Review
Special Issue: Wildlife Parasitology
Biodiversity and parasites of wildlife: Helminths of Australasian marsupials Ian Beveridge1 and David M. Spratt2 1 2
Department of Veterinary Science, University of Melbourne, Veterinary Clinical Centre, Werribee, Victoria, Australia National Wildlife Collection, Commonwealth Scientific and Industrial Research Organisation, Canberra, Australia
Despite current attempts to document the extent of biodiversity on Earth, significant problems exist in fully documenting the helminth parasites of wildlife. Using the Australasian marsupials as an example, we examine some of these difficulties, including challenges in collecting uncommon host species, the ongoing description of new species of marsupials, the presence of cryptic species, and the decline in taxonomic expertise in Australia. Although optimistic global predictions have been made concerning the rate of discovery and description of new species of animals, these predictions may not apply in the case of specific groups of animals such as the Australasian marsupials. Global predictions In recent decades, there has been considerable interest in quantifying the extent of biodiversity on Earth. There are differing views about the numbers of extant eukaryotic species, but this is currently estimated to be 5 3 million, of which 1.5 million are named [1]. A study investigating the feasibility of naming the remaining species presented a positive assessment [1] based on an increase in the number of taxonomists globally and an increase in the number of taxonomic publications. Although parasites were initially overlooked in surveys of biodiversity, the significance of their contribution is now established [2], but the estimated number of potential (helminth) parasites present in vertebrates continues to be disputed [3]. Although the potential number of extant species can be estimated using sophisticated statistical methods [4] and the problems of assessing parasite diversity have been examined in detail [2], the number of named species remains the basis on which most assessments of biodiversity are currently made. For such assessments, global databases such as the Global Biodiversity Information Facility (GBIF) (containing 1474 643 animal species) and, on a regional basis, the Atlas of Living Australia (ALA), provide valuable information. Equally informative can be checklists of parasites for particular groups of hosts, such as those for African vertebrates [5], a particular geographical region of the world such as Papua New Corresponding author: Beveridge, I. ([email protected]). Keywords: helminths; marsupials; Australasia; biodiversity. 1471-4922/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pt.2014.10.007
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Guinea [6], or even a particular group of hosts such as the rhinoceroses [7]. However, such reviews are limited in number and for many regions of the world such databases or checklists do not exist. This is of particular concern with respect to the helminth (nematode, cestode, trematode, and acanthocephalan) parasites of wildlife. Although there is increasing interest in this discipline, the literature documenting the helminth parasites of wildlife is both limited and fragmented, with few overviews. Ideally, for scientists involved in managing wildlife populations, accurate documentation of the parasites present in them as well as their potential pathogenicity would be an extremely useful tool. Unfortunately, these data are rarely available. There are numerous impediments involved in a comprehensive understanding of the biodiversity of parasites in wildlife and in this review these difficulties are investigated using the Australasian marsupials as an example. Australasia here is considered to constitute Australia, Papua New Guinea, and the islands south of Wallace’s Line. As these marsupials constitute a taxonomically and geographically defined group of mammals, they provide an obvious exemplar to investigate what is known and what is not known about the parasites of this highly distinctive group of mammals and to assess the need for such information and how it might be acquired in this specific environment. The Australasian marsupials The Australasian marsupials constitute a phylogenetically defined group of mammals belonging to the Australidelphia. They are essentially confined to Australia and New Guinea, although the South American monito del monte, Dromiciops gliroides, is also included within this taxon. The conventional hypothesis, supported by recent molecular data [8], is that marsupials reached Australia from South America in a single dispersal event before the breaking up of Gondwana, 40–60 million years ago, although limited, contradictory paleontological evidence exists suggesting a reverse migration [9]. In particular, Dromiciops may have migrated from Australia back into South America [8], although it appears to be the only genus in this category. Within Australasia, the marsupials have radiated to occupy various niches. The basally branching clades, the Dasyuromorphia and Peramelemorphia (collectively, the polyprotodont marsupials), contain various insectivores and carnivores ranging from the mouse-sized antechinuses
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(Dasyuridae) to the rat-sized bandicoots (Peramelidae), the cat-sized quolls (Dasyurus spp.), and the Tasmanian devil (Sarcophilus harrisii) (Figure 1). The more recent clades are herbivorous and are characterized by a distinctive diprotodont dentition with two procumbent lower incisors. The basal diprotodonts include the fossorial wombats (Vombatidae), which are the size of a small pig or large dog, as well as their relatives the arboreal, folivorous koalas (Phascolarctidae). The possums range in size from the mouse-sized pigmy possums (Burramyidae) to the rator cat-sized Phalangeridae (possums and cuscuses) and Pseudocheiridae (possums). The latter are arboreal folivores, some species of which have developed the capacity to glide and are therefore commonly referred to as ‘gliders’. The best-known marsupials are the rat kangaroos (Hypsiprymnodontidae and Potoroidae) and the wallabies and kangaroos (Macropodidae), distinguished primarily by their saltatory means of locomotion. Currently, 57 species of wallaby and kangaroo are recognized [10,11]. In addition, bizarre inclusions in the marsupial fauna include the marsupial moles (Notoryctomorphia), which live in sand dunes in central Australia and are probably a sister group to the Dasyuromorphia and Peramelemorphia. From the viewpoint of parasite diversity, it is also important to take into account the remaining terrestrial mammals that occur on the continent, as transfer of parasites has
obviously occurred between these other major groups. Three species of monotreme are currently extant: two species of echidna and the platypus. They are remnants of a much more diverse fauna and have a long fossil record on the continent. The rodent fauna is diverse, with 70 species, all belonging to the Muridae, known at the time of European settlement. Murid rodents are thought to have arrived in Australia between 5 and 15 million years ago from Southeast Asia [12]. Currently, there are 82 species of bat recognized in Australia [10], with the greatest diversity in the north, presumably because the original route of entry to the continent was from Southeast Asia [13]. The dingo, Canis lupus familiaris, is thought to have arrived in northern Australia from Southeast Asia about 4000 years ago [10], while introductions of domestic animals as well as foxes, rabbits, and hares began about 200 years ago. Helminth parasites of Australasian marsupials Due to the relative isolation of the Australasian marsupials during their major period of diversification, it may be expected that they would harbor a relatively limited number of parasite orders and families, even if extensive radiations within particular orders or families were present. However, no fewer than 41 families and 130 genera of helminths had been recorded from Australasian marsupials by 1991 [14] (Table 1). Although many new species
Dasyuromorphia
Exnct
Peramelemorphia
Diprotodona
Macropodoidea
Vombaformes
Notoryctomorphia
Phalangerida
Thylacinidae
Tasmanian ger
Dasyuridae
Nave cats, devils, antechinus
Myrmecobiidae
Ant-eater
Peramelidae
Bandicoots
Thalacomyidae
Rabbit-eared bandicoots
Notorycdae
Mole
Phascolarcdae
Koala
Vombadae
Wombats
Potoroidae
Potoroos
Macropodidae
Kangaroos, Wallabies
Phalangeridae
Cuscus, Phalangers
Burramyidae
Pygmy possums
Pseudocheiridae
Ring-tailed possums
Petauridae
Gliders
Tarsipedidae
Honey possum TRENDS in Parasitology
Figure 1. Phylogenetic relationships of the Australasian families of marsupials. Adapted from [14].
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Table 1. Diversity of families, genera, and species of helminth parasites in Australasian marsupials estimated in 1991a (left) and currently (right) No. families Phylum Platyhelminthes Class Digenea Cestoda Phylum Nematoda Order Ascaridida Spirurida Oxyurida Strongylida Rhabditida Enoplida Phylum Acanthocephala Total
No. genera
No. species
9 5
16 16
19 21
28 77
39 97
4 8 1 8 1 3 2 41
7 14 5 64 2 4 2 130
10 15 6 70 2 3 2 148
13 37 6 261 4 6 2 434
29 46 7 407 5 24 4 658
a
Reproduced from [14].
