Nomenclatural stability and the longevity of helminth species names.

Although most Latin binomial names of species are valid, many are eventually unaccepted when they are found to be synonyms of previously described species, or superseded by a new combination when the species they denote are moved to a different genus. What proportion of parasite species names become unaccepted over time, and how long does it take for incorrect names to become unaccepted? Here, we address these questions using a dataset comprising thousands of species names of parasitic helminths from four higher taxa (Acanthocephala, Nematoda, Cestoda, and Trematoda). Overall, among species names proposed in the past two-and-a-half centuries, nearly one-third have since been unaccepted, the most common reason being that they have been superseded by a new combination. A greater proportion of older names (proposed pre-1950) have since been unaccepted compared to names proposed more recently, however most taxonomic acts leading to species names being unaccepted (through either synonymy or reclassification) occurred in the past few decades. Overall, the average longevity of helminth species names that are currently unaccepted was 29 years; although many remained in use for over 100 years, about 50% of the total were invalidated within 20 years of first being proposed. The patterns observed were roughly the same for all four higher helminth taxa considered here. Our results provide a quantitative illustration of the self-correcting nature of parasite taxonomy, and can also help to calibrate future estimates of total parasite biodiversity.

Description and molecular data of a new cestode parasite, Cladotaenia anomala n. sp. (Paruterinidae) from the Australasian harrier (Circus approximans Peale) in New Zealand.

Currently comprising 12 species infecting the gastrointestinal tracts of diurnal raptors (Falconiformes, Accipitriformes), species of Cladotaenia are diagnosed by their branching uterus, testes in two fields reaching the same level anteriorly, and small rostellum armed with taenioid hooks arranged in two rows. In this study we describe a new species of Cladotaenia recovered from a number of Australasian harriers Circus approximans, from the southern half of South Island, New Zealand. The new species is distinguished from other species by its single circle of hooks. It is closest, morphologically, to C. circi, but differs in the shape of the terminal proglottids and the number of uterine branches. Sequences of 28S and cox1 gene are presented. Genetically, Cladotaenia anomala n. sp. is closest to Cladotaenia globifera but differs morphologically in the size of the suckers, testes and eggs. This description constitutes the first record of a Cladotaenia species in New Zealand. We discuss some potential routes this parasite may have taken to arrive in New Zealand.

Gastrointestinal helminths of the Australasian harrier (Circus approximans Peale, 1848) in New Zealand, and description of a new species of nematode, Procyrnea fraseri n. sp. (Habronematidae).

The Australasian harrier Circus approximans, a native of Australia, New Zealand and the South Pacific, is an opportunistic hunter of small prey, although a large part of its diet consists of carrion, mainly from roadkill. Besides a record of a single, unnamed species of capillariid nematode there have been no investigations into the parasites of Australasian harriers in New Zealand. In this study, a helminthological survey of sixty-five deceased harriers from southern New Zealand uncovered a gastrointestinal helminth fauna consisting of six parasite species. Porrocaecum circinum (Nematoda) was previously described only from fragmented females, and a redescription is presented here. Procyrnea fraseri n. sp. (Nematoda) is described, and distinguished from its congeners by its slender body shape and shorter spicules. Strigea falconis (Trematoda) is reported for the first time in New Zealand. Cladotaenia anomalis (Cestoda) and Polymorphus circi (Acanthocephala) were previously described as new species elsewhere. An unnamed species of capillariid appears to be mainly confined to North Island and is rare in South Island. Prevalence and intensity metrics are given, and DNA sequences provided to accompany new re/descriptions. Potential intermediate hosts are discussed, and the origins of the helminths and their potential for pathogenicity are considered.

Description and molecular data for a new acanthocephalan parasite, Polymorphus circi n. sp. (Polymorphidae) from the Australasian harrier (Circus approximans Peale) in New Zealand.

