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. 2024 Nov 15;110(6):590–606. doi: 10.1645/24-33

PHYLOGENY AND SYSTEMATICS OF CYATHOCOTYLID DIGENEANS (DIGENEA: DIPLOSTOMOIDEA) PARASITIZING SNAKES WITH DESCRIPTION OF THREE NEW SPECIES OF GOGATEA FROM AUSTRALIA AND VIETNAM

Tyler J Achatz 1, Zoe S Von Holten 1, Tran Thi Binh 2, Vasyl V Tkach 3,✉
PMCID: PMC12175293  PMID: 39551077

Abstract

The Cyathocotylidae Mühling, 1896 is a small but broadly distributed family of digeneans parasitic in a wide range of vertebrate definitive hosts, from fish to mammals. Despite existing taxonomic questions, only a few studies have generated DNA sequence data from cyathocotylids, and only a single publication included sequence data from a cyathocotylid parasitic in snakes. Four genera are known to infect snakes: Gogatea Lutz, 1935, Szidatia Dubois, 1938, Mesostephanoides Dubois, 1951, and Serpentostephanus Sudarikov, 1961. Members of these genera were known from only Asia and Africa. In the present study, we describe 2 new species of Gogatea from snakes in Australia and 1 from Vietnam. The new species from Vietnam described herein is the first member of the genus that lacks a ventral sucker. We used partial sequences of the nuclear large ribosomal subunit (28S) and mitochondrial cytochrome c oxidase subunit I (COI) genes to explore phylogenetic relationships among cyathocotylids and species differentiation. In addition, this is the first report of a cyathocotylid from snakes in Australia, thus posing interesting questions regarding the dispersal and historical biogeography of these parasites. Cyathocotylid genera from snakes have a long, convoluted taxonomic history. The genera Gogatea, Mesostephanoides, and Szidatia were distinguished from each other based on very small morphological differences. Therefore, the validity of Szidatia and Mesostephanoides was often questioned in the literature. Based on the detailed morphological analysis of our freshly collected high-quality specimens and comparison with published information, we synonymize Mesostephanoides and Szidatia with Gogatea.

Keywords: Cyathocotylidae, Gogatea, Szidatia, Acrochordus, Fowlea, Snakes, Australia, Vietnam, Molecular phylogeny

The Cyathocotylidae Mühling, 1896 is a small but broadly distributed family of digeneans parasitic in a wide range of vertebrate definitive hosts, including fishes, reptiles, birds, and mammals. Members of 4 cyathocotylid genera are known to infect snakes: Gogatea Lutz, 1935, Szidatia Dubois, 1938, Mesostephanoides Dubois, 1951, and Serpentostephanus Sudarikov, 1961. These genera from snakes have a long, convoluted taxonomic history, with genera Gogatea, Mesostephanoides, and Szidatia distinguished from each other based on very small morphological differences. Therefore, the validity of Szidatia and Mesostephanoides was often questioned in the literature (Chatterji, 1940; Mehra, 1947; Dwivedi and Chauhan, 1969; Curran et al., 2001). Until now, cyathocotylids were known from snakes in only Asia and Africa. In the present study, we describe 2 new species of Gogatea from snakes in Australia and 1 from Vietnam. We generated partial sequences of the large ribosomal subunit (28S) rRNA and cytochrome c oxidase subunit I (COI) mtDNA genes as well as the internal transcribed spacer regions (ITS1 + 5.8S + ITS2) rDNA for all 3 species. Additional COI sequences were generated from various cyathocotylids previously sequenced for 28S by Achatz et al. (2019), including Gogatea mehri Mehra, 1947 and a Gogatea sp. from Thailand. The 28S sequence data were used to test the monophyly of Gogatea spp. and examine their relationships with other cyathocotylids. The COI sequences of Gogatea spp. were used as a helpful tool for species differentiation but were not the sole criteria. Newly generated COI sequences of other cyathocotylids are provided for future comparisons.