have been described more recently (Table 1), the number of orders and families has not changed significantly and the current tally includes most of the families commonly encountered in terrestrial vertebrates. Of the families encountered in marsupials, only two are represented by parasites of introduced livestock that have been able to switch to marsupial hosts [the common liver fluke, Fasciola hepatica (Fasciolidae), and the hydatid Echinococcus granulosus (Taeniidae)]. The currently described marsupial helminth fauna therefore represents a truly diverse radiation for a geographically isolated group of mammals. Current evidence suggests that the helminth fauna of Australasian marsupials has multiple origins [14]. It includes a Gondwanan component related to the parasites of South American marsupials. Examples include the cestode genus Paralinstowia, which occurs on both continents, and the potentially related trichostrongyloid nematode families Viannaiidae in South American marsupials and Herpetostrongylidae in Australasian marsupials [14]. Beyond these few examples, however, the helminth faunas of the two groups of marsupials differ markedly. Other families of parasites have possibly been acquired from monotremes, as exemplified by the endemic Australian trichostrongyloid family Mackerrastrongylidae, which occurs in both monotremes (echidnas) and marsupials [14]. Finally, there are instances of parasites being introduced to the continent by rodents and bats arriving from Southeast Asia [14]. The spirurid nematode Spirura aurangabadensis occurs in bats in Southeast Asia and in Australian carnivorous marsupials, while cestodes of the genus Bertiella (Anoplocephalidae) occur in rodents in Southeast Asia as well as rodents in Australia and in arboreal marsupials [14]. However, all current hypotheses are provisional and are subject to validation by future studies. For many species of parasite, their phylogeny is poorly understood and hence their origins remain debatable. As might be expected, the various parasite families are not distributed evenly among marsupial groups. For example, hymenolepidid and linstowiid cestodes, as well as 144
spirurid nematodes, which utilize arthropods as intermediate hosts, tend to be most common in the insectivorous and carnivorous dasyurids and peramelids. By contrast, anoplocephalid cestodes and strongylid nematodes are restricted to the herbivorous diprotodonts (wombats, koalas, kangaroos, and wallabies), as the infective stages occur on and are ingested with vegetation. Other nematode groups, such as the trichostrongylid, metastrongylid, and filarioid nematodes, occur across host groups because they require no intermediate hosts, use mollusks as intermediate hosts that are ingested deliberately by carnivores or accidentally by herbivores, or are transmitted by biting arthropods. Parasite diversity is relatively high in the terrestrial, omnivorous dasyurids and peramelids but declines substantially in the arboreal pseudocheirids and phalangerids, possibly due to their arboreal lifestyle, and increases again in the terrestrial kangaroos and wallabies [14]. Recent studies of the parasites of tree kangaroos have provided some support for this observation, as most tree kangaroo species harbor very few species of cloacinine nematode, although Dendrolagus mbaiso, a tree kangaroo that is secondarily terrestrial, living mainly above the tree line in Irian Jaya, has an abundant cloacinine nematode fauna [15]. Not only is the Australasian helminth parasite fauna highly endemic (97% [14]), but it also includes remarkable instances of convergent evolution as well as unique morphological diversification. Hypodontus macropi, a parasite of the ileum and large intestine of kangaroos and wallabies, is a strongylid nematode morphologically convergent with the hookworms of eutherians (the ancylostomatids), possessing a deviated anterior end and a large oral opening with cutting plates such as those found in the true hookworms (Figure 2). The anoplocephalid cestode genus Triplotaenia, found in kangaroos and wallabies, contains species with a
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Figure 2. Mouth of Hypodontus macropi (Nematoda: Strongyloidea), a strongyloid nematode parasite of kangaroos, with paired cutting plates resembling those found in the hookworm (ancylostomatoid) parasites of eutherian mammals. Reproduced from [55].
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longitudinally divided strobila and loss of external segmentation (Figure 3), parallels seen only in the cestode parasites of elasmobranchs. Consequently, the parasite fauna of marsupials is not only highly endemic but also contains some remarkable examples of convergent evolution among parasites [14]. However, from the broader perspective, questions need to be posed regarding how well studied this group of parasites is and how far we are from knowing the true extent of diversity in the helminth parasites of Australasian marsupials. First, not all of the extant species of marsupial have been examined for parasites. By 1991, 87 of 211 (41%) marsupial species had no record of helminth parasites; currently, this proportion has fallen slightly (37%), but significant numbers of species remain to be examined (Table 2). On the basis of the proportion of species in each family examined, the families Dasyuridae (48%), Peramelidae (53%), Phalangeridae (52%), Burramyidae (14%), and Petauridae (50%) clearly warrant additional attention. In the case of some marsupial species, it may be that they harbor very few parasite species (e.g., Burramyidae [14]) (possibly due to their small size, arboreal habitat, and feeding on nectar as well as arthropods) and that negative findings have simply not been reported in the scientific literature. However, to what extent this issue extends to other marsupial taxa is not fully known. The lack of collections from particular species may stem from a number of reasons. The species involved may be rare or threatened, thereby limiting opportunities to collect parasites, or they may have remote habitats and the parasites may be difficult to collect. One example is the New Guinea tree kangaroo, Dendrolagus mbaiso, which occurs only at high altitudes in the Sudirman Range in Irian Jaya [16]. Only one scientific specimen (the holotype) has ever been obtained; fortunately, the parasites of this tree kangaroo were preserved and have been described [17–19]. However, many other species of marsupial in both Australia and Papua New Guinea are difficult to collect for similar logistical reasons.
Table 2. Numbers of Australasian marsupials from which parasites have been recorded: current figures (left) and figures from 1991 (right) Host group
Dasyuridae Myrmecobiidae Thylacinidae Notoryctidae Peramelidae Thalacomyidae Phalangeridae Burramyidae Petauridae Hypsiprymnodontidae 1 Potoroidae Macropodidae Phascolarctidae Vombatidae Tarsipedidae Total
No. of species with parasite records 34 1 1 1 9 2 13 1 14 1 8 53 1 3
27 1 1 1 7 2 12 2 13
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124
5 48 1 3
No. of species without parasite records 37
33
1 8
1 9
12 6 14
14 5 11
5
4 9
1 84
1 87
Even in instances where there are published records, they may be from a single host individual, as exemplified above. For marsupial families with low parasite diversity (Phascolarctidae, Pseudocheiridae), examining a few individuals may be adequate as it may be that the few parasites to which they are host occur at a high prevalence and therefore will be encountered in a small sample of hosts. However, for highly diverse parasite communities such as those found in the fore-stomachs of kangaroos and wallabies, with total burdens sometimes reaching 500 000 [20] (Figure 4), uncommon species may be easily overlooked [21]. It has been estimated [22] that in the case of the complex helminth communities found in four species of
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Figure 3. The scolex of Triplotaenia mirabilis (Cestoda: Anoplocephalidae), an intestinal cestode of wallabies, with the strobila split into two, loss of segmentation, and a tag of unsegmented tissue between the two major branches of the strobila, providing the basis for the generic name. Reproduced from [55].
Figure 4. The stomach contents of an agile wallaby (Macropus agilis) showing the abundance of strongyloid nematodes commonly encountered in the stomachs of macropodid marsupials. The large nematodes are Labiostrongylus labiostrongylus, but the smaller nematodes visible include numerous genera and species.