Species of genus Polymorphus Lühe, 1911 (Polymorphidae) are acanthocephalans found in fish-eating birds and waterfowl. Although found in many parts of the world, including Australia, no records exist from New Zealand. Because of the largely aquatic intermediate host, Polymorphus species are rarely found in terrestrial birds of prey. During a study of the helminths of the Australasian harrier Circus approximans Peale specimens of Polymorphus were recovered that were found to be new to science. Polymorphus circi n. sp. is formally described and genetic sequence data presented. Specimens were distinguished from all other species by a combination of characters, including their proboscis hook arrangement (20-22 rows of 11-13 hooks), as well as absence of sexual dimorphism, trunk size, proboscis shape and egg size. These acanthocephalans were found in birds from areas with the potential to support freshwater, brackish or marine amphipods, but as yet the actual intermediate hosts are unknown.

Biases in parasite biodiversity research: why some helminth species attract more research than others.

As the number of known and described parasite species grows every year, one might ask: how much do we actually know about these species beyond the fact they exist? For free-living taxa, research effort is biased toward a small subset of species based on their properties or human-centric factors. Here, using a large data set on over 2500 helminth parasite species described in the past two decades, we test the importance of several predictors on two measures of research effort: the number of times a species description is cited following its publication, and the number of times a species' name is mentioned in the scientific literature. Our analysis highlights some taxonomic biases: for instance, descriptions of acanthocephalans and nematodes tend to receive more citations than those of other helminths, and species of cestodes are less frequently mentioned in the literature than other helminths. We also found that helminths infecting host species of conservation concern receive less research attention, perhaps because of the constraints associated with research on threatened animals, while those infecting host species of human use receive greater research effort. Intriguingly, we found that species originally described by many co-authors subsequently attract more research effort than those described by one or few authors, and that research effort correlates negatively with the human population size of the country where a species was discovered, but not with its economic strength, measured by its gross domestic product. Overall, our findings reveal that we have conducted very little research, or none at all, on the majority of helminth parasite species following their discovery. The biases in study effort we identify have serious implications for future research into parasite biodiversity and conservation.

Physical evidence of direct antagonistic interactions between trematodes in the host gut: the kiss of death?

Although within-host competition among parasites if often assumed to occur based on statistical patterns, actual physical evidence of direct antagonistic interactions between parasites, either intraspecific or interspecific, is very rare. Here, we report such evidence between and within two species of hemiurid trematodes infecting the deep-sea grenadier fish Coryphaenoides subserrulatus. We found pairs of worms attached together, with one worm using its ventral sucker against another worm, and sucking out a large protuberance on the victim. We also found single worms showing clear signs of past attacks. There was no evidence that these interactions were more common at high intensities of infection, where the conditions would be expected to be more conducive to competitive interactions. Our findings provide evidence that trematodes may cause some harm to co-occurring individuals, suggesting a direct form of interference competition among intestinal helminths.

Battle of the sexes: analysis of sex bias in host use and reporting practices in parasitological experiments.

Experimental approaches are among the most powerful tools available to biologists, yet in many disciplines their results have been questioned due to an underrepresentation of female animal subjects. In parasitology, experiments are crucial to understand host-parasite interactions, parasite development, host immune responses, as well as the efficacy of different control methods. However, distinguishing between species-wide and sex-specific effects requires the balanced inclusion of both male and female hosts in experiments and the reporting of results for each sex separately. Here, using data from over 3600 parasitological experiments on helminth-mammal interactions published in the past four decades, we investigate patterns of male versus female subject use and result reporting practices in experimental parasitology. We uncover multiple effects of the parasite taxon used, the type of host used (rats and mice for which subject selection is fully under researcher control versus farm animals), the research subject area and the year of publication, on whether host sex is even specified, whether one or both host sexes have been used (and if only one then which one), and whether the results are presented separately for each host sex. We discuss possible reasons for biases and unjustifiable selection of host subjects, and for poor experimental design and reporting of results. Finally, we make some simple recommendations for increased rigour in experimental design and to reset experimental approaches as a cornerstone of parasitological research.

Tracking life cycles of parasites across a broad taxonomic scale in a marine ecosystem.

