Checklist of marine mammal parasites in New Zealand and Australian waters

Abstract Marine mammals are long-lived top predators with vagile lifestyles, which often inhabit remote environments. This is especially relevant in the oceanic waters around New Zealand and Australia where cetaceans and pinnipeds are considered as vulnerable and often endangered due to anthropogenic impacts on their habitat. Parasitism is ubiquitous in wildlife, and prevalence of parasitic infections as well as emerging diseases can be valuable bioindicators of the ecology and health of marine mammals. Collecting information about parasite diversity in marine mammals will provide a crucial baseline for assessing their impact on host and ecosystem ecology. New studies on marine mammals in New Zealand and Australian waters have recently added to our knowledge of parasite prevalence, life cycles and taxonomic relationships in the Australasian region, and justify a first host–parasite checklist encompassing all available data. The present checklist comprises 36 species of marine mammals, and 114 species of parasites (helminths, arthropods and protozoans). Mammal species occurring in New Zealand and Australian waters but not included in the checklist represent gaps in our knowledge. The checklist thus serves both as a guide for what information is lacking, as well as a practical resource for scientists working on the ecology and conservation of marine mammals.


Introduction
In the oceanic waters around New Zealand (NZ) and Australia, marine mammals are considered as vulnerable wildlife and often endangered due to anthropogenic impacts on their habitat. Strandings of these long-lived top predators and often pelagic species are rare and individuals are seldom available for data collection. A recent assessment has shown that the conservation status of NZ marine mammals has not improved . Furthermore, three endemic NZ marine mammals, i.e. NZ sea lion (Phocarctos hookeri), Hector's dolphin (Cephalorhynchus hectori hectori) (both endangered) and Maui's dolphin (Cephalorhynchus hectori maui) (nationally critical) are regarded as threatened. Thirteen taxa are considered data deficient . Around Australia, at least seven species are classified threatened, among them the iconic blue whale (Balaenoptera musculus), and the conservation status of 25 cetacean species is unknown due to insufficient data (Schumann et al., 2013). Australian and NZ waters include critical feeding and breeding grounds for permanent cetacean residents and visitors that migrate from summer feeding grounds in the Antarctic to the warmer waters of the Australian coast during the winter (Bannister et al., 1996;Salgado Kent et al., 2012). Recent dangers to pinnipeds in Australasian waters include exposure to marine debris and bycatch in fishing gear, which is an acute threat for the endangered Australian sea lion (Neophoca cinerea) (Kovacs et al., 2012) and NZ sea lion (Robertson & Chilvers, 2011). Continuous pressure of anthropogenic impacts such as fisheries, entanglement, vessel strike and chemical and noise pollution has prompted researchers to evaluate the effects of cumulative stress on marine mammals in Oceania and to implement conservation strategies to protect their survival (Kingsford et al., 2009).
Parasitism is ubiquitous in wildlife, and parasites in marine mammals are common. While a certain parasite load may not hamper host physiology, heavy infections can have serious pathogenic effects on host fitness (Measures, 2001;Siebert et al., 2001). Although Australian and NZ waters are a hotspot for marine mammal species richness (Pompa et al., 2011), little is known of their parasite diversity.
