bird species and can affect the life cycle patterns and physiology of Antarctic birds and marine mammals, which could facilitate the exposure to pathogens or reduce the effectiveness of the immune response to infectious disease. Current knowledge of infectious diseases in Antarctic birds and marine mammals has been the subject of several reviews (2, 3,4). Here we focus on viruses, bacteria and protozoa due to their greater potential for outbreaks and host switching when compared to macroparasites (living both externally and internally on the animals) that can have more complex life cycles. A broad variety of pathogens and infectious diseases has been reported in seabirds in Antarctica and the Sub-Antarctic, either through direct evidence of infection or through serological evidence (Table 1). Table 1: Pathogens, and potential pathogenic microorganisms recorded in seabirds from the Antarctic (above 60ºS)(A) or Sub-Antarctic (below 60ºS)(S). References in square brackets. Direct evidence Serological evidence Viral Infectious Bursal Disease Virus (A)) , Influenza virus A (Low Pathogenic strains) (A)(S), Newcastle Disease Virus (A), Petrelpox Virus (A), Paramyxoviridae (A)(S) (unidentified strains)) Infectious Bursal Disease Virus (A)(S) , Influenza virus A (Low Pathogenic strains) (A) , Murray Valley Encephalitis Virus (S)[2,4], Newcastle Disease Virus (S)(A) , Flaviviridae (Kemerovo group, Sakhalin group, other unidentified strains) (S), other Flavirirus not identified (A), Adenovirus (Egg Drop Syndrome) (A) Bacterial Alcaligenes faecalis (A), Bacillus spp. (A), Campylobacter lari (A), Campylobacter jejuni (S), Chlamydophylla spp (A)[], Edwardsiella tarda (A), Erysipelothrix rhusiopathiae (S), Escherichia spp. (A), Enterococcus faecalis (A), Micrococcus sp. (A)), Pasteurella multocida (A,S), Plesiomonas shigelloides (S), Salmonella sp. (A), Staphylococcus saprophyticus (A), Streptococcus fecalis (A), Rickettsia-like organism (S) Borrelia burgdorferi sensu lato (S), Salmonella sp. (A), Chlamydophylla spp. (S), Clostridium sp. (A), Mycoplasma gallisepticum (A), Mycoplasma synoviae (A) Protozoal Cryptosporidium sp. (A), Eimeria pygosceli (A), Isospora sp. (A), Sarcocystis sp. (A), Hepatozoon albatrossi (S), Plasmodium (Haemamoeba) sp. (S) Unknown etiology Penguin feather-loss disorder (A) [6,7] Knowledge of infectious diseases in marine mammals is less extensive than for seabirds and is restricted to pinnipeds (8), with no information on cetaceans in the Southern Ocean. Salmonella has been described in numerous Antarctic pinniped species (9, 10), Cryptosporidium was detected in a single elephant seal faecal sample (11), and Sealpox Virus has been reported in a Weddell seal (3). The presence of antibodies against several pathogens has been demonstrated in pinnipeds in Antarctica and the Sub-Antarctic (Table 2). Table 2: Pathogens and potential pathogenic microorganisms recorded in marine mammals from the Antarctic (above 60ºS) (A) or Sub-Antarctic (below 60ºS) (S). References in square brackets. Direct evidence Serological evidence Viral Sealpox Virus (A) Canine Distemper Virus (A), Phocine Distemper Virus (A), Phocine Herpesvirus 1 (A,S) Bacterial Campylobacter sp. (A) , Salmonella sp. (A)[9,10], E. coli (A) Acinetobacter calco (S), Bordetella bronchispectica (S), Brucella sp. (A), Corynebacterium sp. (S), Moraxella phylpiruvica (S), Neisseria elongate (S), Proteus sp. (S) Protozoal Cryptosporidium sp. (A)  – Figure 1. Adélie penguin chick showing feather loss disease. This is a recently reported emergent disease affecting Adélie penguin chicks in Antarctic Peninsula and Ross Island. It should be noted though that the presence of antibodies in wildlife means that the animal was exposed to a microorganism and developed an immune response. It does not necessarily indicate that the microorganism caused disease in that individual. Mass mortality events are apparently unusual in Antarctica, which suggests that: a) disease outbreaks and health problems have posed a very low risk to Antarctic wildlife, and/or b) the effects of infectious diseases have been underestimated due to the scarcity of studies and lack of a systematic long-term surveillance for mortality events. To date, only eight recorded mortality events probably caused by diseases have been reported, mainly involving seabirds (Table 3). Table 3: Mass mortality events recorded in Antarctica region in seabirds and marine mammals. Species Description of the event (likely pathogen or disease) Location Reference Gentoo penguin (Pygoscelis papua) Several hundred in the late’ 60 (probably by a virus) Signy Island (60º 43’S 45º 36’W) 14 Adélie penguin (Pygoscelis adeliae) 65% of chicks in 1972 by (unknown) disease Mawson Coast (67º 35’S 62º 45’E) 15 King penguin (Aptenodytes patagonicus) 250-300 in 1992/1993 by (unknown) disease Marion Island (46º 52’S 37º 51’E) 16 Macaroni penguin (Eudyptes chrysolophus) 5000-10000 in 1993 (by conjunctivitis) Marion Island (46º 52’S 37º 51’E) 16 Yellow nose albatross (Thalassarche chlororhynchos) 31 chicks in 1995/1996 and unknown number in 1999 and 2000 (by Erysipelothrix