IJP: Parasites and Wildlife 12 (2020) 275–290 Contents lists available at ScienceDirect IJP: Parasites and Wildlife journal homepage: www.elsevier.com/locate/ijppaw Arthropod parasites of Antarctic and Subantarctic birds and pinnipeds: A T review of host-parasite associations ∗ Ralph Eric Thijl Vanstreelsa, , Ricardo L. Palmab, Sergey V. Mironovc a Institute of Research and Rehabilitation of Marine Animals, Cariacica, Brazil b Museum of New Zealand Te Papa Tongarewa, Wellington, New Zealand c Zoological Institute, Russian Academy of Sciences, Saint Petersburg, Russia ARTICLE INFO ABSTRACT Keywords: Due to its cold and dry climate and scarcity of ice-free land, Antarctica has one of the most extreme environments Arthropoda on our planet. To survive in the Antarctic region, parasitic arthropods must either remain closely associated with Carnivora their hosts throughout the entire life cycle or develop physiological adaptations to survive in the terrestrial Ecology habitat while their hosts are away foraging at sea or overwintering at lower latitudes. Forty-eight species of birds Parasite and seven species of pinnipeds breed in the Antarctic region, with 158 species/subspecies of parasitic arthropods Polar biology recorded thus far, comprising: sucking lice (Echinophthiriidae), chewing lice (Menoponidae, Philopteridae), Seabird fleas (Ceratophyllidae, Pygiopsyllidae, Rhopalopsyllidae), pentastomes (Reighardiidae), hard ticks (Ixodidae), nest-associated haematophagous mites (Laelapidae), nasal mites (Halarachnidae, Rhinonyssidae) and feather mites (Alloptidae, Avenzoariidae, Xolalgidae, Freyanidae). In this review, we provide an updated compilation of the available information on the host-parasite associations of arthropods infesting birds and pinnipeds in the Antarctic region, and discuss some over-arching ecological patterns and gaps of knowledge. 1. Introduction and are believed to have established prior to the last glacial maximum, displaying a variety of physiological adaptations to these extreme en- Antarctica has one of the most extreme environments on our planet. vironmental conditions (Convey, 2010; Mortimer et al., 2011; Teets and Ice-free areas comprise c. 2.4% of the continent (Drewry et al., 1982), Denlinger, 2014). For parasitic arthropods, survival in the Antarctic and the biomass generated in these scarce ice-free terrestrial ecosystems environment may be achieved by remaining closely associated with the is dwarfed by the astonishing productivity of the Southern Ocean host throughout the entire life cycle, including when the host forages at (Siegfried et al., 1985). As a result, vertebrates breeding in Antarctica sea, or to develop physiological adaptations to survive in the terrestrial and Subantarctic islands rely primarily on marine resources, playing a habitat while the host is away (e.g. cold-hardiness in ticks; Lee and vital ecological role in transferring biomass from the marine to the Baust, 1987). terrestrial environment (Siegfried et al., 1985). Parasites are also im- Studies on arthropod parasites of Antarctic birds and pinnipeds date portant constituents of the biodiversity of the Antarctic region, and can back to the 19th century (e.g. White, 1852; Giebel, 1876; Taschenberg, also have relevance for the conservation of their hosts as they act as 1880), and extensive taxonomic studies were developed well into the stabilizers or destabilizers depending on ecosystem interactions 20th century (e.g. Kéler, 1952; Meillon, 1952; Timmermann, 1965; Clay (Combes, 1996; Kerry and Riddle, 2009; Diaz et al., 2017). Owing to the and Moreby, 1967; Gressitt, 1967; Smit, 1987). However, with a few relative scarcity of biomass production on the terrestrial environment of notable exceptions (e.g. Stefan et al., 2014; Palma, 2017), the 21st Antarctica, parasites of vertebrates represent a substantial component century has arguably seen a decline in the research effort dedicated to of the invertebrate fauna of Antarctica as they are able indirectly to describe and catalogue the parasitic arthropod fauna of Antarctica. This exploit the marine productivity, even those which remain on land is undoubtedly a reflection of the broader problem of the ‘taxonomic during their entire life cycle. impediment’, i.e. the global shortage of professional taxonomists and Freezing and desiccation are key challenges for the survival of in- systematists (Brooks and Hoberg, 2001; Giangrande, 2003). Further- vertebrates in the Antarctic region (Wharton, 2003; Teets and more, the focus of Antarctic research has gradually shifted towards Denlinger, 2014). Most free-living Antarctic arthropods are endemic technology-based methods (e.g. autonomous and remote