Parasitic infections, their prevalence and intensity as well as emerging species have proven to be valuable bioindicators of the ecology and health of marine mammals (Siebert et al., 2006;Lehnert et al., 2014), reflecting habitat use (Aznar et al., 1995), diet (Marcogliese, 2002), social behaviour and population dynamics (Balbuena and Raga, 1994), but also as markers for exposure and detrimental effects of xenobiotics (Sures, 2004;Pascual & Abollo, 2005;Marcogliese & Pietrock, 2011). They reveal evolutionary host-parasite relationships and highlight their biogeography and phylogeny over historical timescales (Anderson, 1982;Leidenberger et al., 2007). In the future, metazoan parasites, emerging infectious diseases and microparasites like viruses may be used as markers for the effects of anthropogenic stress on the health of marine mammals, as their role also as indicators for global change has become evident (Gulland & Hall, 2007;van Bressem et al., 2009). Additionally, some parasites of marine mammals have zoonotic potential, causing public health concerns and economic harm. Both the tapeworm Diphyllobothrium latum and anisakid nematodes (e.g. Anisakis spp., Pseudoterranova spp.) increasingly cause zoonotic infections in humans (Dorny et al., 2009;Shamsi, 2014), and can induce severe gastro-intestinal disease when ingested via undercooked fish (Mattiucci et al., 2013;Bao et al., 2017). These parasites are transmitted to their definitive cetacean and pinniped hosts via infective larvae within prey intermediate hosts, while infected fillets cause economic losses for the fishery industries (Llarena-Reino et al., 2015). Zoonotic protozoans like Giardia and Cryptosporidium are significant enteropathogens in NZ, causing higher infection rates than in other developed countries (Britton et al., 2010). Faeces from humans, pets and farm animals are discharged in runoff, bringing encysted parasites to coastal waters. They are filtered and concentrated by invertebrates and consumed by marine mammals, infecting a wide range of hosts, resulting in morbidity and mortality to some species (Fayer et al., 2004).
Collecting information about parasite diversity in marine mammals will provide a crucial baseline for assessing their impact on host and ecosystem ecology (Poulin et al., 2016). Study design in live marine mammals is restricted by legal as well as ethical constraints so that, since the cessation of whaling, data are collected mostly opportunistically from stranded or bycaught individuals. In the oceanic waters of the southern hemisphere, many species are seldom found stranded; therefore, few parasitological records (Berón-Vera et al., 2008;Nikolov et al., 2010) exist. Parasitology increasingly complements marine ecology to further our understanding of ecosystem dynamics (Poulin et al., 2016), but, so far, little is known about the biodiversity of Australasian marine parasites (Poulin, 2004;Stockin et al., 2009). New studies on marine mammals in NZ and Australian waters have recently added to our knowledge about parasite prevalence, life cycles (Tomo et al., 2010;Lehnert et al., 2017) and taxonomic relationships , Hernández-Orts et al., 2017, and justify a first hostparasite checklist encompassing all available data. Previous marine mammal parasite checklists include Baylis (1932), Delyamure (1955), Dailey & Brownell (1972), Raga (1994), Felix (2013) and Fraija-Fernández et al. (2016). Most include host data, but geographical data are scanty. Australian lists include that of the internal parasites of mammals by MacKerras (1958), the references of which are unfortunately disconnected from the text and, therefore, not useable, and Arundel (1978), which records parasites found in all marine mammals that are found in Australian waters. This list, however, does not differentiate between parasites found in the host species within Australian waters and those found in the same species in other parts of the world. There are no equivalent lists for the marine mammals of NZ.
Here, we present a host-parasite checklist collating all information about the metazoan and protozoan parasites of marine mammals in NZ and Australian waters. Although viruses (e.g. morbillivirus) and bacteria (e.g. Brucella) are relevant pathogens with zoonotic potential that can cause mortality in marine mammals (Castinel et al., 2007), we limit our list to the better-known eukaryotic parasites. Where possible, we also identify knowledge gaps and research needs, especially with regard to human interactions and zoonoses, as well as marine mammal conservation.

Material and methods
We present a list of the parasites found in pinnipeds, cetaceans and sirenians of NZ and Australia, as far as possible up to date at the time of publication. The list was assembled from primary publications found through searches on Google Scholar using all combinations of relevant keywords, plus searches of the reference lists in those publications. The parasites are presented in alphabetical order of Families under their relevant Phylum, Class and Order. Within Families, species are listed in alphabetical order. Classifications followed for helminths are: Anderson et al. For arthropods and protozoa higher taxonomy was taken from the records cited, or from searches for more up-to-date phylogenetic studies. Synonyms are taken from the references in square brackets following the entries, with corrections and updates from primary sources in some cases.