Parasitic helminths exhibit remarkable diversity in their life cycles, although few parasite species have their whole life cycles resolved. Owing to the fact that parasite life stages within hosts are often not comparable using morphological data, genetic data provides convincing evidence of transmission pathways between intermediate and definitive hosts. We took this approach to an ecosystem level, genetically matching parasite (acanthocephalan, cestode, nematode and trematode) life stages across a broad taxonomic range of intermediate and definitive hosts (invertebrates, seabirds, elasmobranchs and teleost fish) in Otago's (New Zealand) coastal marine ecosystem. We identified which transmission routes are utilized by the most parasite species and assessed which intermediate hosts are most important in facilitating the transmission of parasites in this ecosystem. Our findings reveal 59 new records of larval parasites infecting their respective intermediate hosts and 289 transmission pathways utilized by 35 helminth species to complete their life cycles. Sprat, triplefin and arrow squid all hosted the highest number of larval parasite species, suggesting they play important roles as intermediate hosts. We then used the new life cycle data to provide a synthetic overview of the life cycles known for various parasite groups in New Zealand. This study highlights how studying parasite life cycles can enhance our understanding of the ecology and evolution of parasites and hosts in natural systems, beyond simply resolving life cycles.

Historical dispersal and host-switching formed the evolutionary history of a globally distributed multi-host parasite - The Ligula intestinalis species complex.

Studies on parasite biogeography and host spectrum provide insights into the processes driving parasite diversification. Global geographical distribution and a multi-host spectrum make the tapeworm Ligula intestinalis a promising model for studying both the vicariant and ecological modes of speciation in parasites. To understand the relative importance of host association and biogeography in the evolutionary history of this tapeworm, we analysed mtDNA and reduced-represented genomic SNP data for a total of 139 specimens collected from 18 fish-host genera across a distribution range representing 21 countries. Our results strongly supported the existence of at least 10 evolutionary lineages and estimated the deepest divergence at approximately 4.99-5.05 Mya, which is much younger than the diversification of the fish host genera and orders. Historical biogeography analyses revealed that the ancestor of the parasite diversified following multiple vicariance events and was widespread throughout the Palearctic, Afrotropical, and Nearctic between the late Miocene and early Pliocene. Cyprinoids were inferred as the ancestral hosts for the parasite. Later, from the late Pliocene to Pleistocene, new lineages emerged following a series of biogeographic dispersal and host-switching events. Although only a few of the current Ligula lineages show narrow host-specificity (to a single host genus), almost no host genera, even those that live in sympatry, overlapped between different Ligula lineages. Our analyses uncovered the impact of historical distribution shifts on host switching and the evolution of host specificity without parallel host-parasite co-speciation. Historical biogeography reconstructions also found that the parasite colonized several areas (Afrotropical and Australasian) much earlier than was suggested by only recent faunistic data.

Large-scale genetic investigation of nematode diversity and their phylogenetic patterns in New Zealand's marine animals.

Nematodes constitute one of the most speciose metazoan groups on earth, and a significant proportion of them have parasitic life styles. Zooparasitic nematodes have zoonotic, commercial and ecological significance within natural systems. Due to their generally small size and hidden nature within their hosts, and the fact that species discrimination using traditional morphological characteristics is often challenging, their biodiversity is not well known, especially within marine ecosystems. For instance, the majority of New Zealand's marine animals have never been the subject of nematode studies, and many currently known nematodes in New Zealand await confirmation of their species identity with modern taxonomic techniques. In this study, we present the results of an extensive biodiversity survey and phylogenetic analyses of parasitic nematodes infecting New Zealand's marine animals. We used genetic data to differentiate nematodes to the lowest taxonomic level possible and present phylogenies of the dominant clades to illustrate their genetic diversity in New Zealand. Our findings reveal a high diversity of parasitic nematodes (23 taxa) infecting New Zealand's marine animals (62 of 94 free-living animal species investigated). The novel data collected here provide a solid baseline for future assessments of change in diversity and distribution of parasitic nematodes.