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Review kangaroo and wallaby, samples of 10–18 animals resulted in the recovery of between 93% and 97% of the helminth parasite species. A similar estimate suggested that a sample size of 18 western grey kangaroos (Macropus fuliginosus) was needed to recover all of the species of helminth parasite [23] whereas examination of a single specimen of a rock wallaby species (Petrogale) results in the recovery on average of 8.6 helminth species [24]. It is therefore noteworthy that for only 31 (57%) of the known 54 species of kangaroo and wallaby have more than five individuals been examined (unpublished observations), suggesting that current estimates of parasite biodiversity even within this family of marsupials are gross underestimates. An additional factor influencing the discovery of new species is their geographical distribution. Recently, a new species of the nematode genus Cloacina has been described that has an extremely restricted geographical range despite the fact that the kangaroo host, which is abundant, is distributed across thousands of square kilometers virtually over the entire continent [25]. In a continent of the size of Australia, the possibility of finding highly localized parasite species presents a significant problem. The examples cited here are derived from the parasite faunas of macropodids, but the extent to which these factors apply to marsupial families with less diverse helminth faunas remains unclear. Cryptic species Additional difficulties in estimating levels of biodiversity are provided by the presence of cryptic species detectable in parasitic helminths primarily by molecular methods. In Australasian marsupials, this appears to be a significant issue in the case of both cestodes and nematodes. The topic was reviewed recently [26], with several instances of apparently generalist helminth parasites being split into ten or more species once genetic studies had been undertaken. Two nematode taxa – Hypodontus macropi, found in the ileum, cecum, and colon, and Rugopharynx australis, found in the stomach – and the cestode Progamotaenia festiva, found in the bile ducts of macropodids, were cited as examples [27–29], but several others were identified in which taxonomic recognition lags behind the molecular recognition of cryptic species. These studies targeted parasite taxa that appeared to be generalists and occur in a wide range of host species. However, substantial numbers of taxa occurring in more than a single host await genetic examination. It was concluded [26] that the occurrence of cryptic species in marsupial helminths appeared to be almost random, thereby severely limiting any predictions concerning estimates of biodiversity. Nevertheless, the use of molecular tools is dramatically increasing the number of species and hence the biodiversity found within the parasites of marsupials. New hosts A further potentially confounding factor in assessments of biodiversity is the rate at which new species of marsupial hosts are being described through the discovery of entirely new species, such as within the dasyurid genus Antechinus [30–32], the rediscovery of species previously thought to be extinct such as Gilbert’s potoroo (Potorous gilberti) [33], or 146
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the splitting of existing species such as has occurred within the rock wallabies (Petrogale spp.), with 10 species (including 20 chromosome races) recognized in 1982 [34] compared with the 16 species now recognized [35]. Currently, the systematics of the short-eared rock wallaby, Petrogale brachyotis, from northern Australia is under review, with eight geographically distinct lineages recognized, several of which may represent independent species [36]. Such changes in host status may have significant implications for parasite biodiversity. Preliminary genetic studies of three species of nematode belonging to the genus Cloacina (Cloacina robertsi, Cloacina caenis, and Cloacina pearsoni) from the stomachs of a series of parapatric species of rock wallaby occurring along the north-east coast of Australia have demonstrated genetic differences between specimens from each host species, leading to the possibility that the three currently recognized morphospecies occurring in this range of closely related hosts may represent 15 genetically distinguishable nematode species [37]. Studies of the large numbers of remaining helminth parasites of this host species complex are yet to be undertaken. As previously noted [26], molecular studies to date have concentrated on the parasites of kangaroos and wallabies, with no studies of the equally highly diverse nematode parasite fauna found in dasyurids and peramelids. Additional surprises in terms of biodiversity may await molecular investigations examining the helminth parasites of these groups. Site in host An additional factor in assessing parasite biodiversity is that the largest and most easily recovered parasites are those most likely to be described first. This phenomenon has been demonstrated quantitatively in the case of monogenean parasites of fish, with a greater number of smaller species having been described in recent years [2]. In the case of marsupials, rather than parasite size, more species are being described from locations outside the gastrointestinal tract, which has been the focus of many parasitologists in the past. Nematodes in particular are being recovered from the subcutaneous connective tissues, the accessory male genital glands, the tongue, the orbit of the eye, the vasculature, and other sites that may not be routinely examined [38–46]. In the case of the filarioid nematodes, detecting infection may be difficult, and in the abdominal cavity it is often only nematode movement that differentiates the parasites from nerves and lymphatics, rendering reliable collection difficult and the likelihood of overlooking infections high. Parasite extinctions Australia has one of the worst records globally in terms of mammal extinctions [47] and we can have little idea of the extent of parasite biodiversity that has already been lost. This issue has been addressed by several authors (e.g., [48]). The Australian state of Tasmania has been the only jurisdiction in the country to include a parasite on its list of endangered species. Dasyurotaenia robusta, a cestode parasite of the Tasmanian devil, has been described from specimens collected in captive animals [49] but apparently has a very localized distribution in Tasmania, having been found at only one locality, Collins Gap, in a survey of 153 devils
Review from around Tasmania [50] (D.L. Obendorf, personal communication). The current decimation of the devil population due to facial tumor disease [51] may already have resulted in the extinction of D. robusta, although this is unknown as no surveys have been established to monitor the fate of this parasite, despite it being placed on an endangered species list. In the case of other critically endangered marsupial species such as the northern hairy-nosed wombat, Lasiorhinus krefftii, no consideration appears to have been given to its unique parasites such as the nematode Oesophagostomoides eppingensis. The parasites of additional endangered marsupial species are very poorly known. Taxonomic impediment In recent years it has been widely recognized that a significant limitation to the description of new species of parasites has been the decline in the number of active taxonomists [52]. By contrast, other reports [1] suggest that globally the numbers of taxonomists and of taxonomic publications are increasing. However, the impact of the taxonomic decline is probably most important at the local rather than the global scale. Despite the Australasian region being recognized as a region of high biodiversity [53], and this being also evident in the case of helminth parasites, within the country taxonomic expertise is in serious decline and has been described as a ‘crisis’ [54]; currently there are virtually no taxonomists employed within the area of helminth biodiversity in Australia. As a consequence, the optimistic global perspective [1] hardly applies to Australia and its endemic helminths are not readily available to workers in overseas institutions, even if such workers existed. Consequently, the optimistic view of describing all new taxa [1] is probably not applicable to this localized situation and probably not to several other, similar regions. Concluding remarks The helminth parasites of Australasian marsupials highlight the significance and difficulties of assessing the biodiversity of parasites of wildlife. This example is relevant for several reasons. At a purely scientific level, it matters in terms of our attempts to understand the processes of parasite evolution and to assess levels of parasite diversity as increasing numbers of marsupial hosts move toward extinction. Once the hosts are extinct, we can never study their parasites and hence how they might have coevolved with their hosts. We therefore lose significant insights into parasite evolution. On a more practical basis, wildlife managers and those managing recovery programs for endangered marsupial species require information about their parasites, which might be lost with the extinction of host populations. In the current recovery program for the threatened Tasmanian devil, no consideration has been directed toward its host-specific parasites, although one (D. robusta) has been for some time included on an official endangered species list. In addition, wildlife managers dealing with declines in the number of mammalian species are obliged to deal with potential threats due to parasites. Without an adequate catalog of parasite diversity and an assessment of the pathogenicity of individual parasites, it is difficult to