Localities of records are given as indicated in the original source. Standard abbreviations are used for Australian states: New South Wales, NSW; Queensland, QLD; South Australia, SA; Victoria, VIC; Tasmania, TAS; Western Australia, WA; and New Zealand, NZ. We have included only those records that fall within the geographical boundaries of Australia and NZ, and their subantarctic islands. Records for mainland Antarctica have not been included, because there is no geographical distinction between Australian or NZ-held territory, and those territories belonging to other countries. Although there are many records for mainland Antarctica, these are best dealt with as a separate entity.
Where there is more than one reference source, hosts and localities bear a superscript number that refers to the numbered reference. In a few cases, where references cite differing infection sites, these are also numbered with the relevant superscript number. Multiple references are listed in chronological order.
For host taxonomy we have adhered to WoRMS (2018) (Pinnipeda and Cetacea), Berta and Churchill (2012) (Pinnipeda) and Perrin (2018) (Cetacea). Host names listed are considered to be up to date as of publication. Where hosts were named differently in the original source, we have noted this in the relevant Remarks section. Hosts' common names can be found in the host-parasite list.
The developmental stage of the parasite has been noted, where given in the original source. If such information was not given, worms are assumed to be adult if egg presence is noted or egg measurements are given.
Remarks sections contain information on intermediate hosts when available, notes on prevalence and intensity, and on pathology when available; short summaries of the latest research on disputed or complicated species; and mention of molecular data Stage. All stages are reported from larvae to adults. References. Johnston & Mawson ((1) 1939, (2) 1941, (3) 1942 1945, (5) 1953); (6) Mawson (1953); (7) Brundson (1956); (8) Cannon (1977); (9) Morgan et al. (1978); (10) Cordes & O'Hara (1979); (11) Hurst (1980); (12) McColl & Obendorf (1982); (13) Bowie (1984); (14) McManus et al. (1984). Remarks. Anisakis simplex is widely accepted to be a complex of closely related species (Nascetti et al., 1986;Mattiucci et al., 1997Mattiucci et al., , 2009Mattiucci et al., , 2014D'Amelio et al., 2000;Abe et al., 2006;Abe, 2008), and the name has been attached to specimens the world over and in numerous hosts. Davey (1971) alone lists 34 different hosts from both Cetacea and Pinnipedia. While it is not possible to assign specimens reported in the literature over the years, Mattiucci et al. (2014) have made worthy inroads into resolving some of the ambiguity. As a result of their findings, it is likely that at least some of those specimens found in NZ will be their newly erected A. berlandi Mattiucci, Cipriani, Webb, Paoletti, Marcer, Bellisario, Gibson & Nascetti, 2014 (See entry for Anisakis berlandi above). Without further information, or examining each of the specimens mentioned in the literature, we here assign all references to A. simplex in the Australasian region, except those of Mattiucci et al. (2014), which have been characterized to A. simplex sensu lato. Anisakis simplex has been shown to occur as a larva in many species of fish under various names (Johnston & Mawson, 1943a, b, 1945, 1951, 1953. Brundson (1956) was able infect eels with encapsulated A. simplex from barracouta, where they re-established, demonstrating that horizontal infection is possible. This is not surprising in a system where the species complex appears to be highly generalist in its choice of host and where there exists a cascade in size of predatory fish. The larva must be able to withstand being eaten by a succession of fish before being finally taken by a cetacean, where it can mature in the stomach. Hurst (1980) completed the life cycle of A. simplex with Nyctiphanes australis (first intermediate host), large fishfor example, Thyrsites atun, Trachurus sp. (second intermediate host)and squid or small fishfor example, hoki, anchovy, sprat (paratenic host). While host specificity does appear extremely broad when all reports are taken into account, this effect may be exaggerated by the fact that A. simplex is, in fact, many cryptic species that are yet to be fully disentangled.
In the above references the species is called A. kogiae (1), A. similis (2), S. marinus (7) and S. similis (4, 6). Host species are called D. forsteri (2). In the literature cited in this section, the maximum number of worms per infection amounted to several hundred (13). The species is widely reported to cause gastric ulceration and, according to some sources, mortality (10, 11).

Synonyms.
