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Myxidium cf. immersum spores recovered from the Australian Museum. Light microscopy (A), histological section through the gallbladder stained with Giemsa (B) and scanning electron microscopy on black background. White arrows show the surface ridges and black arrows show two polar capsules per myxospore. Scale bar 10 μm (A, B), 2.5 μm (C); AM#158500 (A, C; Bufo marinus) and AM#162439 (B; Limnodynastes peronii).
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A parasite morphologically indistinguishable from Myxidium immersum (Myxozoa: Myxosporea) found in gallbladders of the invasive cane toad (Bufo marinus) was identified in Australian frogs. Because no written record exists for such a parasite in Australian endemic frogs in 19th and early 20th century, it was assumed that the cane toad introduced thi...
Contexts in source publication
Context 1
... examined myxospores from museum vouchers had 5-9 ridges on the myxospore surface (Additional file 1). Myxospore morphology was consistent under light microscopy (Figure 2A), histology ( Figure 2B) and scan- ning electron microscopy ( Figure 2C). The myxospores from individual host species were not identical in size, likely due to the effect of the ethanol or formalin fixation for an unknown period of time prior to being transferred into 70% ethanol at the Australian Museum. ...Context 2
... examined myxospores from museum vouchers had 5-9 ridges on the myxospore surface (Additional file 1). Myxospore morphology was consistent under light microscopy (Figure 2A), histology ( Figure 2B) and scan- ning electron microscopy ( Figure 2C). The myxospores from individual host species were not identical in size, likely due to the effect of the ethanol or formalin fixation for an unknown period of time prior to being transferred into 70% ethanol at the Australian Museum. ...Context 3
... examined myxospores from museum vouchers had 5-9 ridges on the myxospore surface (Additional file 1). Myxospore morphology was consistent under light microscopy (Figure 2A), histology ( Figure 2B) and scan- ning electron microscopy ( Figure 2C). The myxospores from individual host species were not identical in size, likely due to the effect of the ethanol or formalin fixation for an unknown period of time prior to being transferred into 70% ethanol at the Australian Museum. ...Citations
... We were not able to draw conclusions about individual parasite species due to low replication at the level of individual parasite species, but we had high statistical power for addressing questions about groups of parasite species (Wood et al. in press). If an extremely low number of specimens exist in your area of interest, you might alternatively consider re-orienting your question so that it requires only qualitative data (in which case taxonomic and geographical coverage are probably as crucial as statistical power); for example, simple presence/absence data have addressed questions about the date of invasion for non-native parasite species (Hartigan et al., 2010;Jorissen et al., 2020). ...
Many of the most contentious questions that concern the ecology of helminths could be resolved with data on helminth abundance over the past few decades or centuries, but unfortunately these data are rare. A new sub-discipline - the historical ecology of parasitism - is resurrecting long-term data on the abundance of parasites, an advancement facilitated by the use of biological natural history collections. Because the world's museums hold billions of suitable specimens collected over more than a century, these potential parasitological datasets are broad in scope and finely resolved in taxonomic, temporal and spatial dimensions. Here, we set out best practices for the extraction of parasitological information from natural history collections, including how to conceive of a project, how to select specimens, how to engage curators and receive permission for proposed projects, standard operating protocols for dissections and how to manage data. Our hope is that other helminthologists will use this paper as a reference to expand their own research programmes along the dimension of time.
... For parasite diversity, richness estimators can allow researchers to estimate parasite species richness at the saturation point of the species accumulation curve, even if sampling is insufficient to reach that saturation point (Gotelli & Colwell, 2001). Finally, if replication is truly limiting, researchers can pose questions that require only qualitative or semi-quantitative information; for example, presence/absence data are sufficient for estimating the date of a parasite species' invasion (Hartigan et al., 2010;Jorissen et al., 2020). ...
Many disease ecologists and conservation biologists believe that the world is wormier than it used to be—that is, that parasites are increasing in abundance through time. This argument is intuitively appealing. Ecologists typically see parasitic infections, through their association with disease, as a negative endpoint, and are accustomed to attributing negative outcomes to human interference in the environment, so it slots neatly into our worldview that habitat destruction, biodiversity loss and climate change should have the collateral consequence of causing outbreaks of parasites.
But surprisingly, the hypothesis that parasites are increasing in abundance through time remains entirely untested for the vast majority of wildlife parasite species. Historical data on parasites are nearly impossible to find, which leaves no baseline against which to compare contemporary parasite burdens. If we want to know whether the world is wormier than it used to be, there is only one major research avenue that will lead to an answer: parasitological examination of specimens preserved in natural history collections.