Short and sweet: an analysis of the length of parasite species names.

In its advice to taxonomists, the International Commission on Zoological Nomenclature (ICZN) recommends that scientific species names should be compact, memorable, and easy to pronounce. Here, using a dataset of over 3000 species of parasitic helminths described in the past two decades, we investigate trends in the length of Latin specific names (=epithets) chosen by taxonomists. Our results reveal no significant temporal change in the length of species epithets as a function of year of description, with annual averages fluctuating around the overall average length of just over 9 letters. We also found that lengths of species epithets did not differ among the various host taxa from which the parasites were recovered, however acanthocephalan species have been given longer species epithets than other helminth taxa. Finally, although species epithets were shorter than genus names for three-quarters of the species in our dataset, we detected no relationship between the length of species epithets and that of genus names across all species included, i.e., there was no evidence that shorter species epithets are chosen to compensate for long genus names. We conclude by encouraging parasite taxonomists to follow the recommendations of the ICZN and choose species epithets that are, as much as possible, compact and easy to remember, pronounce and spell.

Male-biased selection of holotypes in parasite taxonomy: is it justified?

When a new parasite species is identified, a name-bearing specimen or holotype is designated as its reference standard. For most acanthocephalans and nematodes, the holotype is male, a bias which lacks scientific justification. We propose ways of redressing this imbalance and achieving fuller representation of each species in museum collections.

New specimens and molecular data provide validation of Apatemon jamiesoni n. sp. (Trematoda: Strigeidae) from water birds in New Zealand.

A study published in 2016 reported on an undescribed species of Apatemon (Strigeidae) from New Zealand that was previously well known from its larval stages. Only a single specimen from a mallard duck was available at the time, which was described and given the provisional name Apatemon sp. "jamiesoni". Specimens also obtained from a spotted shag were not in good enough condition to form the basis of a new species description. A black-backed gull has since been discovered with specimens of this strigeid, their identity confirmed by genetic similarity, allowing formal description and naming of this species. This paper provides a description of the new specimens from the black-backed gull, along with a comparison with the specimens from other bird hosts, reprises some data from Blasco-Costa et al. (Parasitol Res 115:271-289, 2016) and presents formally the name Apatemon jamiesoni n. sp. This species differs from all other species of Apatemon in its small size, particularly that of the ovary and testes. It is most similar to A. jamesi from which it differs in the size of the oral and ventral suckers.

What's in a name? Taxonomic and gender biases in the etymology of new species names.

As our inventory of Earth's biodiversity progresses, the number of species given a Latin binomial name is also growing. While the coining of species names is bound by rules, the sources of inspiration used by taxonomists are an eclectic mix. We investigated naming trends for nearly 2900 new species of parasitic helminths described in the past two decades. Our analysis indicates that the likelihood of new species being given names that convey some information about them (name derived from morphology, host or locality of origin) or not (named after an eminent scientist, or for something else) depends on the higher taxonomic group to which the parasite or its host belongs. We also found a consistent gender bias among species named after eminent scientists, with male scientists being immortalized disproportionately more frequently than female scientists. Finally, we found that the tendency for taxonomists to name new species after a family member or close friend has increased over the past 20 years. We end by offering suggestions for future species naming, aimed at honouring the scientific community's diversity and avoiding etymological nepotism and cronyism, while still allowing for creativity in crafting new Latin species names.

Is parasite taxonomy really in trouble? A quantitative analysis.