MATERIALS AND METHODS

Multiple adult specimens of Gogatea spp. were collected from the intestines of Arafura file snake Acrochordus arafurae McDowell in the Northern Territory and Queensland, Australia, and checkered keelback Fowlea piscator (Schneider) in Vietnam (Table I). Gogatea specimens were stained with aqueous alum carmine and mounted on slides following the protocol of Lutz et al. (2017). The morphology of the digeneans was studied with a BX53 compound microscope (Olympus, Tokyo, Japan) equipped with differential interference contrast optics and a digital imaging system. Illustrations were prepared with the aid of a drawing tube mounted on a DM 5500 (Leica, Deerfield, Illinois) compound microscope equipped with differential interference contrast. All measurements are provided in micrometers. Type series are deposited in the collection of the H. W. Manter Laboratory (HWML), University of Nebraska, Lincoln, Nebraska (Table I).

Table I.

Hosts, geographical origin, GenBank accession numbers, and H. W. Manter Laboratory (HWML) accession numbers of cyathocotylids described and species of Achatz et al. (2019) that were sequenced in this study.

Cyathocotylid species Host species Country HWML no(s). Accession nos.
28S COI
Cyathocotyle bushiensis Aythya affinis United States 139967 MK650440 PP991441*
Gogatea acrochordi n. sp. Acrochordus arafurae Australia 217835–217836* PP992053–PP992057†, PP992067* PP991442–PP9914426*
Gogatea anacetabulata n. sp. Fowlea piscator Vietnam 217831–217832* PP992058†, PP992059† PP991447*, PP9914478*
Gogatea bijirrii n. sp. Acrochordus arafurae Australia 217833–217834* PP992060–PP992063† PP991449–PP991452*
Gogatea mehri Xenochrophis flavipunctatus Vietnam 217837* MK650441, PP992064†, PP992065† PP991453*, PP991454*
Gogatea sp. Acrochordus javanicus Thailand 217838* MK650442, PP992066† PP991455*
Holostephanoides ictaluri Ameiurus sp. United States 217839* MK650443 PP991456*
Holostephanus dubinini Phalacrocorax carbo Ukraine 139968 MK650444 PP991457*
Mesostephanus cubaensis Morus bassanus United States 139969 MK650445 PP991458*
Neogogatea sp. Lophodytes cucullatus United States 139971 MK650447−MK650449 PP991459*, PP991460*
Suchocyathocotyle crocodili Crocodylus johnstoni Australia 139972 MK650450, MK650451 PP991461*, PP991462*
Suchocyathocotyle fraterna Crocodylus niloticus South Africa 139373 MK650452 PP991463*
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*

New sequences and slides.

†

New sequences that include the ITS region.

Specimens used for scanning electron microscopy were dehydrated in a graded series of ethanol, dehydrated in mixtures of 100% ethanol and hexamethyldisilazane (HMDS) followed by pure HMDS, dried and mounted on conductive double-sided carbon tape on aluminum scanning electron microscope (SEM) stubs, coated with gold-palladium in a sputter coater, and examined under a Hitachi 4700 SEM (Hitachi Ltd., Tokyo, Japan).

DNA extraction, amplification, and sequencing of partial 28S and COI genes were performed as previously described by Achatz et al. (2019, 2023b). The ITS region was amplified and sequenced as previously described by Achatz et al. (2022). We also generated COI sequences from cyathocotylid isolates previously sequenced for 28S by Achatz et al. (2019). Contiguous sequences were assembled in Sequencher version 4.2 software (GeneCodes Corp., Ann Arbor, Michigan) and deposited in GenBank (Table I).

The phylogenetic analysis of the 28S gene was based on an alignment that included 3 newly generated sequences from Gogatea spp., and 23 previously published sequences from cyathocotylids. Harmotrema laticaudae Yamaguti, 1933 was used as the outgroup based on the study by Pérez-Ponce de León and Hernández-Mena (2019). Sequences were aligned in MEGA7 using ClustalW (Kumar et al., 2016). The alignment was trimmed to the length of the shortest sequence, and ambiguous positions were excluded from the analyses. The general time-reversible model with estimates of invariant sites and gamma-distributed among-site variation (GTR + G + I) was determined as the best-fitting model of nucleotide substitution using MEGA7 (Kumar et al., 2016). The phylogenetic analysis was conducted using Bayesian inference as implemented in MrBayes version 3.2.6 software (Ronquist and Huelsenbeck, 2003); the analysis conditions were identical to those used by Achatz et al. (2023b). Pairwise comparisons were performed using MEGA7.