Recent advances demonstrate that, for many specimen types, it is possible to extract reliable data on parasite presence and abundance. There are millions of suitable specimens that exist in collections around the world. When paired with contemporaneous environmental data, these parasitological data could even point to potential drivers of change in parasite abundance, including climate, pollution or host density change.
We explain how to use preserved specimens to address pressing questions in parasite ecology, give a few key examples of how collections‐based parasite ecology can resolve these questions, identify some pitfalls and workarounds, and suggest promising areas for research. Natural history specimens are ‘parasite time capsules’ that give ecologists the opportunity to test whether infectious disease is on the rise and to identify what forces might be driving these changes over time. This approach will facilitate major advances in a new sub‐discipline: the historical ecology of parasitism.
... Assessing and protecting more endangered parasites will eventually increase the number of recorded extinctions (Goals 5 and 6), but we can also search for previously missed extinction events, and retrospectively reconstruct parasite declines. This can be accomplished for the recent past (i.e.,~150 years) by parasitological dissection of liquid-preserved specimens (Black, 1983;Hartigan et al., 2010;Howard et al., 2019;Johnson et al., 2003), combing feathers/fur for ectoparasites on preserved skins (Bell et al., 2015;Clayton and Walther, 1997;Hellenthal and Price, 1991;Mey, 2002;Valdez et al., 2009), or extracting parasite DNA from specimens (Ouellet et al., 2005;Talley et al., 2015;Weldon et al., 2004). To go further back in time (centuries to thousands of years), other sources, such as woodrat middens (Cole and Arundel, 2005;Webb and Betancourt, 1990), raptor pellets (Beltrame et al., 2016;Grayson, 2000), ancient DNA preserved in coprolites (Boast et al., 2018), host-symbiont cophylogenies (Doña and Johnson, in this special issue), and even whole parasites in frozen mammoths (Grunin, 1973) can be used to document prior parasite extinctions (Harmon et al., 2019). ...
Found throughout the tree of life and in every ecosystem, parasites are some of the most diverse, ecologically important animals on Earth—but in almost all cases, the least protected by wildlife or ecosystem conservation efforts. For decades, ecologists have been calling for research to understand parasites' important ecological role, and increasingly, to protect as many species from extinction as possible. However, most conservationists still work within priority systems for funding and effort that exclude or ignore parasites, or treat parasites as an obstacle to be overcome. Our working group identified 12 goals for the next decade that could advance parasite biodiversity conservation through an ambitious mix of research, advocacy, and management.
... For example, Howard, Davis, Lippert, Quinn, and Wood (2019) investigated the abundance of the nematode parasite Clavinema mariae in English sole Parophrys vetulus over 84 years by counting the C. mariae present in fluid-preserved fish specimens from the University of Washington Burke Museum Ichthyology Collection (UWFC). Hartigan, Phalen, and Šlapeta (2010) used natural history collections to assess whether a myxozoan parasite of an invasive cane toad was present in native Australian amphibian species before the introduction of the cane toad in 1935, and Johnson, Lunde, Zelmer, and Werner (2003) used fluid-preserved amphibians to determine whether amphibian limb abnormalities were caused by trematode metacercaria in the past, as they are in contemporary amphibians. ...
Long‐term datasets are needed to evaluate temporal patterns in wildlife disease burdens, but historical data on parasite abundance are extremely rare. For more than a century, natural history collections have been accumulating fluid‐preserved specimens, which should contain the parasites infecting the host at the time of its preservation. However, before this unique data source can be exploited, we must identify the artifacts that are introduced by the preservation process. Here, we experimentally address whether the preservation process alters the degree to which metazoan parasites are detectable in fluid‐preserved fish specimens when using visual parasite detection techniques. We randomly assigned fish of three species (Gadus chalcogrammus, Thaleichthys pacificus, and Parophrys vetulus ) to two treatments. In the first treatment, fish were preserved according to the standard procedures used in ichthyological collections. Immediately after the fluid‐preservation process was complete, we performed parasitological dissection on those specimens. The second treatment was a control, in which fish were dissected without being subjected to the fluid‐preservation process. We compared parasite abundance between the two treatments. Across 298 fish individuals and 59 host–parasite pairs, we found few differences between treatments, with 24 of 27 host–parasite pairs equally abundant between the two treatments. Of these, one pair was significantly more abundant in the preservation treatment than in the control group, and two pairs were significantly less abundant in the preservation treatment than in the control group. Our data suggest that the fluid‐preservation process does not have a substantial effect on the detectability of metazoan parasites. This study addresses only the effects of the fixation and preservation process; long‐term experiments are needed to address whether parasite detectability remains unchanged in the months, years, and decades of storage following preservation. If so, ecologists will be able to reconstruct novel, long‐term datasets on parasite diversity and abundance over the past century or more using fluid‐preserved specimens from natural history collections.
