Species of Apatemon Szidat, 1928 and Australapatemon Sudarikov, 1959 (Trematoda: Strigeidae) from New Zealand: Linking and Chara
Total Page:16
File Type:pdf, Size:1020Kb
Parasitol Res (2016) 115:271–289 DOI 10.1007/s00436-015-4744-0 ORIGINAL PAPER Species of Apatemon Szidat, 1928 and Australapatemon Sudarikov, 1959 (Trematoda: Strigeidae) from New Zealand: linking and characterising life cycle stages with morphology and molecules Isabel Blasco-Costa1,2 & Robert Poulin2 & Bronwen Presswell2 Received: 26 August 2015 /Accepted: 4 September 2015 /Published online: 18 September 2015 # Springer-Verlag Berlin Heidelberg 2015 Abstract Species of Apatemon Szidat, 1928 and patterns of host specialisation and distribution, alongside con- Australapatemon Sudarikov, 1959 are reported from New current molecular and morphological evidence would be use- Zealand for the first time, and their life cycles are resolved ful for an integrative taxonomical approach towards the eluci- using molecular sequence data (28S and ITS rDNA regions dation of species diversity in this group. and mitochondrial COI). The metacercaria of Apatemon sp. ‘jamiesoni’ ex Gobiomorphus cotidianus and its cercaria ex Keywords Apatemon . Australapatemon . Strigeidae . Potamopyrgus antipodarum are described in detail. Its adult, Taxonomy . Phylogenetics . Genetic divergence found in Anas platyrhynchos and Phalacrocorax punctatus,is identified by molecular sequence data. Apatemon sp. ‘jamiesoni’ uses a different species of snail host, exhibits con- Introduction sistent differences in the genetic markers examined and its single described adult differs from known species so as to be The Strigeidae Railliet, 1919 is a species-rich family compris- considered distinct, but its formal description awaits addition- ing mainly parasites of birds. The criterion of host specificity al adult specimens. Australapatemon niewiadomski n. sp. is has been utilised as the basis for the systematics of members described from Anas platyrhynchos. It is distinguished mor- of this group on several occasions (Dubois 1938;Sudarikov phologically by the absence of a ringnapf and its overall small- 1959). For instance, two subfamilies are recognised according er size compared to most other Australapatemon spp. except to their host groups (birds or mammals). At a lower taxonomic Au. magnacetabulum and Au. minor, which are smaller in level, Sudarikov (1959) recognised two genera based on dif- nearly all features than the new species. Au. niewiadomski n. ferences observed in the life cycles of several species of sp. metacercaria and its intermediate host (Barbronia weberi) Apatemon Szidat, 1928: Apatemon, with metacercariae are identified via matching of molecular sequence data. The encysting in fish and Australapatemon Sudarikov, 1959,with status of Apatemon and Australapatemon as distinct genera is metacercariae encysting in leeches. Their taxonomic status confirmed based on their respective monophyly, and genetic has been questioned several times: Dubois and Pearson divergence between them is comparable to other well- (1965) reduced Australapatemon to the level of subgenus, established genera in the Strigeidae. The diagnosis of but Yamaguti (1971) restored it to generic level. In the most Australapatemon is emended. Life history data, accurate recent review of the family they were proposed as distinct genera (Niewiadomska 2002), but different authors still seem to hold different opinions (Bell and Sommerville 2002;Bell * Isabel Blasco-Costa et al. 2002). Independent evidence that confirms the validity [email protected] of their status is still lacking. The taxonomic history of species within these genera is 1 Natural History Museum of Geneva, Route de Malagnou 1, also complex. For example, the morphological variability of CH-1211 Geneva 6, Switzerland the type species Apatemon gracilis (Rudolphi, 1819) has been 2 Department of Zoology, University of Otago, PO Box 56, noted repeatedly (Dubois 1938;Stunkardetal.1941; Dubois Dunedin, New Zealand and Rausch 1948; Dubois 1968). Some workers suggested 272 Parasitol Res (2016) 115:271–289 that it be divided into numerous subspecies (Dubois 1953; therefore, a need to establish a phylogenetic context in which Dubois 1968), and yet others, noting that variability can occur to explore the relationships amongst genera and species, and within the same host, preferred to consider A. gracilis as a to aid species delineation for newly collected specimens be- cosmopolitan species with a wide host range and polytypic longing to these genera and more generally to the Strigeidae. morphology (Beverley-Burton 1961). Elucidating the range In this study, we describe morphologically and characterise of variability within this species, or species complex, is con- genetically a new species of Australapatemon based on adults founded by the fact