RESULTS

Molecular phylogenies

The 28S alignment was 1,111 bp long after trimming to the length of the shortest sequence; 36 nucleotide positions were excluded due to ambiguous homology. Suchocyathocotyle spp. appeared as a 100% supported sister group to the 100% supported clade of all other cyathocotylids (Fig. 1), which in turn formed 2 strongly supported clades. The first clade (100% supported) included Braunina sp. + an 83% supported subclade (unidentified cyathocotylid + Mesostephanus spp.; 100% supported). The second clade (98% supported) contained 2 subclades indicated as subclades A and B in Figure 1. Subclade A (99% supported) contained an 87% supported grouping of Holostephanoides ictaluri Vernberg, 1952 + Neogogatea sp. of Achatz et al. (2019) and a 100% grouping of Gogatea spp. Within the Gogatea subclade, Gogatea sp. from Thailand formed a weakly supported cluster with a 100% supported clade of Gogatea acrochordi n. sp. + Gogatea bijirrii n. sp., while G. mehri and Gogatea anacetabulata n. sp. formed a weakly (84%) supported clade, positioned as a sister group to the 3 remaining Gogatea spp. (Fig. 1). Subclade B (100% supported) contained 5 Cyathocotyle sp. sequences, which were non-monophyletic due to the inclusion of Holostephanus dubinini Vojtek and Vojtkova, 1968, and an unidentified Cyathocotylidae sp.

Figure 1.

Figure 1.

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Phylogenetic interrelationships among 26 cyathocotylids based on Bayesian inference analysis of partial 28S rDNA sequences. Bayesian inference posterior probability values lower than 80% are not shown. The new sequences generated in this study are indicated in bold. The scale bar indicates the number of substitutions per site. GenBank accession numbers are provided after the names of taxa.

DESCRIPTIONS

Genus Gogatea Lutz, 1935

The new species described herein expand the morphological features used in the most recent generic diagnosis of Gogatea by Niewiadomska (2002). Below is an amended diagnosis for the genus.

Diagnosis:

Cyathocotylidae. Body bipartite, may be distinct or somewhat indistinct; prosoma flattened with slight ventral concavity; opisthosoma much shorter, cylindrical. Tegument armed. Oral sucker larger than ventral sucker. Ventral sucker in adult digeneans typically present, rarely absent. Pseudosuckers absent. Holdfast organ rounded, with slit-like median opening, immediately posterior to ventral sucker when present. Pharynx smaller than oral sucker. Ceca may reach anterior margin of opisthosoma or extend posterior to testes. Testes 2, rounded, tandem. Anterior testis positioned in prosoma or opisthosoma; posterior testis positioned in opisthosoma, rarely in prosoma. Cirrus sac well developed, variable in length. Ovary intertesticular or opposite to anterior testis. Oötype intertesticular. Vitelline follicles large, situated around or dorsal to holdfast organ in 2 lateral elongated fields, which may be confluent anteriorly forming a horseshoe-like shape or be confluent throughout their length. Vitelline reservoir intertesticular. Genital pore slightly subterminal on dorsal side. Excretory pore not observed. In snakes. Australasia, Indomalaya, Palearctic (northern Africa).

Type species:

Gogatea serpentum (Gogate, 1932).

Other species:

Gogatea acrochordi n. sp. Achatz, Von Holten and Tkach, Gogatea anacetabulata n. sp. Achatz, Von Holten and Tkach, Gogatea bijirrii n. sp. Achatz, Von Holten and Tkach, Gogatea joyeuxi (Hughes, 1929) n. comb., Gogatea karachiensis Farooq, 1973, Gogatea mehri Mehra, 1947, Gogatea taiwanensis (Fischthal and Kuntz, 1975) n. comb.

Gogatea bijirrii n. sp. Achatz, Von Holten and Tkach (Figs. 2–19)

Figures 2–7.

Figures 2–7.