Hosts. Arctocephalus pusillus doriferus (1), Arctophoca australis forsteri (2), Balaenoptera acutorostrata ( Grey's beaked whale (Valentini et al., 2006) grouped with some from the South African coast, also unnamed. They were closest to Anisakis ziphidarum in phylogenic analyses. A lack of adult specimens limited the morphological description and proper naming of this new species. Type 1 larvae were identified from Aphanopus carbo (black scabbard fish) from Madeira and from Trachurus trachurus (Atlantic horse mackerel) from the North Atlantic. The host in Johnston & Mawson's (1941) report is called Gypsophoca tasmanica.  Cannon (1977). Remarks. Shamsi (2014) note that A. typica specimens in Australia appear to be genetically different from those reported in other countries. Jabbar et al. (2012) found larval stages (confirmed by DNA sequence) in a number of different fish species.
Family: Ascarididae Baird, 1853  [Sprent, 1980].  Remarks. This species is usually found as adults in elasmobranchs, with the larval stages in molluscs and teleosts. This finding of a larval stage in the intestine of a dolphin almost certainly represents an accidental infection from predation on a paratenic fish host. Johnston and Mawson (1941) listed this as Echinocephalus uncinatus Molin, 1858. However, Beveridge (1987) showed that all adult and larval specimens found in elasmobranchs in Australian waters belonged to E. overstreeti, and that earlier records of E. uncinatus can probably be attributed to E. overstreeti. Moravec and Justine (2006), however, questioned this decision.
(2015). Remarks. Molecular data available (18S) (2). The phylogeny in Jabbar et al. (2015) moves the genus Crassicauda from Tetrameridae to Acuariidae. This huge worm seems to be found only in fragments due to the difficulty of extracting it whole from the subcutaneous flesh.

Remarks.
Undoubtedly, based upon infection site alone, these records refer to different species of Crassicauda. Most records agree that worms of this genus embed their cephalic end into the tissues of their favoured organ, with the body of the worm projecting freely into the lumen or sinus for the release of the eggs. The species occurring in kidneys of Z. cavirostris caused '…massive destruction of reniculi with fibrosis and necrosis…' (Duignan, 2000 p. 452). Twenty specimens were present in this host animal (1).  (cox1) (1). Haynes et al. (2014) found that all pups examined were infected and that the infection route was trans-mammary. They also found that hookworms were genetically highly variable, but female host natal site fidelity and the transmammary route of infection do not restrict hookworm gene flow between N. cinerea populations.
(1, 2) NZ; (3) Nicholson & Fanning (1981); (2) Boren (2005) Remarks. Nicholson & Fanning (1981) stated that their specimens were probably a new species of Parafilaroides, but did not describe or name them. These authors also reported that, although the animals appeared healthy when captured, they showed signs of acute verminous pneumonia. The report of Stockin et al. (2009) Bowie (1984). Remarks. The anterior end of this nematode was tightly knotted, embedded in the parenchyma of the lung and surrounded by purulent fluid in a fibrous or calcified capsule (Bowie, 1984).  (1984) reported 'huge masses of worms: average 2300, range 1140-4200 per ear' in the lead bulls, and their data led them to conclude that this auditory parasitism played a significant role in the mass stranding of 183 pilot whales on this occasion. However, a study on by-caught porpoises with good nutritional status has revealed high loads of Stenurus minor, with no apparent effect on echo-location or hunting ability, and no pathological changes (Faulkner et al., 1998). Another recent study on S. minor in the inner ear of harbour porpoises highlights the need of further research to assess the impact these nematodes may have on hearing (Morell et al., 2017 (1982); (2) Bowie (1984); (3) Tomo et al. (2010). Remarks. McColl & Obendorf (1982) report the lungs of their host specimen were highly congested with worms, causing verminous pneumonia and greatly impairing respiratory function.  Drummond (1937); (2) Johnston (1937). Remarks. Described in Drummond (1937) as Dip. arctocephali n. sp., and host called A. tasmanicus. Described in Johnston (1937) as Dip. arctocephalinum n. sp. and host called A. forsteri, but Johnston corrected this to N. cinerea in Johnston & Mawson (1941) and Johnston & Best (1942). Johnston (1937) described the worms as a 'tangled mass' in the intestine.