... For example, Johnson et al. (2003) dissected preserved North American amphibian specimens and confirmed that historical cases of amphibian limb malformation were -like contemporary cases -associated with infection by metacercariae (300-350 μm in length; Johnson et al. 2004) of the trematode Ribeiroia ondatrae. Myxospores of the myxozoan parasite Myxidium immersum were found in eight specimens of endemic Australian frog species but never in specimens collected before 1966, suggesting that the parasite may have been introduced when the cane toad (Rhinella marina) arrived in Australia in 1935 (Hartigan et al. 2010). Myxospores are minute, barely multicellular structures, and yet their integrity is maintained in liquid-preserved hosts. ...
Recent decades have brought countless outbreaks of infectious disease among wildlife. These events appear to be increasing in frequency and magnitude, but to objectively evaluate whether ecosystems are experiencing rising rates of disease, scientists require historical data on disease abundance. Specimens held in natural history collections represent a chronological archive of life on Earth and may, in many cases, be the only available source of data on historical disease patterns. It is possible to extract information on past disease rates by studying trace fossils (indirect fossilized evidence of an organism's presence or activity, including coprolites or feces), sequencing ancient DNA of parasites, and examining sediment samples, mummified remains, study skins (preserved animal skins prepared by taxidermy for research purposes), liquid‐preserved hosts, and hosts preserved in amber. Such use of natural history collections could expand scientific understanding of parasite responses to environmental change across deep time (that is, over the past several centuries), facilitating the development of baselines for managing contemporary wildlife disease.
... The potential impact of these parasites on the conservation of Australian frogs remains unknown but it has been suggested that myxosporean infections may represent a key threatening process contributing to amphibian decline (Sitjà-Bobadilla 2009; Hartigan et al. 2012cHartigan et al. , 2013. These two species originally were thought to be a single species, Cystodiscus immersus, that was introduced to Australia with the exotic cane toad (Rhinella marina) (Hartigan et al. 2010(Hartigan et al. , 2011(Hartigan et al. , 2012b(Hartigan et al. , 2012c. This hypothesis was put forward by Delvinquier (1986) after a survey of Australian frog gallbladders demonstrated similar myxospores to C. immersus in native Australian frogs and R. marina. ...
Wildlife parasitology is a highly diverse area of research encompassing many fields including taxonomy, ecology, pathology and epidemiology, and with participants from extremely disparate scientific fields. In addition, the organisms studied are highly dissimilar, ranging from platyhelminths, nematodes and acanthocephalans to insects, arachnids, crustaceans and protists. This review of the parasites of wildlife in Australia highlights the advances made to date, focussing on the work, interests and major findings of researchers over the years and identifies current significant gaps that exist in our understanding. The review is divided into three sections covering protist, helminth and arthropod parasites. The challenge to document the diversity of parasites in Australia continues at a traditional level but the advent of molecular methods has heightened the significance of this issue. Modern methods are providing an avenue for major advances in documenting and restructuring the phylogeny of protistan parasites in particular, while facilitating the recognition of species complexes in helminth taxa previously defined by traditional morphological methods. The life cycles, ecology and general biology of most parasites of wildlife in Australia are extremely poorly understood. While the phylogenetic origins of the Australian vertebrate fauna are complex, so too are the likely origins of their parasites, which do not necessarily mirror those of their hosts. This aspect of parasite evolution is a continuing area for research in the case of helminths, but remains to be addressed for many other parasitic groups.
... Many natural history collections contain vertebrates that were fixed in formalin and stored in ethanol, preserving parasite tissue as well as host tissue (e.g. Black, 1983;Hartigan, Phalen, & Šlapeta, 2010;Johnson, Lunde, Zelmer, & Werner, 2003). ...
... Past studies have used museum specimens to establish the historical presence of a parasite (e.g. Black, 1983;Frederick, McGehee, & Spalding, 1996;Hartigan et al., 2010;Hewson et al., 2014), but none-to our knowledge-have used museum specimens to reconstruct trajectories of change in the abundance of parasites. ...
Does disturbance increase or decrease parasite transmission among wildlife hosts? Ecologists cannot answer this controversial question, in part because few historical datasets rigorously document parasite abundance. Without such a baseline, it is difficult to determine whether contemporary ecosystems are experiencing elevated parasite burdens.
Here, we investigate change over time in the abundance of a parasite that affects the economic value of a fish species. Clavinema mariae is a nematode parasite of benthic fishes that is common in English sole (Parophrys vetulus) of Puget Sound, WA. We obtained historical records of its abundance from the literature and from unpublished government agency data, and resampled the same locations using the same methods in 2017. We also used a new approach by estimating the C. mariae burden for museum specimens of English sole collected between 1930 and 2016.