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assess their possible threat to host survival. For this reason alone, the documentation of parasite diversity is valuable. The Australasian region has always been recognized as having a diverse endemic fauna, much of which has not been described. This applies equally to the parasitic helminths of marsupials. However, due to the decline of local taxonomic expertise it seems highly unlikely that the existing biodiversity will ever be adequately catalogued. The factors affecting helminth biodiversity in a general sense have been exhaustively evaluated elsewhere [2]. Here we substantiate many of their general conclusions using the specific example of the helminths of marsupials, but can provide no substantive evidence to support the suggestion [1] that the description of this unique parasite fauna of Australasian wildlife is ever likely to be comprehensively described. References 1 Costello, M.J. et al. (2013) Can we name the Earth’s species before they go extinct? Science 339, 413–416 2 Poulin, R. and Morand, S. (2004) Parasite Biodiversity, Smithsonian Institution Press 3 Strona, G. and Fattorini, S. (2014) Parasitic worms: how many really? Int. J. Parasitol. 44, 269–272 4 Gotelli, N.J. and Colwell, R.K. (2011) Estimating species richness. In Biological Diversity: Frontiers in Measurement and Assessment (Magurran, A.E. and McGill, B.J., eds), pp. 39–54, Oxford University Press 5 Canaris, A.G. and Gardner, S.L. (2003) Bibliography of Helminth Species Described from African Vertebrates 1800–1967, Harold W. Manter Laboratory for Parasitology (http://digitalcommons.unl.edu/ parasitologyfacpubs/3) 6 Owen, I.L. (2011) Parasites of animals in Papua New Guinea recorded at the national veterinary laboratory: a catalogue, historical review and zoogeographical affiliations. Zootaxa 3143, 1–163 7 Knapp, S.E. et al. (1997) Helminths and arthropods of black and white rhinoceroses in southern Africa. J. Wildl. Dis. 33, 492–502 8 Nilsson, M.A. et al. (2010) Tracking marsupial evolution using archaic genomic retroposon insertions. PLoS Biol. 8, e1000436 9 Beck, M.D.B. et al. (2007) Australia’s oldest marsupial fossils and their biogeographical implications. PLoS ONE 3, e1858 10 van Dyck, S. and Strahan, R. (2008) The Mammals of Australia. (3rd edn), Reed New Holland 11 Flannery, T.F. (1995) Mammals of New Guinea, Reed Books 12 Breed, W.G. and Aplin, K.P. (2008) Order Rodentia and Family Muridae. In The Mammals of Australia (3rd edn) (van Dyck, S. and Strahan, R., eds), pp. 574–577, Reed New Holland 13 Richards, G.C. (2008) Order Chiroptera. In The Mammals of Australia (3rd edn) (van Dyck, S. and Strahan, R., eds), pp. 420–423, Reed New Holland 14 Beveridge, I. and Spratt, D.M. (1996) The helminth fauna of Australasian marsupials: origins and evolutionary biology. Adv. Parasitol. 37, 135–254 15 Flannery, T.F. et al. (1996) Tree Kangaroos: A Curious Natural History, Reed Books 16 Flannery, T. et al. (1995) A new tree kangaroo (Dendrolagus: Marsupialia) from Irian Jaya, Indonesia, with notes on ethnography and the evolution of tree kangaroos. Mammalia 59, 65–84 17 Beveridge, I. (1997) Macropostrongyloides dendrolagi n. sp. and Mbaisonema coronatum n.g., n.sp., two new species of nematodes (Strongyloidea: Cloacinidae) from tree-kangaroos, Dendrolagus spp. (Marsupialia: Macropodidae) from Irian Jaya, Indonesia. Syst. Parasitol. 38, 25–31 18 Beveridge, I. (2002) New species and new records of Cloacina von Linstow, 1898 (Nematoda: Strongyloidea) parasitic in macropodid marsupials from Papua New Guinea. Rec. S. Aust. Mus. 35, 1–32 19 Smales, L.R. (1997) A new species of Dorcopsinema Mawson, 1977 (Nematoda: Cloacinidae) from the tree kangaroo Dendrolagus mbaiso (Marsupialis: Macropodidae) from Irian Jaya, Indonesia and new host records for Dorcopsinema dendrolagi. Syst. Parasitol. 38, 131–135 147
Review 20 Beveridge, I. and Arundel, J.H. (1979) Helminth parasites of grey kangaroos, Macropus giganteus Shaw and M. fuliginosus (Desmarest), in eastern Australia. Aust. Wildl. Res. 6, 69–77 21 Vendl, C. and Beveridge, I. (2014) Estimation of species richness in the complex communities of nematode parasites found in the stomachs of kangaroos and wallabies (Family Macropodidae). Trans. R. Soc. S. Aust. 138, 105–112 22 Aussavy, M. et al. (2011) Helminth parasite communities in four species of sympatric macropodids in western Victoria. Aust. Mammal. 33, 13–20 23 Webley, L.S. et al. (2004) Endoparasites of an insular subspecies of the western grey kangaroo, Macropus fuliginosus. Aust. J. Zool. 52, 623–634 24 Beveridge, I. et al. (1989) Helminth parasites of rock wallabies, Petrogale spp. (Marsupialia) from Queensland. Aust. Wildl. Res. 16, 273–287 25 Beveridge, I. et al. (2014) Description of Cloacina atthis sp. nov. from the stomach of the euro (Macropus robustus) (Marsupialia: Macropodidae) from Western Australia based on morphological and molecular criteria. Parasitol. Res. 113, 3485–3493 26 Beveridge, I. and Gasser, R.B. (2014) Diversity in parasitic helminths in Australasian marsupials and monotremes: a molecular perspective. Int. J. Parasitol. 44, 859–864 27 Chilton, N.B. et al. (2012) Genetic variation within the Hypodontus macropi (Nematoda: Strongyloidea) complex from macropodid marsupial hosts in Australia. Electrophoresis 33, 3544–3554 28 Beveridge, I. and Chilton, N.B. (1999) Revision of the Rugopharynx australis (Moennig, 1926) complex (Nematoda: Strongyloidea) from macropodid marsupials. Invert. Taxon. 13, 805–843 29 Beveridge, I. and Shamsi, S. (2009) Revision of the Progamotaenia festiva species complex (Cestoda: Anoplocephalidae) from Australasian marsupials, with the resurrection of P. fellicola (Nybelin, 1917) comb. nov. Zootaxa 1990, 1–29 30 Baker, A.M. et al. (2012) A new dasyurid marsupial from eastern Queensland, Australia: the buff-footed antechinus, Antechinus mysticus sp. nov. (Marsupialia: Dasyuridae). Zootaxa 3515, 1–237 31 Baker, A.M. et al. (2013) A new dasyurid marsupial from Kroombit Tops, south-east Queensland, Australia: the silver-headed antechinus, Antechinus argentus sp. nov. (Marsupialia: Dasyuridae). Zootaxa 3746, 201–239 32 Baker, A.M. et al. (2014) The black-tailed antechinus, Antechinus arktos sp. nov.: a new species of carnivorous marsupial from montane regions of the Tweed Volcano caldera, eastern Australia. Zootaxa 3765, 101–133 33 Sinclair, E.A. and Westerman, M. (1997) Phylogenetic relationships within the genus Potorous (Marsupialia: Potoroidae) based on allozyme electrophoresis and sequence analysis of the cytochrome-b gene. J. Mamm. Evol. 4, 147–167 34 Briscoe, D.A. et al. (1982) Isolation, introgression and genetic variation in rock wallabies. In Species at Risk: Research in Australia (Groves, R.H. and Ride, W.D.L., eds), pp. 73–97, Australian Academy of Science 35 Eldridge, M.D.B. (2008) Rock wallabies: Petrogale. In The Mammals of Australia (3rd edn) (van Dyck, S. and Strahan, R., eds), pp. 361–362, Reed New Holland
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36 Potter, S. et al. (2012) Multiple biogeographical barriers across the monsoon tropics of northern Australia: phylogeographic analysis of the brachyotis group of rock wallabies. Mol. Ecol. 21, 2254–2269 37 Chilton, N.B. et al. (2009) Genetic variation within species of the nematode genus Cloacina (Strongyloidea: Cloacininae) parasitic in the stomachs of rock wallabies, Petrogale spp. (Marsupialia: Macropodidae) in Queensland. Aust. J. Zool. 57, 1–10 38 Spratt, D.M. (1972) Aspects of the life-history of Dirofilaria roemeri in naturally and experimentally infected kangaroos and wallabies. Int. J. Parasitol. 2, 139–156 39 Spratt, D.M. (1982) Anatrichosoma haycocki sp. n. (Nematoda: Trichuridae) from the paracloacal glands of Antechinus spp., with notes on Skrjabinocapillaria Skarbilovitsch. Ann. Parasitol. Hum. Comp. 57, 63–71 40 Spratt, D.M. (1984) Further studies of the lung parasites (Nematoda) from Australian marsupials. Aust. J. Zool. 32, 283–310 41 Spratt, D.M. (2006) Description of capillariid nematodes (Trichinelloidea: Capillariidae) parasitic in Australian marsupials and rodents. Zootaxa 1348, 1–82 42 Spratt, D.M. (2011) New records of filarioid nematodes (Nematoda: Filarioidea) parasitic in Australasian monotremes, marsupials and murids, with descriptions of nine new species. Zootaxa 2860, 1–61 43 Spratt, D.M. and Speare, R. (1982) Durikainema macropi gen. et sp. nov. (Muspiceoidea: Robertdollfusidae), a remarkable nematode from Macropodidae (Marsupialia). Ann. Parasitol. Hum. Comp. 57, 53–62 44 Spratt, D.M. and Whittington, R. (1989) Nematode parasites from the skin of the platypus, Ornithorhynchus anatinus (Monotremata). Syst. Parasitol. 13, 223–229 45 Spratt, D.M. and Gill, P.A. (1998) Durikainema phascolarcti sp. nov. (Muspiceoidea: Robertdollfusidae) from the pulmonary arteries of the koala, Phascolarctos cinereus, and associated pathological changes. Syst. Parasitol. 39, 101–106 46 Spratt, D.M. and Hobbs, R.P. (2003) Breinlia (Breinlia) ventricola sp. nov. from the heart of the red kangaroo, Macropus rufus, in Western Australia. Trans. R. Soc. S. Aust. 128, 67–71 47 Hatton, T. et al. (2011) Australia State of the Environment Report, Australian Government Department of Sustainability, Environment, Water, Population and Communities 48 Sprent, J.F.A. (1992) Parasites lost. Int. J. Parasitol. 22, 139–151 49 Beveridge, I. (1984) Dasyurotaenia robusta Beddard, 1912, and D. dasyuri sp. nov., from carnivorous Australian marsupials. Trans. R. Soc. S. Aust. 108, 185–195 50 Obendorf, D.L. et al. (1990) Trichinella pseudospiralis infection in Tasmanian wildlife. Aust. Vet. J. 67, 108–110 51 Loh, R. et al. (2006) The pathology of devil facial tumor disease (DFTD) in Tasmanian devils (Sarcophilus harrisii). Vet. Pathol. 43, 890–895 52 Kim, K.C. and Byrne, L.B. (2006) Biodiversity loss and the taxonomic bottleneck: emerging biodiversity science. Ecol. Res. 21, 794–810 53 Joseph, L. et al. (2014) Australia’s biodiversity: major features. In Biodiversity. Science and Solutions for Australia. pp. 13–36, CSIRO 54 Hall, K. (2008) Proceedings of the National Taxonomy Forum (Australia), Federation of Australian Scientific and Technological Societies 55 Beveridge, I. (1986) Biogeography of parasites in Australia. Parasitol. Today 2 (Suppl.), 53–57