rhusiopathidae, Pasteurella multocida) Amsterdam Island (37º 49’S 77º 33’ E) 17 Adélie penguin, kelp gull (Larus dominicanus), and skua (Catharacta sSp.) 86 birds in 1999/2000 and 2000/2001 (due to avian cholera) Hope Bay (63º 23’S 57º 00’W 18 Amsterdam albatross (Diomediea amsterdamensis) 66% and 74% chicks in 2000 and 2001 respectively (unknown disease) Amsterdam Island (37º 49’S 77º 33’ E) 17 Macaroni penguin (Eudyptes chrysolophus) 2000 in 2004 (due to avian cholera) Marion Island (46º 52’S 37º 51’E) 16 Crabeater seals (Lobodon carcinophagus) 3000 in 1955 (suspected by a virus) Crown Prince Gustav Channel (64º 00’S 57º 45’W) 19 However, in some cases it is difficult to attribute mortality directly to disease, as in the majority of circumstances, limited or no diagnostic investigations have been undertaken. The introduction of pathogens to Antarctic wildlife may arise from two main sources: a) migratory species that disperse over great distances between the Antarctic and other areas (20, 21) (for example, albatrosses, polar skuas, giant petrels, Arctic terns, elephant seals, Antarctic fur seals); or b) through human activity (scientific and associated logistic activities and tourism). Multiple pathways for the introduction of non-endemic species, including direct transport and inadequate management of waste and sewage from ships, research stations and field camps, have the potential to introduce micro-organisms (22). Introduction of novel pathogens through human activities must be one of the principal concerns for long-term conservation of the Antarctic ecosystem. Human presence has increased in the last decades with recent data (2013-2014) from IAATO and COMNAP showing that 37,405 tourists visited Antarctica and at least 4462 researchers plus logistics staff worked in the region in one year. Given the higher density of activities in the Antarctic Peninsula and Ross Sea regions, these areas could have the higher risk of novel pathogens introduction if the pathways are similar to those for the introduction of invasive plant propagules (23). Special attention also needs to be paid to the risk of anthropogenic spread of potential pathogens between locations within Antarctica. Monitoring the health of Antarctic wildlife is a necessary part of good environmental stewardship. Parties have previously recognised the importance of wildlife disease research and the importance of establishing co-ordinated international programmes of research and monitoring, as yet without success. Current knowledge on Antarctic wildlife diseases is limited to only a few research groups studying organisms in their areas of expertise, without any overall framework. This results in a bias towards disease-related information from small geographical regions or on a limited number of species, for example penguins in the South Shetland Islands, with little known or observed data for much of the continent. To address knowledge gaps in Antarctic wildlife health and disease status a working group for health monitoring of Antarctic species has been created within the SCAR Expert Group of Birds and Marine Mammals (EGBAMM). While there are existing tools to assess disease risks for wildlife, for Antarctic wildlife the fragmented and limited nature of available disease information makes their use impossible. Effective health monitoring encompassing long-term studies on a broader number of species and populations at selected sites, including ecological information on Antarctic wildlife, their pathogens and parasites, and resident microbiome, are all required to understand potential risks. The establishment of tissue banks would allow material to be reanalysed in future with new methods whilst the application of genomic techniques could substantially change our understanding of the pathogen/host interactions. Key Events 1964 Agreed Measures for the Conservation of Antarctic Flora and Fauna –initial recognition of the possibility of the accidental introductions of pathogens 1991 Protocol on Environmental Protection to the Antarctic Treaty – Annex II Article 4 and Appendix C and Annex III Article 2 specifically provides prohibitions on introductions of non-native species including viruses, bacteria, yeasts and fungi as well as directions on the treatment of sewage and wastes. 1998 Workshop on diseases of Antarctic wildlife in Australia http://www.ats.aq/documents/SATCM12/att/SATCM12_att002_e.pdf 2000 Introduction by IAATO of mandatory boot washing protocol for tourists. 2001 Report of Open-ended Contact Group on diseases of Antarctic Wildlife- review and risk assessment http://www.ats.aq/documents/ATCM24/wp/ATCM24_wp010_e.pdf 2007-2008 International Polar Year project number 172 BIRDHEALTH: Health of Arctic and Antarctic bird populations. 2007 Symposia on Health of Arctic and Antarctic birds in the 6th European Ornithologists Union in Vienna 2009 Publication of book Health of Antarctic Wildlife edited by KR Kerry and MJ Riddle. 2011 Revised Guidelines for Visitors Resolution 10 www.ats.aq/documents/ATCM34/att/ATCM34_att050_e.doc 2015 Workshop on microbial/parasite impacts on Antarctic wildlife, Sydney, Australia.