that many studies claiming to refer to and larval stages, and the larval stages and one adult specimen A. gracilis have been found to be referring to other named, of an unnamed Apatemon species. Life cycle stages of these or unnamed species (e.g. Szidat 1929; Stunkard et al. 1941; species are matched using sequence data for three molecular Dubois and Rausch 1948). The distinction between other spe- markers, 28S and ITS rDNA, and mitochondrial COI. Their cies of Apatemon may be questionable, as exemplified by the sequences are analysed together with available sequences of morphometric and molecular synonymisation of A. gracilis strigeid species from GenBank and the phylogenetic analyses and A. annuligerum (von Nordmann, 1832) (Bell and confirm the validity and distinct status of the two genera, Sommerville 2002;Belletal.2002). Likewise, the problem Australapatemon and Apatemon. Furthermore, we present an extends to other strigeid genera and species. Australapatemon amended diagnosis of Australapatemon and explore the pat- burti (Miller, 1923), described originally from North America terns of intraspecific and interspecific genetic divergence in a (now distributed in the Holarctic and Neotropical regions), has number of strigeid genera. been reported several times as A. gracilis (e.g. Stunkard et al. 1941; Dubois and Rausch 1948, 1950; Dubois 1951; Sudarikov 1959; Dubois and Rausch 1960) with a host range Materials and methods that includes at least ten different anatid species (see Dubois 1968; Drago et al. 2007; Hinojosa-Saez et al. 2009; Specimen collection Hernández-Mena et al. 2014). Despite the efforts of multiple researchers over the last century, it seems obvious that our Potamopyrgus antipodarum (Gray) (Gastropoda: Tateidae) understanding of the diversity in this trematode group has were sampled from Lake Waihola and Tomahawk Lagoon in been severely hampered by the intraspecific plasticity and Otago, South Island, New Zealand, using dip nets, at various interspecific/intergeneric homogeneity in morphological fea- times of year between 2011 and 2013. Infected tures. The use of molecular species diagnostics in combination P. antipodarum (freshwater mudsnail) were screened for cer- with detailed morphological examination of specimens (e.g. cariae after incubating them in lake water at 25 °C under Blasco-Costa et al. 2010;Barcaketal.2014; McNamara et al. intense light for 24 h. Cercariae were collected for live obser- 2014) represents the best approach to elucidate the species vation and digital microphotography and fixed with 96 % eth- diversity and assess the extent of morphological plasticity anol for subsequent DNA extraction. Barbronia weberi within these strigeid taxa. (Blanchard) (Hirudinea: Salifidae) were collected by hand Within the Strigeidae, the extent of morphological variabil- from beneath rocks at Lake Hayes in Otago. In the lab, leech ity appears to differ between groups, and molecular studies specimens were pressed between glass slides to confirm infec- designed to examine species delineation have produced a tion and were killed in hot water before dissection and remov- range of results: some molecular studies have upheld the mor- al of metacercarial cysts. Metacercarial cysts and host tissue phologically diagnosed species (Bell et al. 2001), others have were fixed in 96 % ethanol for molecular identification. found new species (Hernández-Mena et al. 2014), and still Gobiomorphus cotidianus McDowall (Actinopterygii: others have found separately described species to be geneti- Eleotridae; common bully) were collected from Lakes cally identical (Bell and Sommerville 2002). It is therefore Waihola and Waipori (Otago) as part of other studies during imperative that morphological studies are supported by mo- 2009–2010. Fish were euthanized by spinal severance and, in lecular evidence when possible. At this stage, although larval some cases, frozen for later dissection. Metacercariae extract- or adult specimens of Apatemon (Bell et al. 2001;Belland ed from the body cavity and mesenteries were fixed in either Sommerville 2002; Moszczynska et al. 2009; Locke et al. 96 % ethanol for molecular analyses or 70 % ethanol for 2010) and Australapatemon (Hernández-Mena et al. 2014) morphological study. have been used in molecular phylogenies at various taxonom- Adult mallard ducks (Anas platyrhynchos L.) were donated ic levels, these specimens were seldom identified to species. by duck hunters from Manuka Island in Clutha River, Mount Furthermore, sequence data exist for the 28S ribosomal DNA Watkin and Karitane Estuary, South Island (New Zealand), (rDNA) region, the internal transcribed spacers (ITS) of the during the official hunting season (May to July 2013), shot ribosomal gene or the mitochondrial cytochrome c oxidase under licence in accordance with the Fish and Game New subunit