Special Issue: Wildlife Parasitology
Biodiversity and parasites of wildlife: Helminths of Australasian marsupials Ian Beveridge1 and David M. Spratt2 1 2
Department of Veterinary Science, University of Melbourne, Veterinary Clinical Centre, Werribee, Victoria, Australia National Wildlife Collection, Commonwealth Scientific and Industrial Research Organisation, Canberra, Australia
Despite current attempts to document the extent of biodiversity on Earth, significant problems exist in fully documenting the helminth parasites of wildlife. Using the Australasian marsupials as an example, we examine some of these difficulties, including challenges in collecting uncommon host species, the ongoing description of new species of marsupials, the presence of cryptic species, and the decline in taxonomic expertise in Australia. Although optimistic global predictions have been made concerning the rate of discovery and description of new species of animals, these predictions may not apply in the case of specific groups of animals such as the Australasian marsupials. Global predictions In recent decades, there has been considerable interest in quantifying the extent of biodiversity on Earth. There are differing views about the numbers of extant eukaryotic species, but this is currently estimated to be 5 3 million, of which 1.5 million are named [1]. A study investigating the feasibility of naming the remaining species presented a positive assessment [1] based on an increase in the number of taxonomists globally and an increase in the number of taxonomic publications. Although parasites were initially overlooked in surveys of biodiversity, the significance of their contribution is now established [2], but the estimated number of potential (helminth) parasites present in vertebrates continues to be disputed [3]. Although the potential number of extant species can be estimated using sophisticated statistical methods [4] and the problems of assessing parasite diversity have been examined in detail [2], the number of named species remains the basis on which most assessments of biodiversity are currently made. For such assessments, global databases such as the Global Biodiversity Information Facility (GBIF) (containing 1474 643 animal species) and, on a regional basis, the Atlas of Living Australia (ALA), provide valuable information. Equally informative can be checklists of parasites for particular groups of hosts, such as those for African vertebrates [5], a particular geographical region of the world such as Papua New Corresponding author: Beveridge, I. ([email protected]). Keywords: helminths; marsupials; Australasia; biodiversity. 1471-4922/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pt.2014.10.007
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Guinea [6], or even a particular group of hosts such as the rhinoceroses [7]. However, such reviews are limited in number and for many regions of the world such databases or checklists do not exist. This is of particular concern with respect to the helminth (nematode, cestode, trematode, and acanthocephalan) parasites of wildlife. Although there is increasing interest in this discipline, the literature documenting the helminth parasites of wildlife is both limited and fragmented, with few overviews. Ideally, for scientists involved in managing wildlife populations, accurate documentation of the parasites present in them as well as their potential pathogenicity would be an extremely useful tool. Unfortunately, these data are rarely available. There are numerous impediments involved in a comprehensive understanding of the biodiversity of parasites in wildlife and in this review these difficulties are investigated using the Australasian marsupials as an example. Australasia here is considered to constitute Australia, Papua New Guinea, and the islands south of Wallace’s Line. As these marsupials constitute a taxonomically and geographically defined group of mammals, they provide an obvious exemplar to investigate what is known and what is not known about the parasites of this highly distinctive group of mammals and to assess the need for such information and how it might be acquired in this specific environment. The Australasian marsupials The Australasian marsupials constitute a phylogenetically defined group of mammals belonging to the Australidelphia. They are essentially confined to Australia and New Guinea, although the South American monito del monte, Dromiciops gliroides, is also included within this taxon. The conventional hypothesis, supported by recent molecular data [8], is that marsupials reached Australia from South America in a single dispersal event before the breaking up of Gondwana, 40–60 million years ago, although limited, contradictory paleontological evidence exists suggesting a reverse migration [9]. In particular, Dromiciops may have migrated from Australia back into South America [8], although it appears to be the only genus in this category. Within Australasia, the marsupials have radiated to occupy various niches. The basally branching clades, the Dasyuromorphia and Peramelemorphia (collectively, the polyprotodont marsupials), contain various insectivores and carnivores ranging from the mouse-sized antechinuses
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(Dasyuridae) to the rat-sized bandicoots (Peramelidae), the cat-sized quolls (Dasyurus spp.), and the Tasmanian devil (Sarcophilus harrisii) (Figure 1). The more recent clades are herbivorous and are characterized by a distinctive diprotodont dentition with two procumbent lower incisors. The basal diprotodonts include the fossorial wombats (Vombatidae), which are the size of a small pig or large dog, as well as their relatives the arboreal, folivorous koalas (Phascolarctidae). The possums range in size from the mouse-sized pigmy possums (Burramyidae) to the rator cat-sized Phalangeridae (possums and cuscuses) and Pseudocheiridae (possums). The latter are arboreal folivores, some species of which have developed the capacity to glide and are therefore commonly referred to as ‘gliders’. The best-known marsupials are the rat kangaroos (Hypsiprymnodontidae and Potoroidae) and the wallabies and kangaroos (Macropodidae), distinguished primarily by their saltatory means of locomotion. Currently, 57 species of wallaby and kangaroo are recognized [10,11]. In addition, bizarre inclusions in the marsupial fauna include the marsupial moles (Notoryctomorphia), which live in sand dunes in central Australia and are probably a sister group to the Dasyuromorphia and Peramelemorphia. From the viewpoint of parasite diversity, it is also important to take into account the remaining terrestrial mammals that occur on the continent, as transfer of parasites has
obviously occurred between these other major groups. Three species of monotreme are currently extant: two species of echidna and the platypus. They are remnants of a much more diverse fauna and have a long fossil record on the continent. The rodent fauna is diverse, with 70 species, all belonging to the Muridae, known at the time of European settlement. Murid rodents are thought to have arrived in Australia between 5 and 15 million years ago from Southeast Asia [12]. Currently, there are 82 species of bat recognized in Australia [10], with the greatest diversity in the north, presumably because the original route of entry to the continent was from Southeast Asia [13]. The dingo, Canis lupus familiaris, is thought to have arrived in northern Australia from Southeast Asia about 4000 years ago [10], while introductions of domestic animals as well as foxes, rabbits, and hares began about 200 years ago. Helminth parasites of Australasian marsupials Due to the relative isolation of the Australasian marsupials during their major period of diversification, it may be expected that they would harbor a relatively limited number of parasite orders and families, even if extensive radiations within particular orders or families were present. However, no fewer than 41 families and 130 genera of helminths had been recorded from Australasian marsupials by 1991 [14] (Table 1). Although many new species
Dasyuromorphia
Exnct
Peramelemorphia
Diprotodona
Macropodoidea
Vombaformes
Notoryctomorphia
Phalangerida
Thylacinidae
Tasmanian ger
Dasyuridae
Nave cats, devils, antechinus
Myrmecobiidae
Ant-eater
Peramelidae
Bandicoots
Thalacomyidae
Rabbit-eared bandicoots
Notorycdae
Mole
Phascolarcdae
Koala
Vombadae
Wombats
Potoroidae
Potoroos
Macropodidae
Kangaroos, Wallabies
Phalangeridae
Cuscus, Phalangers
Burramyidae
Pygmy possums
Pseudocheiridae
Ring-tailed possums
Petauridae
Gliders
Tarsipedidae
Honey possum TRENDS in Parasitology
Figure 1. Phylogenetic relationships of the Australasian families of marsupials. Adapted from [14].
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Table 1. Diversity of families, genera, and species of helminth parasites in Australasian marsupials estimated in 1991a (left) and currently (right) No. families Phylum Platyhelminthes Class Digenea Cestoda Phylum Nematoda Order Ascaridida Spirurida Oxyurida Strongylida Rhabditida Enoplida Phylum Acanthocephala Total
No. genera
No. species
9 5
16 16
19 21
28 77
39 97
4 8 1 8 1 3 2 41
7 14 5 64 2 4 2 130
10 15 6 70 2 3 2 148
13 37 6 261 4 6 2 434
29 46 7 407 5 24 4 658
a
Reproduced from [14].