Synonyms.
Hosts. Arctophoca australis forsteri. Locality Marsh et al. (1984) postulate that these could be the eggs of a spirorchid trematode, members of which parasitize the circulatory system of aquatic reptiles in the same habitat as dugongs.
(1) Blair (1979); (2) Blanshard (2001). Remarks. Blair (1979) found these trematodes in all 21 specimens he observed. They were so unusual that he erected the Family Labicolidae to contain the species. Several worms together formed pus-filled abscesses along the sides of the upper lip, with pores to the outside.

Synonyms
Remarks. Occurs in pairs in the wall of the stomach glands with their posterior ends towards the lumen of the gland. Their capsules are similar to those reported by Crusz & Fernand (1954) for L. mannarense. There appears to be no host response to their presence (Blair, 1981).  (1) Dexler & Freund (1906); (2) Johnston (1913); (3) Blair (1981); (4) Olson et al. (2003). Remarks. Molecular data available (18S, 28S) (4). Dexler and Freund (1906) and Johnston (1913) Johnston (1913) found R. taylori in both dugongs he examined, ten in one and 16 in the other. (2) Shakespeare Peak and Waiake Beach, Auckland, NZ. Infection site. Liver and bile ducts. Stage. Adult. References. (1) Cordes & O'Hara (1979); (2) Lehnert et al. (2017). Remarks. Cordes and O'Hara (1979) found over 100 of this species in one dolphin. The worms were associated with parasitic hepatitis in four dolphins with lesions, but no worms were found in the livers of two more. Worms and lesions blocked bile ducts, and were either contributory to, or the cause of, death.

Synonyms.
Hosts. Cephalorhynchus hectori ( (2000) and Hutton et al. (1987) found these worms encapsulated within the mesenteric lymph nodes of the host. The lymph node had granulomatous lesions with inflammatory response associated with eggs/was enlarged with a tumour-like mass which contained purulent necrotic debris and a single parasitic worm. A secondary bacterial infection, Eikenella corrodens, was cultured from the lesion (2). Remarks. This species was originally described by Pearson (1973) from the Caspian ternas mentioned in the passing reference to G. angelae in Dubois and Angel (1976). There is a perpetuated error in the citation of this species and the referencing of this paper. Note that both Dailey et al. (2002) and Hernández-Orts et al. (2012) list Dubois and Angel (1976) with the title 'Galactosomum angelae Pearson 1973  Remarks. This species was originally described from the pied cormorant.
Remarks. This species has been found to be highly specific in its choice of host, the humpback whale, M. novaeangliae (Carvalho et al., 2010), so it seems probable that the unidentified whales belonged to this species.  Leung (1965).
Remarks. In his paper, Leung (1965) lists a large number of cyamid specimens from all over the world, collected for a study of ectocommensal protozoans. No details are given other than the locality, date and collector. Leung names the sperm whale host as P. catodon.  Leung (1965); (2) Berzin & Vlasova (1982); (3) Sedlak-Weinstein (1991). Remarks. Leung (1965) names the host G. malaena. Berzin and Vlasova (1982) list this species as occurring in Phocoena phocoena, which is probably a host identification error, as this porpoise does not inhabit the Australasian region. It seems probable that this host was Phocoena dioptrica.