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Gogatea bijirrii n. sp. (2) Holotype, entire, ventral view. (3) Holotype, ventral view of posterior portion of opisthosoma with male reproductive system omitted (testes shown as outline). (4) Ventral view of posterior portion of opisthosoma with female reproductive system omitted (ovary shown as outline). (5, 6) Arrangement of vitelline follicles in holotype and a paratype, respectively. (7) Paratype, entire, ventral view with ceca, cirrus sac, and uterus omitted. Abbreviations: C, ceca; CS, cirrus sac; E, egg; GA, genital atrium; M, metraterm; O, ovary; T, testis; U, uterus; VR, vitelline reservoir.

Figures 13–19.

Figures 13–19.

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Scanning electron micrographs of Gogatea bijirrii n. sp. (13) Entire, ventral view. (14) Ventral view of anterior portion of prosoma. (15) Ventral view of ventral sucker and holdfast organ. (16) Ventral sucker region. (17) Palm-like spines with 4 or 5 sharply pointed digitiform processes at mid-distance between oral and ventral suckers. (18) Spines with 2 digitiform processes at level of ventral sucker. (19) Simple spines posterior to ventral sucker.

Description (based on 22 adult specimens):

Measurements of holotype in text (all measurements in micrometers); measurements of entire series given in Table II. Body 1,491 long, consisting of weakly separated prosoma and opisthosoma; prosoma oval, anterior margin concave, 926 long, usually widest at a point between level of holdfast organ and pharynx, 409; opisthosoma elongated, cylindrical, 565 × 313. Prosoma:opisthosoma length ratio 1.6. Forebody 52% of body length. Tegument of prosoma armed with spines. Spines between anterior end of body and approximately level of anterior margin of ventral sucker have 4–6 thin, sharply pointed digitiform protrusions; spines at level of ventral sucker and holdfast organ usually have 2 digitiform protrusions; posterior-most spines posterior to holdfast organ mostly simple, sharply pointed (Figs. 13–19). Oral sucker antero-ventral, 161 × 160. Ventral sucker 61 × 60. Oral sucker:ventral sucker width ratio 2.7. Pseudosuckers absent. Holdfast organ oval, with longitudinal opening, 206 × 109. Prepharynx absent. Pharynx subspherical, 64 × 52. Esophagus 172 long. Cecal bifurcation in anterior 25% of prosoma length. Ceca slender, extend to posterior margin of prosoma.

Table II.

Morphometric characters of the new Gogatea spp. Ranges provided followed by mean in parentheses.

Species
 Gogatea bijirrii n. sp.
 Gogatea acrochordi n. sp.
 Gogatea anacetabulata n. sp.
Host
 Acrochordus arafurae
Fowlea piscator
Locality Northern Territory, Australia Queensland, Australia Vietnam
No. of specimens 22 6 29
Body length (μm) 984–1,857 (1,502) 1,072–1,356 (1,233) 1,272–1,791 (1,545)
Prosoma length (μm) 698–1,744 (1,112) 782–990 (904) 994–1,509 (1,208)
Prosoma width (μm) 295–591 (422) 324–405 (356) 503–712 (597)
Opisthosoma length (μm) 278–687 (448) 290–408 (329) 208–475 (325)
Opisthosoma width (μm) 197–403 (277) 196–300 (240) 226–452 (320)
Prosoma:opisthosoma length ratio 1.6–3.6 (2.5) 2.2–3.4 (2.8) 2.3–7.3 (3.9)
Forebody (as % of body length) 39–62 (49) 45–54 (48)
Oral sucker length (μm) 128–220 (151) 132–157 (144) 92–136 (117)
Oral sucker width (μm) 142–185 (163) 133–161 (153) 110–147 (124)
Ventral sucker length (μm) 42–69 (54) 41–52 (48)
Ventral sucker width (μm) 36–71 (56) 43–57 (51)
Oral sucker:ventral sucker width ratio 2.4–4.2 (3.0) 2.6–3.6 (3.0)
Holdfast organ length (μm) 160–294 (238) 204–237 (218) 145–440 (331)
Holdfast organ width (μm) 79–154 (113) 90–273 (191) 125–453 (262)
Pharynx length (μm) 50–75 (65) 40–58 (49) 41–66 (56)
Pharynx width (μm) 52–76 (61) 46–56 (51) 50–68 (58)
Esophagus length (μm) 91–198 (142) 111–161 (135) 157–297 (205)
Anterior testis length (μm) 103–239 (176) 103–170 (145) 115–224 (162)
Anterior testis width (μm) 120–196 (158) 102–113 (109) 110–204 (159)
Posterior testis length (μm) 105–218 (171) 73–163 (126) 111–212 (161)
Posterior testis width (μm) 120–275 (168) 67–141 (115) 108–202 (160)
Cirrus sac length (μm) 297–511 (418) 402–508 (454) 502–849 (680)
Cirrus sac width (μm) 31–60 (47) 37–42 (40) 43–74 (57)
Cirrus sac length (as % of body length) 23–31 (28) 35–39 (37) 32–55 (42)
Ovary length (μm) 49–104 (75) 49–67 (56) 71–130 (91)
Ovary width (μm) 46–90 (65) 42–51 (49) 64–116 (87)
Number of eggs 0–3 (1) 0–1 (1) 1–6 (2)
Egg length (μm) 115–153 (132) 125–141 (134) 115–188 (157)
Egg width (μm) 81–101 (92) 87–96 (92) 68–110 (88)
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Testes 2, tandem, rounded, entire. Anterior testis 212 × 162; posterior testis 153 × 131. Short intertesticular space may be present, or posterior margin of anterior testis may be ventral to part of posterior testis. Cirrus sac extends to level of or slightly anterior to anterior testis, containing seminal vesicle and cirrus, 439 × 59, occupies 29% of body length. Genital pore slightly subterminal, dorsal.