have been described more recently (Table 1), the number of orders and families has not changed significantly and the current tally includes most of the families commonly encountered in terrestrial vertebrates. Of the families encountered in marsupials, only two are represented by parasites of introduced livestock that have been able to switch to marsupial hosts [the common liver fluke, Fasciola hepatica (Fasciolidae), and the hydatid Echinococcus granulosus (Taeniidae)]. The currently described marsupial helminth fauna therefore represents a truly diverse radiation for a geographically isolated group of mammals. Current evidence suggests that the helminth fauna of Australasian marsupials has multiple origins [14]. It includes a Gondwanan component related to the parasites of South American marsupials. Examples include the cestode genus Paralinstowia, which occurs on both continents, and the potentially related trichostrongyloid nematode families Viannaiidae in South American marsupials and Herpetostrongylidae in Australasian marsupials [14]. Beyond these few examples, however, the helminth faunas of the two groups of marsupials differ markedly. Other families of parasites have possibly been acquired from monotremes, as exemplified by the endemic Australian trichostrongyloid family Mackerrastrongylidae, which occurs in both monotremes (echidnas) and marsupials [14]. Finally, there are instances of parasites being introduced to the continent by rodents and bats arriving from Southeast Asia [14]. The spirurid nematode Spirura aurangabadensis occurs in bats in Southeast Asia and in Australian carnivorous marsupials, while cestodes of the genus Bertiella (Anoplocephalidae) occur in rodents in Southeast Asia as well as rodents in Australia and in arboreal marsupials [14]. However, all current hypotheses are provisional and are subject to validation by future studies. For many species of parasite, their phylogeny is poorly understood and hence their origins remain debatable. As might be expected, the various parasite families are not distributed evenly among marsupial groups. For example, hymenolepidid and linstowiid cestodes, as well as 144
spirurid nematodes, which utilize arthropods as intermediate hosts, tend to be most common in the insectivorous and carnivorous dasyurids and peramelids. By contrast, anoplocephalid cestodes and strongylid nematodes are restricted to the herbivorous diprotodonts (wombats, koalas, kangaroos, and wallabies), as the infective stages occur on and are ingested with vegetation. Other nematode groups, such as the trichostrongylid, metastrongylid, and filarioid nematodes, occur across host groups because they require no intermediate hosts, use mollusks as intermediate hosts that are ingested deliberately by carnivores or accidentally by herbivores, or are transmitted by biting arthropods. Parasite diversity is relatively high in the terrestrial, omnivorous dasyurids and peramelids but declines substantially in the arboreal pseudocheirids and phalangerids, possibly due to their arboreal lifestyle, and increases again in the terrestrial kangaroos and wallabies [14]. Recent studies of the parasites of tree kangaroos have provided some support for this observation, as most tree kangaroo species harbor very few species of cloacinine nematode, although Dendrolagus mbaiso, a tree kangaroo that is secondarily terrestrial, living mainly above the tree line in Irian Jaya, has an abundant cloacinine nematode fauna [15]. Not only is the Australasian helminth parasite fauna highly endemic (97% [14]), but it also includes remarkable instances of convergent evolution as well as unique morphological diversification. Hypodontus macropi, a parasite of the ileum and large intestine of kangaroos and wallabies, is a strongylid nematode morphologically convergent with the hookworms of eutherians (the ancylostomatids), possessing a deviated anterior end and a large oral opening with cutting plates such as those found in the true hookworms (Figure 2). The anoplocephalid cestode genus Triplotaenia, found in kangaroos and wallabies, contains species with a
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Figure 2. Mouth of Hypodontus macropi (Nematoda: Strongyloidea), a strongyloid nematode parasite of kangaroos, with paired cutting plates resembling those found in the hookworm (ancylostomatoid) parasites of eutherian mammals. Reproduced from [55].
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longitudinally divided strobila and loss of external segmentation (Figure 3), parallels seen only in the cestode parasites of elasmobranchs. Consequently, the parasite fauna of marsupials is not only highly endemic but also contains some remarkable examples of convergent evolution among parasites [14]. However, from the broader perspective, questions need to be posed regarding how well studied this group of parasites is and how far we are from knowing the true extent of diversity in the helminth parasites of Australasian marsupials. First, not all of the extant species of marsupial have been examined for parasites. By 1991, 87 of 211 (41%) marsupial species had no record of helminth parasites; currently, this proportion has fallen slightly (37%), but significant numbers of species remain to be examined (Table 2). On the basis of the proportion of species in each family examined, the families Dasyuridae (48%), Peramelidae (53%), Phalangeridae (52%), Burramyidae (14%), and Petauridae (50%) clearly warrant additional attention. In the case of some marsupial species, it may be that they harbor very few parasite species (e.g., Burramyidae [14]) (possibly due to their small size, arboreal habitat, and feeding on nectar as well as arthropods) and that negative findings have simply not been reported in the scientific literature. However, to what extent this issue extends to other marsupial taxa is not fully known. The lack of collections from particular species may stem from a number of reasons. The species involved may be rare or threatened, thereby limiting opportunities to collect parasites, or they may have remote habitats and the parasites may be difficult to collect. One example is the New Guinea tree kangaroo, Dendrolagus mbaiso, which occurs only at high altitudes in the Sudirman Range in Irian Jaya [16]. Only one scientific specimen (the holotype) has ever been obtained; fortunately, the parasites of this tree kangaroo were preserved and have been described [17–19]. However, many other species of marsupial in both Australia and Papua New Guinea are difficult to collect for similar logistical reasons.
Table 2. Numbers of Australasian marsupials from which parasites have been recorded: current figures (left) and figures from 1991 (right) Host group
Dasyuridae Myrmecobiidae Thylacinidae Notoryctidae Peramelidae Thalacomyidae Phalangeridae Burramyidae Petauridae Hypsiprymnodontidae 1 Potoroidae Macropodidae Phascolarctidae Vombatidae Tarsipedidae Total
No. of species with parasite records 34 1 1 1 9 2 13 1 14 1 8 53 1 3
27 1 1 1 7 2 12 2 13
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124
5 48 1 3
No. of species without parasite records 37
33
1 8
1 9
12 6 14
14 5 11
5
4 9
1 84
1 87
Even in instances where there are published records, they may be from a single host individual, as exemplified above. For marsupial families with low parasite diversity (Phascolarctidae, Pseudocheiridae), examining a few individuals may be adequate as it may be that the few parasites to which they are host occur at a high prevalence and therefore will be encountered in a small sample of hosts. However, for highly diverse parasite communities such as those found in the fore-stomachs of kangaroos and wallabies, with total burdens sometimes reaching 500 000 [20] (Figure 4), uncommon species may be easily overlooked [21]. It has been estimated [22] that in the case of the complex helminth communities found in four species of
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Figure 3. The scolex of Triplotaenia mirabilis (Cestoda: Anoplocephalidae), an intestinal cestode of wallabies, with the strobila split into two, loss of segmentation, and a tag of unsegmented tissue between the two major branches of the strobila, providing the basis for the generic name. Reproduced from [55].
Figure 4. The stomach contents of an agile wallaby (Macropus agilis) showing the abundance of strongyloid nematodes commonly encountered in the stomachs of macropodid marsupials. The large nematodes are Labiostrongylus labiostrongylus, but the smaller nematodes visible include numerous genera and species.