Discussion
In this first host-parasite checklist, information about metazoan and protozoan parasites of marine mammals in NZ and Australian waters was collated. From 51 species of cetacean known from Australian and NZ waters, only 27 species have recorded parasites. From 11 species of pinnipeds known from Australian and NZ waters, eight have recorded parasites. The absence of records certainly does not signify that the remaining hosts are parasite free. There is still a lot left to learn. However, checklists such as this one remain valuable tools to ecologists and can help to further our understanding of parasite diversity and be a practical resource for scientists. Nematodes were the most diverse group reported, with 30 different species determined, and many more records where identification was restricted to the genus or family level. Anisakid stomach nematodes (14 species) represented the family most often found in a wide range of host species, reflecting their generalist nature, followed by pseudaliid lungworms (seven species), specific to the respiratory tract of odontocetes. Trematodes (22 species), mostly from the gastro-intestinal tract, were found in sirenians (15 species), cetaceans (six species) and pinnipeds (six species). Six species of acanthocephalans were identified from pinniped (n = 6) and cetacean (n = 3) hosts. Adult cestodes (five species) were recorded in the intestinal tract of three cetacean and two pinniped species. Cestode larvae within the subcutaneous blubber and the peritoneum were recorded from multiple cetacean (n = 9) and pinniped (n = 3) species. Thirteen different ectoparasitic crustacean species were found on cetaceans and sirenians. Other arthropod ecto-(Insecta, three species) and endoparasites (Arachnida, four species) were recorded from pinniped species. Three protozoan species were encountered in several marine mammal species including sirenians, pinnipeds and cetaceans within studies dating from 1997 to 2017. This may reflect, on the one hand, the relatively recent occurrence of some of these pathogens in the marine environment due to human activities and, on the other hand, new survey and diagnostic techniques (Lasek-Nesselquist et al., 2010), as well as growing awareness of these emerging zoonotic agents in the research community.
Thirty-four parasite records were from dugongs and 25 species were found in common dolphins, while leopard seals with 17 parasite species were the pinnipeds most often infected. This reflects the opportunistic nature of sampling these animals. The findings indicate that, for example, sperm whales with one crustacean ectoparasite record or elusive beaked whales with 2-3 species records are seldom encountered hosts.
Many old records have complicated histories with multiple synonyms, which need updating. Also, the advent of molecular tools has identified several species complexes (Mattiucci et al., 2014;Klotz et al., 2018), for which retrospective analyses would be useful. New techniques will likely also continue to improve the identification of parasite fragments and minute larvae (Jabbar et al., 2015), as well as provide insights on the phylogeny of parasite species (Hernández-Orts et al., 2017).
The protozoans Toxoplasma, Giardia and Cryptosporidium are emerging parasites in marine mammals. In the future, the combination of prevalence surveys with molecular techniques will probably identify further protozoans and provide knowledge on host specificity and transmission pathways (Fayer et al., 2004;Applebee et al., 2005;Grilo et al., 2018).
Foodborne parasites like cestodes (Diphyllobothrium sp.) and anisakids (Anisakis sp., Pseudoterranova sp.) are abundant in marine mammals in Australasia and pathogenic for humans when infective larvae are accidentally consumed with undercooked fish (Yamasaki & Kuramochi, 2009;Shamsi & Butcher, 2011). Human health concerns as well as implications for fisheries and seafood control underline the importance of better understanding the epidemiology of relevant species (Cipriani et al., 2016).
Opportunistic parasite surveys of dead or live stranded cetaceans, in cooperation with established stranding networks (e.g. that of NZ's Department of Conservation) and systematic, minimally invasive studies to monitor live and free ranging pinnipeds (e.g. analysing faeces from pinniped colonies; Presswell & Lagrue, 2016), would enable a better overview of prevalence, intensity of infections and emerging parasite species. The importance of wellmaintained and curated museum collections cannot be underestimated in their contribution towards our ongoing knowledge of parasite biodiversity . It remains unclear how contaminant exposure causing immune suppression or cumulative effects of human-induced pressures (shipping, fisheries, global change) make marine mammals more susceptible to infectious disease in Australasian waters (Van Bressem et al., 2009). Studies combining ecotoxicological analyses with systematic monitoring of parasite prevalence and impact (Lehnert 670 K. Lehnert et al. et al., 2018) would help to elucidate these relationships in the future. Parasites should be an integral part of biodiversity and conservation research in their marine mammal hosts (Aznar et al., 2010;Poulin et al., 2016). Ultimately, this research can inform managers and may guide species, habitat and population assessment and conservation, as well as encourage further investigations into the biodiversity and ecology of marine mammal parasites.