sensors) and ∗ Corresponding author. E-mail address: [email protected] (R.E.T. Vanstreels). https://doi.org/10.1016/j.ijppaw.2020.03.007 Received 21 February 2020; Received in revised form 27 March 2020; Accepted 28 March 2020 Available online 25 May 2020 2213-2244/ © 2020 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). R.E.T. Vanstreels, et al. IJP: Parasites and Wildlife 12 (2020) 275–290 climate change research (Kennicutt et al., 2014, 2015). Considering the which comprises the Antarctic continent and most Subantarctic islands. high costs associated with maintaining research bases and organizing Fig. 1 represents the Antarctic sub-regions as defined in this study field expeditions to Antarctica and Subantarctic islands, research pro- (adapted from the CCAMLR statistical areas). jects in the region often have to compete for logistical support. Un- All birds and mammals breeding on land in the Antarctic region fortunately, in recent decades the research on the diversity and ecology were considered as ‘Antarctic hosts’, comprising 55 species (48 birds of parasites has lost prominence when competing with more ‘global’ or and 7 mammals), of which 14 breed exclusively in the Antarctic region ‘cutting-edge’ topics. (10 birds and 4 mammals) (Table 1). The taxonomy and the geographic On the other hand, we have recently seen a great improvement in distribution were derived from public datasets (BirdLife International our knowledge about the distribution of the terrestrial Antarctic fauna and Handbook of the Birds of the World, 2019; International Union for through satellite imagery (e.g. Lynch and LaRue, 2014; Borowicz et al., Conservation of Nature and Natural Resources, 2019). Information 2018) and at sea through satellite tracking and geolocation tagging (e.g. about arthropod parasites was obtained from the peer-reviewed lit- Delord et al., 2019; Granroth-Wilding and Phillips, 2019), and about erature and the collection of the Museum of New Zealand (Te Papa) phylogenetic relationships and taxonomy (e.g. Penhallurick and Wink, (https://collections.tepapa.govt.nz/). 2004; Cole et al., 2019). Furthermore, the development of computa- We compiled a dataset of host-parasite-location associations within tional tools to process geographic information (Durr and Gatrell, 2004) the Antarctic region and host-parasite associations outside the Antarctic and analyse networks (Poulin, 2010) has also provided new insight into region (Multimedia Component 1). Subspecies was used as the taxo- the complex relationships among parasites and their hosts. Here, we nomic unit for parasites that show consistent geographical or host provide an updated compilation of the available information on the distribution differences at this rank (e.g. species of Ixodes, Notiopsylla, host-parasite associations of arthropods infesting birds and pinnipeds in Saemundssonia, Quadraceps). We use “stragglers” to refer to parasites the Antarctic region (including Subantarctic islands), and use modern found occasionally on a bird but which appear not to be regular para- analytical tools to evaluate our current state and gaps of knowledge and sites of that host (e.g. ground-nesting birds being temporarily infested to identify over-arching ecological patterns. by parasites from other species breeding nearby), and “contaminants” to refer to parasites transferred to a bird by human agency (e.g. para- 2. Definitions and methods sites transferred due to careless handling of carcasses or museum spe- cimens) (Pilgrim and Palma, 1982). Because there are conflicting definitions of the Antarctic region, for Gephi 0.9.2 (Bastian et al., 2009) was used to analyse the network of the purpose of this review we will refer to the area of the Convention on host-parasite associations (excluding stragglers and contaminants). The the Conservation of Antarctic Marine Living Resources (CCAMLR), ForceAtlas2 algorithm (Jacomy et al., 2014) was used to graphically Fig. 1. Sub-areas of the Antarctic region. Legend: AAP = Antarctic Peninsula (in- cluding South Shetland Islands and Palmer Archipelago), AWS = Antarctica Weddell Sea sector, AAT = Antarctica Atlantic Ocean sector (including Bouvet Island), AIW = Antarctica Indian Ocean West sector, AIE = Antarctica Indian Ocean East sector, ARS = Antarctica Ross Sea sector (including Scott and Balleny Islands), APW = Antarctica Pacific Ocean West sector, APE = Antarctica Pacific Ocean East sector (including Peter I Island), SOI = South Orkney Island, SGI = South Georgia Island, SSI = South Sandwich Islands, PEI = Prince Edward Islands, CRI = Crozet Islands, KEI = Kerguelen Islands, HMI = Heard and McDonald Islands. The Antarctic Polar Front was drawn from