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 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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Morphological and molecular characterisation of a new genus and species of acanthocephalan, Tenuisoma tarapungi n. g., n. sp. (Acanthocephala: Polymorphidae) infecting red-billed gulls in New Zealand, with a key to the genera of the Polymorphidae Meyer, 1931.

Acanthocephalans of the family Polymorphidae Meyer, 1931 are cosmopolitan parasites that infect the intestines of fish-eating birds and mammals. Polymorphid acanthocephalans recovered from the intestines of red-billed gulls (Chroicocephalus scopulinus (Forster)) from the Otago coast, New Zealand, although morphologically similar to the genus Arhythmorhynchus Lühe, 1911 nevertheless have a unique molecular profile showing considerable genetic differentation, and are here diagnosed and described as Tenuisoma tarapungi n. g., n. sp. Characters which distinguish T. tarapungi include a very elongate, cylindrical hindtrunk, swollen anterior trunk with a spinose region, a secondary swelling in males only containing the testes, and hypodermal nuclei distributed throughout the length of the trunk. Molecular data (cox1, 18S, 28S) confirm that the representative of the new genus is closest to, but nonetheless strongly divergent from species of Pseudocorynosoma Aznar, Pérez-Ponce de León & Raga, 2006. Immature specimens are described and illustrated, demonstrating the extreme degree of hindtrunk inversion occurring in immature individuals of this species. We provide a key to the genera of the family Polymorphidae.

Parasitological research in the molecular age.

New technological methods, such as rapidly developing molecular approaches, often provide new tools for scientific advances. However, these new tools are often not utilized equally across different research areas, possibly leading to disparities in progress between these areas. Here, we use empirical evidence from the scientific literature to test for potential discrepancies in the use of genetic tools to study parasitic vs non-parasitic organisms across three distinguishable molecular periods, the allozyme, nucleotide and genomics periods. Publications on parasites constitute only a fraction (<5%) of the total research output across all molecular periods and are dominated by medically relevant parasites (especially protists), particularly during the early phase of each period. Our analysis suggests an increasing complexity of topics and research questions being addressed with the development of more sophisticated molecular tools, with the research focus between the periods shifting from predominantly species discovery to broader theory-focused questions. We conclude that both new and older molecular methods offer powerful tools for research on parasites, including their diverse roles in ecosystems and their relevance as human pathogens. While older methods, such as barcoding approaches, will continue to feature in the molecular toolbox of parasitologists for years to come, we encourage parasitologists to be more responsive to new approaches that provide the tools to address broader questions.

Morphology and molecules resolve the identity and life cycle of an eye trematode, Philophthalmus attenuatus n. sp. (Trematoda: Philophthalmidae) infecting gulls in New Zealand.

Trematodes of the genus Philophthalmus are cosmopolitan parasites that infect the eyes of birds and mammals. They have the potential to affect the survival of their hosts and a few cases of human philophthalmiasis have occurred worldwide. Adults of known Philophthalmus species have never been recorded from bird hosts in New Zealand, despite their cercarial stage being a focus of various studies. Here, we describe a new species of Philophthalmus infecting New Zealand red-billed and black-backed gulls, Philophthalmus attenuatus n. sp. It is distinguished from other marine species of Philophthalmus by its long, thin body shape, consistently longer vitelline field on the left, and its body reflexed at the ventral sucker. We use molecular methods to complete the life cycle of this species, matching it with the larval stage infecting the mud whelk, Zeacumantus subcarinatus, and present a preliminary cox1 phylogeny. In addition, we comment on the validity of some taxonomic characters used to differentiate species of this genus, discuss potential colonisation routes to New Zealand and comment on the potential for zoonotic infection.

The invasive cestode parasite Ligula from salmonids and bullies on the South Island, New Zealand.

Freshwater ecosystems are often impacted by biological invasions, including the introduction of exotic parasites capable of infecting native species. Here, we report the occurrence of the introduced tapeworm Ligula sp. from common bully, Gobiomorphus cotidianus, and quinnat salmon, Oncorhynchus tshawytscha, in Lake Hawea, South Island, New Zealand. This parasite has a complex life cycle, reaching its adult stage in fish-eating birds. Worms recovered from the body cavity of fish hosts reached huge sizes (60-300 mm long); however, their low prevalence in fish populations suggests that infections are rare or localised. Molecular analysis (internal transcribed spacer (ITS)1 and ITS2 sequences) confirms that these specimens belong to the genus Ligula and suggests tentative routes of invasion into New Zealand. Monitoring the spread of this parasite is important, as it can impact fish populations and also, when infection levels are high, those of piscivorous birds.

Taxonomic Quality of Species Descriptions Varies over Time and with the Number of Authors, but Unevenly among Parasitic Taxa.