In recent years, several authors have warned that the number of trained experts in parasite taxonomy and systematics is declining rapidly, and that the whole field is at risk. However, to date there has been no quantitative analysis to support these claims. Here, we provide the first such assessment, focusing on helminths parasitic in fish as an example, and using a representative dataset comprising over 2000 helminth species described in the past two decades. Based on standard indices of inequality, we demonstrate that a small group of highly prolific taxonomists are associated with the vast majority of new species descriptions, indicating that the research output in parasite discovery is concentrated in the hands of a small number of individuals. This situation has not improved over time. Furthermore, there has been no turnover over time, i.e., no replacement of the most prolific taxonomists: the individual researchers ranking among the most prolific describers of new parasite helminth species in the past decade were generally also the most prolific in the decade before that. Finally, based on the year in which these most prolific taxonomists published their first species description, we estimate that a large proportion of them are in the latter stages of their career. Inequalities in research output are the norm across scientific disciplines. However, persistent inequality in the number of species description per author, coupled with the same individuals ranking as most prolific over time and a majority of them in late career, all combine to support earlier claims that parasite taxonomy may well face a crisis in the form of an impending loss of taxonomic expertise.

Gastrointestinal helminth parasites of the threatened Australasian crested grebe (Podiceps cristatus australis, Gould 1844) in New Zealand, with descriptions of Baruscapillaria kamanae n. sp. (Nematoda: Trichuridae) and Cryptocotyle micromorpha n. sp. (Trematoda: Opisthorchiidae).

The Australasian crested grebe Podiceps cristatus australis, Gould 1844 is restricted to Australia and New Zealand, where it is listed as Threatened and Nationally Vulnerable. For the first time in New Zealand, we report on the parasitic helminths infecting three individuals from Lake Wanaka, Otago, using morphological and molecular tools. Seven helminth species were found in the gastrointestinal tract: 2 nematodes (Contracaecum ovale and Baruscapillaria kamanae n. sp.), 4 trematodes (Australapatemon minor, Cryptocotyle micromorpha n. sp., Tylodelphys darbyi and Neopetasiger neocomensis), and 1 cestode (Confluaria pseudofurcifera). Except for T. darbyi, all are new records for New Zealand. A change of orthography is proposed for Neopetasiger neocomensis and N. pseudoneocomensis. Cryptocotyle micromorpha n. sp. (Opisthorchiidae) is distinguished from similar species by its small size, wholly extracaecal vitellaria and anteriorly looped uterus. Baruscapillaria kamanae n. sp. (Trichuridae) is distinguished from other freshwater species by a combination of vulva and spicule morphology. The helminth parasites found here are mostly the same as those from the grebe in the northern hemisphere, indicating that they have been carried with the host species in its spread to Australasia. However, the parasite fauna may be depauperate due to a diminishing reservoir of intermediate hosts in that geographical migration.

DISTRIBUTION AND DIVERSITY OF DIPLOSTOMIDS IN NEW ZEALAND.

Parasitism is one of the most common consumer strategies and contributes a large portion to biological diversity. Trematodes in the family Diplostomidae are common in freshwater ecosystems worldwide, often residing in the eyes or brain of fish and then infecting fish-eating birds as adults. As a result, some species have broad geographic distributions due to the bird host's motility. In contrast to the cosmopolitan nature of diplostomids, only a single species, Tylodelphys darbyi, has been identified in New Zealand to date, and only from the South Island. Tylodelphys darbyi has a 3-host life cycle consisting of an unidentified snail, a freshwater fish (Gobiomorphus cotidianus), and the Australasian crested grebe (Podiceps cristatus australis). To date, T. darbyi has been found in 2 locations, Lake Hayes, in the eyes of G. cotidianus, and Lake Wanaka, adults recovered from grebes. Considering the near ubiquity of the fish host in New Zealand, it is likely the bird, listed as nationally vulnerable, is the limiting factor in the range of T. darbyi. Up to 10 G. cotidianus were sampled from 10 mountain lakes known to have populations of grebe in the Otago and Canterbury regions of New Zealand's South Island. The eyes of all fish were examined and any metacercariae present were set aside for genetic analysis. In addition to expanding the known range of T. darbyi to at least 4 water bodies across the South Island, 2 new taxa of diplostomid were identified. A lens-infecting metacercariae clustered with Diplostomum spathaceum, while the metacercariae from the humor clustered with Diplostomum baeri.