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Review kangaroo and wallaby, samples of 10–18 animals resulted in the recovery of between 93% and 97% of the helminth parasite species. A similar estimate suggested that a sample size of 18 western grey kangaroos (Macropus fuliginosus) was needed to recover all of the species of helminth parasite [23] whereas examination of a single specimen of a rock wallaby species (Petrogale) results in the recovery on average of 8.6 helminth species [24]. It is therefore noteworthy that for only 31 (57%) of the known 54 species of kangaroo and wallaby have more than five individuals been examined (unpublished observations), suggesting that current estimates of parasite biodiversity even within this family of marsupials are gross underestimates. An additional factor influencing the discovery of new species is their geographical distribution. Recently, a new species of the nematode genus Cloacina has been described that has an extremely restricted geographical range despite the fact that the kangaroo host, which is abundant, is distributed across thousands of square kilometers virtually over the entire continent [25]. In a continent of the size of Australia, the possibility of finding highly localized parasite species presents a significant problem. The examples cited here are derived from the parasite faunas of macropodids, but the extent to which these factors apply to marsupial families with less diverse helminth faunas remains unclear. Cryptic species Additional difficulties in estimating levels of biodiversity are provided by the presence of cryptic species detectable in parasitic helminths primarily by molecular methods. In Australasian marsupials, this appears to be a significant issue in the case of both cestodes and nematodes. The topic was reviewed recently [26], with several instances of apparently generalist helminth parasites being split into ten or more species once genetic studies had been undertaken. Two nematode taxa – Hypodontus macropi, found in the ileum, cecum, and colon, and Rugopharynx australis, found in the stomach – and the cestode Progamotaenia festiva, found in the bile ducts of macropodids, were cited as examples [27–29], but several others were identified in which taxonomic recognition lags behind the molecular recognition of cryptic species. These studies targeted parasite taxa that appeared to be generalists and occur in a wide range of host species. However, substantial numbers of taxa occurring in more than a single host await genetic examination. It was concluded [26] that the occurrence of cryptic species in marsupial helminths appeared to be almost random, thereby severely limiting any predictions concerning estimates of biodiversity. Nevertheless, the use of molecular tools is dramatically increasing the number of species and hence the biodiversity found within the parasites of marsupials. New hosts A further potentially confounding factor in assessments of biodiversity is the rate at which new species of marsupial hosts are being described through the discovery of entirely new species, such as within the dasyurid genus Antechinus [30–32], the rediscovery of species previously thought to be extinct such as Gilbert’s potoroo (Potorous gilberti) [33], or 146
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the splitting of existing species such as has occurred within the rock wallabies (Petrogale spp.), with 10 species (including 20 chromosome races) recognized in 1982 [34] compared with the 16 species now recognized [35]. Currently, the systematics of the short-eared rock wallaby, Petrogale brachyotis, from northern Australia is under review, with eight geographically distinct lineages recognized, several of which may represent independent species [36]. Such changes in host status may have significant implications for parasite biodiversity. Preliminary genetic studies of three species of nematode belonging to the genus Cloacina (Cloacina robertsi, Cloacina caenis, and Cloacina pearsoni) from the stomachs of a series of parapatric species of rock wallaby occurring along the north-east coast of Australia have demonstrated genetic differences between specimens from each host species, leading to the possibility that the three currently recognized morphospecies occurring in this range of closely related hosts may represent 15 genetically distinguishable nematode species [37]. Studies of the large numbers of remaining helminth parasites of this host species complex are yet to be undertaken. As previously noted [26], molecular studies to date have concentrated on the parasites of kangaroos and wallabies, with no studies of the equally highly diverse nematode parasite fauna found in dasyurids and peramelids. Additional surprises in terms of biodiversity may await molecular investigations examining the helminth parasites of these groups. Site in host An additional factor in assessing parasite biodiversity is that the largest and most easily recovered parasites are those most likely to be described first. This phenomenon has been demonstrated quantitatively in the case of monogenean parasites of fish, with a greater number of smaller species having been described in recent years [2]. In the case of marsupials, rather than parasite size, more species are being described from locations outside the gastrointestinal tract, which has been the focus of many parasitologists in the past. Nematodes in particular are being recovered from the subcutaneous connective tissues, the accessory male genital glands, the tongue, the orbit of the eye, the vasculature, and other sites that may not be routinely examined [38–46]. In the case of the filarioid nematodes, detecting infection may be difficult, and in the abdominal cavity it is often only nematode movement that differentiates the parasites from nerves and lymphatics, rendering reliable collection difficult and the likelihood of overlooking infections high. Parasite extinctions Australia has one of the worst records globally in terms of mammal extinctions [47] and we can have little idea of the extent of parasite biodiversity that has already been lost. This issue has been addressed by several authors (e.g., [48]). The Australian state of Tasmania has been the only jurisdiction in the country to include a parasite on its list of endangered species. Dasyurotaenia robusta, a cestode parasite of the Tasmanian devil, has been described from specimens collected in captive animals [49] but apparently has a very localized distribution in Tasmania, having been found at only one locality, Collins Gap, in a survey of 153 devils
Review from around Tasmania [50] (D.L. Obendorf, personal communication). The current decimation of the devil population due to facial tumor disease [51] may already have resulted in the extinction of D. robusta, although this is unknown as no surveys have been established to monitor the fate of this parasite, despite it being placed on an endangered species list. In the case of other critically endangered marsupial species such as the northern hairy-nosed wombat, Lasiorhinus krefftii, no consideration appears to have been given to its unique parasites such as the nematode Oesophagostomoides eppingensis. The parasites of additional endangered marsupial species are very poorly known. Taxonomic impediment In recent years it has been widely recognized that a significant limitation to the description of new species of parasites has been the decline in the number of active taxonomists [52]. By contrast, other reports [1] suggest that globally the numbers of taxonomists and of taxonomic publications are increasing. However, the impact of the taxonomic decline is probably most important at the local rather than the global scale. Despite the Australasian region being recognized as a region of high biodiversity [53], and this being also evident in the case of helminth parasites, within the country taxonomic expertise is in serious decline and has been described as a ‘crisis’ [54]; currently there are virtually no taxonomists employed within the area of helminth biodiversity in Australia. As a consequence, the optimistic global perspective [1] hardly applies to Australia and its endemic helminths are not readily available to workers in overseas institutions, even if such workers existed. Consequently, the optimistic view of describing all new taxa [1] is probably not applicable to this localized situation and probably not to several other, similar regions. Concluding remarks The helminth parasites of Australasian marsupials highlight the significance and difficulties of assessing the biodiversity of parasites of wildlife. This example is relevant for several reasons. At a purely scientific level, it matters in terms of our attempts to understand the processes of parasite evolution and to assess levels of parasite diversity as increasing numbers of marsupial hosts move toward extinction. Once the hosts are extinct, we can never study their parasites and hence how they might have coevolved with their hosts. We therefore lose significant insights into parasite evolution. On a more practical basis, wildlife managers and those managing recovery programs for endangered marsupial species require information about their parasites, which might be lost with the extinction of host populations. In the current recovery program for the threatened Tasmanian devil, no consideration has been directed toward its host-specific parasites, although one (D. robusta) has been for some time included on an official endangered species list. In addition, wildlife managers dealing with declines in the number of mammalian species are obliged to deal with potential threats due to parasites. Without an adequate catalog of parasite diversity and an assessment of the pathogenicity of individual parasites, it is difficult to