Although concerns are being raised about a potential shortage of taxonomists and systematists, recent analyses suggest instead that the number of researchers involved in taxonomic descriptions is higher than ever and that the average number of new species described annually per taxonomist has declined in recent decades. Here, using nine metrics of taxonomic quality, such as the number of morphological traits measured, the number of separate line drawings included, and whether or not gene sequences are provided, we explore variation in taxonomic quality as a function of the number of authors and other potential determinants across 2366 descriptions of parasitic helminths published in 1337 articles between 1980 and 2014. Taxonomic quality has generally increased over time, but unequally among different groups of helminths. For example, the number of scanning electron micrographs per description has risen significantly over time in cestodes and nematodes, but decreased for digeneans. For most metrics used, the greater the number of authors per species description, the higher its quality, suggesting not more taxonomists but more collaborations between taxonomists and experts from other fields to produce more comprehensive species characterizations. Re-descriptions of species were of higher quality than their original descriptions, and the improved quality correlated with the number of years elapsed between them. However, the extent of this improvement varied among helminth species with different host taxa. Overall, our findings provide a note of caution for anyone using trends in the number of species described per author to extrapolate the total number of extant species. They also reveal cultural differences among taxonomists working on different groups of parasites that can serve to identify areas for potential improvement. [Biodiversity; Cestoda; Digenea; integrative taxonomy; Nematoda.].

Behavioural modification of personality traits: testing the effect of a trematode on nymphs of the red damselfly Xanthocnemis zealandica.

Research on animal personality is increasingly demonstrating that individuals in a population are characterised by distinct sets of behavioural traits that show consistency over time and across different situations. Parasites are known to alter the behaviour of their hosts, although their role in shaping host personality remains little studied. Here, we test the effect of trematode infection on two traits of their host's personality, activity and boldness, in nymphs of the red damselfly Xanthocnemis zealandica. Genetic analyses indicate that the undescribed trematode species falls within the superfamily Microphalloidea. Results of laboratory behavioural tests indicate that the two behavioural traits are related to each other: bolder individuals also show higher levels of spontaneous activity than shy ones. However, parasite infection had no effect on either of these behaviours or on their repeatability over three separate testing sessions. Although our findings suggest that this trematode does not influence personality traits of the damselfly host, it remains possible that other standard personality traits not tested here (exploratory tendency, aggressiveness) are affected by infection.

Species of Apatemon Szidat, 1928 and Australapatemon Sudarikov, 1959 (Trematoda: Strigeidae) from New Zealand: linking and characterising life cycle stages with morphology and molecules.

Species of Apatemon Szidat, 1928 and Australapatemon Sudarikov, 1959 are reported from New Zealand for the first time, and their life cycles are resolved using molecular sequence data (28S and ITS rDNA regions and mitochondrial COI). The metacercaria of Apatemon sp. 'jamiesoni' ex Gobiomorphus cotidianus and its cercaria ex Potamopyrgus antipodarum are described in detail. Its adult, found in Anas platyrhynchos and Phalacrocorax punctatus, is identified by molecular sequence data. Apatemon sp. 'jamiesoni' uses a different species of snail host, exhibits consistent differences in the genetic markers examined and its single described adult differs from known species so as to be considered distinct, but its formal description awaits additional adult specimens. Australapatemon niewiadomski n. sp. is described from Anas platyrhynchos. It is distinguished morphologically by the absence of a ringnapf and its overall smaller size compared to most other Australapatemon spp. except Au. magnacetabulum and Au. minor, which are smaller in nearly all features than the new species. Au. niewiadomski n. sp. metacercaria and its intermediate host (Barbronia weberi) are identified via matching of molecular sequence data. The status of Apatemon and Australapatemon as distinct genera is confirmed based on their respective monophyly, and genetic divergence between them is comparable to other well-established genera in the Strigeidae. The diagnosis of Australapatemon is emended. Life history data, accurate patterns of host specialisation and distribution, alongside concurrent molecular and morphological evidence would be useful for an integrative taxonomical approach towards the elucidation of species diversity in this group.

Two new species of Maritrema Nicoll, 1907 (Digenea: Microphallidae) from New Zealand: morphological and molecular characterisation.

Two new species of the microphallid genus Maritrema (Maritrema) Nicoll, 1907 are described from freshwaters in the South Island of New Zealand. Maritrema deblocki n. sp. occurs as an adult in the mallard Anas platyrhynchos (L.); Maritrema poulini n. sp. is found as sporocysts/cercariae in Potamopyrgus antipodarum (Gray) and as metacercariae in two species of amphipod and two species of isopod. We use morphological and molecular characterisation to distinguish between the two species, and compare them to their four morphologically closest congeners. M. deblocki n. sp. and M. poulini n. sp. are distinguished from each other by the relative sucker size, the positions of the genital pore and ovary, the convergence of the vitelline ribbons, and overall size. With the aid of molecular data, we matched life cycle stages of M. poulini n. sp. and assessed its use of multiple second intermediate hosts. Phylogenetic analyses included sequences for the two new species and the available microphallid sequences for the large ribosomal subunit and the internal transcribed spacer 1 of the ribosomal RNA gene. Closer to each other than to any other species, the sister species together with Maritrema novaezealandense Martorelli, Fredensborg, Mouritsen & Poulin, 2004, Maritrema heardi (Kinsella & Deblock, 1994), Maritrema eroliae Yamaguti, 1939 and Maritrema oocysta (Lebour, 1907) formed a well-supported clade. In addition, we clarify the taxonomic identity of several unidentified Microphallus spp. in the recent ecological literature from New Zealand and propose corrected spellings for a number of Maritrema species epithets.