Diomedenema dinarctos n. sp. (Spiruromorpha: Desmidocercidae), a new species of lung nematode in Fiordland crested penguins (Eudyptes pachyrhynchus; Sphenisciformes), from South Island, New Zealand.

Fiordland crested penguins Eudyptes pachyrhynchus Gray are thick-billed, crested penguins endemic to New Zealand that breed in small colonies in inaccessible places. They are assessed as Vulnerable by the IUCN. This is the first report of helminth parasites from this penguin species. Herein a new species of Diomedenema is described (Spiruromorpha, Desmidocercidae) from the lungs of Fiordland crested penguins. Diomedenema dinarctos n. sp. has only two congeners and is closest morphologically to D. tavaresi. It differs from D. tavaresi in overall larger size, longer buccal cavity and oesophagus, in the distance of the excretory pore and nerve ring from the anterior end, and the ratio of spicule sizes. Eggs are twice the size reported for D. tavaresi. The only other species, D. diomedeae, is far larger in body size, with a shorter buccal cavity and oesophagus and a reduced body length to oesophagus ratio. The position in the body length of the vulva and the spicule ratio also differ strongly. We provide a DNA sequence for the 18S rDNA gene. Species of Diomedenema have been reported as causing death in albatross, so any deceased Fiordland crested penguins should be examined specifically for this worm to enable evaluation of this potentially damaging parasite in the population.

Gastrointestinal helminths of little blue penguins, Eudyptula novaehollandiae (Stephens), from Otago, New Zealand.

Data regarding helminth communities can provide insights into health, feeding interactions, behaviour and evolution of their host organisms. Penguins (Spheniscidae) are important components of marine food webs and tracking their helminth communities can be indicative of ecosystem health. New Zealand is home to 5 of the world's 19 penguin species and little is known about their gastrointestinal helminths. Here, we provide the first study on the gastrointestinal helminths of little blue penguins from south-eastern South Island, New Zealand. The helminth community consisted of two species of tapeworm; Tetrabothrius lutzi and Tetrabothrius sp.; three nematode species, Contracaecum eudyptulae, Capillaria sp. and Stegophorus macronectes; two acanthocephalans, Andracantha sigma and Bolbosoma balaenae; and one trematode, Galactosomum otepotiense. The most prevalent parasites were T. lutzi, A. sigma, and C. eudyptulae. This work includes three new host records and five new geographic records. This is the first report of B. balaenae occurring in a host other than a marine mammal. This study adds to our knowledge about the helminth community of New Zealand little blue penguins, and includes new genetic data on helminth species, providing a baseline against which future studies may be compared.

The state of fish parasite discovery and taxonomy: a critical assessment and a look forward.

Efforts to find and characterise new parasite species in fish hosts are crucial not just to complete our inventory of Earth's biodiversity, but also to monitor and mitigate disease threats in fisheries and aquaculture in the face of global climate change. Here, we review recent quantitative assessments of research efforts into fish parasite discovery and taxonomy. We address broad questions including: Are efforts aimed at finding new parasite species targeted at geographical hotspots of fish biodiversity, where there should be more parasite species to be found? Is the application of molecular tools to study parasite genetic diversity deployed strategically across regions of the world, or focused disproportionately on certain areas? How well coordinated is the search for new parasite species of fish among workers specialising on different higher helminth taxa? Are parasite discovery efforts in any geographical area consistent over time, or subject to idiosyncrasies due to the waxing and waning of highly prolific research careers? Is the quality of taxonomic descriptions of new species improving over time, with the incorporation of new tools to characterise species? Are taxonomic descriptions moving away from a focus on the adult stage only toward attempts to characterise the full life cycle of newly-discovered helminth species? By using empirical evidence to answer these questions, we assess the current state of research into fish parasite discovery and taxonomy. We also explore the far-reaching implications of recent research on parasite microbiomes for parasite taxonomy. We end with recommendations aimed at maximising the knowledge gained per fish sacrificed, and per dollar and time invested into research on fish parasite biodiversity.