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assess their possible threat to host survival. For this reason alone, the documentation of parasite diversity is valuable. The Australasian region has always been recognized as having a diverse endemic fauna, much of which has not been described. This applies equally to the parasitic helminths of marsupials. However, due to the decline of local taxonomic expertise it seems highly unlikely that the existing biodiversity will ever be adequately catalogued. The factors affecting helminth biodiversity in a general sense have been exhaustively evaluated elsewhere [2]. Here we substantiate many of their general conclusions using the specific example of the helminths of marsupials, but can provide no substantive evidence to support the suggestion [1] that the description of this unique parasite fauna of Australasian wildlife is ever likely to be comprehensively described. References 1 Costello, M.J. et al. (2013) Can we name the Earth’s species before they go extinct? Science 339, 413–416 2 Poulin, R. and Morand, S. (2004) Parasite Biodiversity, Smithsonian Institution Press 3 Strona, G. and Fattorini, S. (2014) Parasitic worms: how many really? Int. J. Parasitol. 44, 269–272 4 Gotelli, N.J. and Colwell, R.K. (2011) Estimating species richness. In Biological Diversity: Frontiers in Measurement and Assessment (Magurran, A.E. and McGill, B.J., eds), pp. 39–54, Oxford University Press 5 Canaris, A.G. and Gardner, S.L. (2003) Bibliography of Helminth Species Described from African Vertebrates 1800–1967, Harold W. Manter Laboratory for Parasitology (http://digitalcommons.unl.edu/ parasitologyfacpubs/3) 6 Owen, I.L. (2011) Parasites of animals in Papua New Guinea recorded at the national veterinary laboratory: a catalogue, historical review and zoogeographical affiliations. Zootaxa 3143, 1–163 7 Knapp, S.E. et al. (1997) Helminths and arthropods of black and white rhinoceroses in southern Africa. J. Wildl. Dis. 33, 492–502 8 Nilsson, M.A. et al. (2010) Tracking marsupial evolution using archaic genomic retroposon insertions. PLoS Biol. 8, e1000436 9 Beck, M.D.B. et al. (2007) Australia’s oldest marsupial fossils and their biogeographical implications. PLoS ONE 3, e1858 10 van Dyck, S. and Strahan, R. (2008) The Mammals of Australia. (3rd edn), Reed New Holland 11 Flannery, T.F. (1995) Mammals of New Guinea, Reed Books 12 Breed, W.G. and Aplin, K.P. (2008) Order Rodentia and Family Muridae. In The Mammals of Australia (3rd edn) (van Dyck, S. and Strahan, R., eds), pp. 574–577, Reed New Holland 13 Richards, G.C. (2008) Order Chiroptera. In The Mammals of Australia (3rd edn) (van Dyck, S. and Strahan, R., eds), pp. 420–423, Reed New Holland 14 Beveridge, I. and Spratt, D.M. (1996) The helminth fauna of Australasian marsupials: origins and evolutionary biology. Adv. Parasitol. 37, 135–254 15 Flannery, T.F. et al. (1996) Tree Kangaroos: A Curious Natural History, Reed Books 16 Flannery, T. et al. (1995) A new tree kangaroo (Dendrolagus: Marsupialia) from Irian Jaya, Indonesia, with notes on ethnography and the evolution of tree kangaroos. Mammalia 59, 65–84 17 Beveridge, I. (1997) Macropostrongyloides dendrolagi n. sp. and Mbaisonema coronatum n.g., n.sp., two new species of nematodes (Strongyloidea: Cloacinidae) from tree-kangaroos, Dendrolagus spp. (Marsupialia: Macropodidae) from Irian Jaya, Indonesia. Syst. Parasitol. 38, 25–31 18 Beveridge, I. (2002) New species and new records of Cloacina von Linstow, 1898 (Nematoda: Strongyloidea) parasitic in macropodid marsupials from Papua New Guinea. Rec. S. Aust. Mus. 35, 1–32 19 Smales, L.R. (1997) A new species of Dorcopsinema Mawson, 1977 (Nematoda: Cloacinidae) from the tree kangaroo Dendrolagus mbaiso (Marsupialis: Macropodidae) from Irian Jaya, Indonesia and new host records for Dorcopsinema dendrolagi. Syst. Parasitol. 38, 131–135 147
Review 20 Beveridge, I. and Arundel, J.H. (1979) Helminth parasites of grey kangaroos, Macropus giganteus Shaw and M. fuliginosus (Desmarest), in eastern Australia. Aust. Wildl. Res. 6, 69–77 21 Vendl, C. and Beveridge, I. (2014) Estimation of species richness in the complex communities of nematode parasites found in the stomachs of kangaroos and wallabies (Family Macropodidae). Trans. R. Soc. S. Aust. 138, 105–112 22 Aussavy, M. et al. (2011) Helminth parasite communities in four species of sympatric macropodids in western Victoria. Aust. Mammal. 33, 13–20 23 Webley, L.S. et al. (2004) Endoparasites of an insular subspecies of the western grey kangaroo, Macropus fuliginosus. Aust. J. Zool. 52, 623–634 24 Beveridge, I. et al. (1989) Helminth parasites of rock wallabies, Petrogale spp. (Marsupialia) from Queensland. Aust. Wildl. Res. 16, 273–287 25 Beveridge, I. et al. (2014) Description of Cloacina atthis sp. nov. from the stomach of the euro (Macropus robustus) (Marsupialia: Macropodidae) from Western Australia based on morphological and molecular criteria. Parasitol. Res. 113, 3485–3493 26 Beveridge, I. and Gasser, R.B. (2014) Diversity in parasitic helminths in Australasian marsupials and monotremes: a molecular perspective. Int. J. Parasitol. 44, 859–864 27 Chilton, N.B. et al. (2012) Genetic variation within the Hypodontus macropi (Nematoda: Strongyloidea) complex from macropodid marsupial hosts in Australia. Electrophoresis 33, 3544–3554 28 Beveridge, I. and Chilton, N.B. (1999) Revision of the Rugopharynx australis (Moennig, 1926) complex (Nematoda: Strongyloidea) from macropodid marsupials. Invert. Taxon. 13, 805–843 29 Beveridge, I. and Shamsi, S. (2009) Revision of the Progamotaenia festiva species complex (Cestoda: Anoplocephalidae) from Australasian marsupials, with the resurrection of P. fellicola (Nybelin, 1917) comb. nov. Zootaxa 1990, 1–29 30 Baker, A.M. et al. (2012) A new dasyurid marsupial from eastern Queensland, Australia: the buff-footed antechinus, Antechinus mysticus sp. nov. (Marsupialia: Dasyuridae). Zootaxa 3515, 1–237 31 Baker, A.M. et al. (2013) A new dasyurid marsupial from Kroombit Tops, south-east Queensland, Australia: the silver-headed antechinus, Antechinus argentus sp. nov. (Marsupialia: Dasyuridae). Zootaxa 3746, 201–239 32 Baker, A.M. et al. (2014) The black-tailed antechinus, Antechinus arktos sp. nov.: a new species of carnivorous marsupial from montane regions of the Tweed Volcano caldera, eastern Australia. Zootaxa 3765, 101–133 33 Sinclair, E.A. and Westerman, M. (1997) Phylogenetic relationships within the genus Potorous (Marsupialia: Potoroidae) based on allozyme electrophoresis and sequence analysis of the cytochrome-b gene. J. Mamm. Evol. 4, 147–167 34 Briscoe, D.A. et al. (1982) Isolation, introgression and genetic variation in rock wallabies. In Species at Risk: Research in Australia (Groves, R.H. and Ride, W.D.L., eds), pp. 73–97, Australian Academy of Science 35 Eldridge, M.D.B. (2008) Rock wallabies: Petrogale. In The Mammals of Australia (3rd edn) (van Dyck, S. and Strahan, R., eds), pp. 361–362, Reed New Holland
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36 Potter, S. et al. (2012) Multiple biogeographical barriers across the monsoon tropics of northern Australia: phylogeographic analysis of the brachyotis group of rock wallabies. Mol. Ecol. 21, 2254–2269 37 Chilton, N.B. et al. (2009) Genetic variation within species of the nematode genus Cloacina (Strongyloidea: Cloacininae) parasitic in the stomachs of rock wallabies, Petrogale spp. (Marsupialia: Macropodidae) in Queensland. Aust. J. Zool. 57, 1–10 38 Spratt, D.M. (1972) Aspects of the life-history of Dirofilaria roemeri in naturally and experimentally infected kangaroos and wallabies. Int. J. Parasitol. 2, 139–156 39 Spratt, D.M. (1982) Anatrichosoma haycocki sp. n. (Nematoda: Trichuridae) from the paracloacal glands of Antechinus spp., with notes on Skrjabinocapillaria Skarbilovitsch. Ann. Parasitol. Hum. Comp. 57, 63–71 40 Spratt, D.M. (1984) Further studies of the lung parasites (Nematoda) from Australian marsupials. Aust. J. Zool. 32, 283–310 41 Spratt, D.M. (2006) Description of capillariid nematodes (Trichinelloidea: Capillariidae) parasitic in Australian marsupials and rodents. Zootaxa 1348, 1–82 42 Spratt, D.M. (2011) New records of filarioid nematodes (Nematoda: Filarioidea) parasitic in Australasian monotremes, marsupials and murids, with descriptions of nine new species. Zootaxa 2860, 1–61 43 Spratt, D.M. and Speare, R. (1982) Durikainema macropi gen. et sp. nov. (Muspiceoidea: Robertdollfusidae), a remarkable nematode from Macropodidae (Marsupialia). Ann. Parasitol. Hum. Comp. 57, 53–62 44 Spratt, D.M. and Whittington, R. (1989) Nematode parasites from the skin of the platypus, Ornithorhynchus anatinus (Monotremata). Syst. Parasitol. 13, 223–229 45 Spratt, D.M. and Gill, P.A. (1998) Durikainema phascolarcti sp. nov. (Muspiceoidea: Robertdollfusidae) from the pulmonary arteries of the koala, Phascolarctos cinereus, and associated pathological changes. Syst. Parasitol. 39, 101–106 46 Spratt, D.M. and Hobbs, R.P. (2003) Breinlia (Breinlia) ventricola sp. nov. from the heart of the red kangaroo, Macropus rufus, in Western Australia. Trans. R. Soc. S. Aust. 128, 67–71 47 Hatton, T. et al. (2011) Australia State of the Environment Report, Australian Government Department of Sustainability, Environment, Water, Population and Communities 48 Sprent, J.F.A. (1992) Parasites lost. Int. J. Parasitol. 22, 139–151 49 Beveridge, I. (1984) Dasyurotaenia robusta Beddard, 1912, and D. dasyuri sp. nov., from carnivorous Australian marsupials. Trans. R. Soc. S. Aust. 108, 185–195 50 Obendorf, D.L. et al. (1990) Trichinella pseudospiralis infection in Tasmanian wildlife. Aust. Vet. J. 67, 108–110 51 Loh, R. et al. (2006) The pathology of devil facial tumor disease (DFTD) in Tasmanian devils (Sarcophilus harrisii). Vet. Pathol. 43, 890–895 52 Kim, K.C. and Byrne, L.B. (2006) Biodiversity loss and the taxonomic bottleneck: emerging biodiversity science. Ecol. Res. 21, 794–810 53 Joseph, L. et al. (2014) Australia’s biodiversity: major features. In Biodiversity. Science and Solutions for Australia. pp. 13–36, CSIRO 54 Hall, K. (2008) Proceedings of the National Taxonomy Forum (Australia), Federation of Australian Scientific and Technological Societies 55 Beveridge, I. (1986) Biogeography of parasites in Australia. Parasitol. Today 2 (Suppl.), 53–57