Both the historical data and museum specimen data suggested increases over time in C. mariae abundance, with robust agreement between the two approaches.
In addition to documenting a previously unrecognised ~eightfold increase in the burden of an economically important parasite, our work demonstrates—for the first time—that parasitological examination of liquid‐preserved museum specimens can produce reliable data on long‐term trends in parasite abundance, at a much greater temporal resolution than is possible to obtain from historical records.
Synthesis and applications. Defining a baseline state of infection is vital for natural resource management and policy, which must respond to the threat of disease; without such a baseline, managers attempting to maintain or recover the health of ecosystems under their stewardship are shooting in the dark. The method we present here—using museum specimens to reconstruct detailed chronologies of parasite abundance change—offers a solution. Our approach would allow managers to accurately characterise past disease states, informing the development of appropriate disease management targets. Given the broad representation and availability of liquid‐preserved specimens across ecosystems, geographic regions and host taxa, this solution may be feasible for the management of biological resources not only in marine ecosystems, but in freshwater and terrestrial ecosystems as well.
... However, museum collections could play an important role in revealing this historical baseline. For example, the emergence of a novel parasite in Australian frogs facilitated by the introduction of the cane toad (Rhinella marina) was discovered through the dissection of historical museum specimens [34]. Improved accessibility and utilisation of museum collections will help us to build a picture of 'what we had', and enable the analysis of historical trends [35]. ...
Parasites are the most abundant form of life on earth and are vital components of ecosystem health. Yet, it is only relatively recently that attention has been given to the risks of extinction that parasites face when their hosts, particularly wildlife, are endangered. In such circumstances, parasites that are host-specific with complicated life cycles are most at risk. Such extinction/coextinction events have been poorly documented, principally because of the difficulties of following such extinction processes in nature. Fortunately, we were presented with the rare opportunity to catalogue an endangered Australian marsupial's parasites; we present our near-complete catalogue here. We incorporate this catalogue into a predictive framework to understand which parasites might be most vulnerable to coextinction, which we hope will serve as a model for endangered hosts and their parasites elsewhere.
... A local extinction of Dasyurus hallucatus occurred in Australia where quolls were poisoned when they preyed on R. marina (Oakwood and Foster 2008), however as the effect was considered reversible, it was given MR in EICAT. R. marina have also been shown to be the hosts of a parasite negatively affecting native Australian frogs, which was not present in the area before the toads arrived (Hartigan et al. 2010(Hartigan et al. , 2011(Hartigan et al. , 2012. The formulation in GISS of a maximum disease impact (see Nentwig et al. 2016) leaves room for different assessors to score different impacts, based on their interpretation, which might have led to a high score in GISS and a MO in EICAT. ...
Classification of alien species’ impacts can aid policy making through evidence based listing and manage-ment recommendations. We highlight differences and a number of potential difficulties with two scoring tools, the Environmental Impact Classification of Alien Taxa (EICAT) and the Generic Impact Scoring System (GISS) using amphibians as a case study. Generally, GISS and EICAT assessments lead to very similar impact levels, but scores from the schemes are not equivalent. Small differences are attributable to discrepancies in the verbal descriptions for scores. Differences were found in several impact categories. While the issue of disease appears to be related to uncertainties in both schemes, hybridisation might be inflated in EICAT. We conclude that GISS scores cannot directly be translated into EICAT classifications, but they give very similar outcomes and the same literature base can be used for both schemes.
... A local extinction of Dasyurus hallucatus occurred in Australia where quolls were poisoned when they preyed on R. marina (Oakwood and Foster 2008), however as the effect was considered reversible, it was given MR in EICAT. R. marina have also been shown to be the hosts of a parasite negatively affecting native Australian frogs, which was not present in the area before the toads arrived (Hartigan et al. 2010(Hartigan et al. , 2011(Hartigan et al. , 2012. The formulation in GISS of a maximum disease impact (see Nentwig et al. 2016) leaves room for different assessors to score different impacts, based on their interpretation, which might have led to a high score in GISS and a MO in EICAT. ...
Classification of alien species' impacts can aid policy making through evidence based listing and management recommendations. We highlight differences and a number of potential difficulties with two scoring tools, the Environmental Impact Classification of Alien Taxa (EICAT) and the Generic Impact Scoring System (GISS) using amphibians as a case study. Generally, GISS and EICAT assessments lead to very similar impact levels, but scores from the schemes are not equivalent. Small differences are attributable to discrepancies in the verbal descriptions for scores. Differences were found in several impact categories. While the issue of disease appears to be related to uncertainties in both schemes, hybridisation might be inflated in EICAT. We conclude that GISS scores cannot directly be translated into EICAT classifications, but they give very similar outcomes and the same literature base can be used for both schemes.