Ovary subspherical, 77 × 51; its position varies from opposite to anterior margin of anterior testis to intertesticular. Oötype and Mehlis’ gland intertesticular.

Vitelline follicles large, distributed in 2 lateral elongated fields extending from level of ventral sucker to near prosoma–opisthosoma junction; vitelline follicle fields confluent or nearly confluent throughout their length on dorsal side and near anterior margin of holdfast organ only on ventral side. Vitelline reservoir primarily intertesticular, elongated, large. Uterus ventral to gonads, extends anteriorly beyond level of ovary before turning and extending posteriorly as metraterm, opening into genital atrium. Uterus contains 3 eggs in holotype and up to 3 eggs in paratypes. Eggs 115–153 × 81–101. Excretory pore not observed.

Taxonomic summary

Type host:

Acrochordus arafurae McDowell (Squamata: Serpentes).

Site of infection:

Small intestine.

Type locality:

Northern Territory, Australia; 12°33′28.7″S, 131°17′47.1″E.

Type material:

Holotype: HWML 217833, ex. Acrochordus arafurae, small intestine, Fogg Dam, Northern Territory, Australia, 10 June 2008, coll. V. Tkach. Paratypes: HWML 217834 (29 specimens on 11 slides), labeled identical to the holotype.

Representative DNA sequences:

ITS region +28S: PP992060; COI: PP991449.

ZooBank registration:

urn:lsid:zoobank.org:act:AFC907BC-5E2D-4E78-9A21-F974CCED5413.

Etymology:

The specific epithet refers to the word for file snake in 1 of the indigenous Australian languages, Alawa, spoken by the Alawa people in the Northern Territory.

Remarks

This new species belongs to Gogatea based on a combination of several features, including the presence of a cirrus sac and holdfast organ, the elongated opisthosoma, and the horseshoe-like arrangement of the vitellarium in the holdfast organ area. The phylogenetic analysis (Fig. 1) also positioned the species within a 100% supported clade that contained congeners, including G. mehri.

Gogatea bijirrii is distinguishable from its congeners based on its weakly distinct or indistinct separation of prosoma and opisthosoma (vs. more distinct in all other species, based on written descriptions) and a generally longer esophagus compared with other species of similar body size (esophagus length of 91–198 in G. bijirrii vs. 36–106 in G. serpentum, G. mehri, and G. joyeuxi (Hughes, 1929) n. comb.; see discussion below).

The new species can be further separated from G. serpentum based on the anterior extent of the cirrus sac, which is positioned at a level near the anterior margin of anterior testis in the new species vs. between levels of the posterior margin of the posterior testis and ovary in G. serpentum. The new species also has a larger oral sucker (128–220 × 142–185) than does G. serpentum (103–126 × 64–80). Based on the measurements in the original description (which did not show the ventral sucker on the drawing) and the re-description by Mehra (1947), the 2 species also differ in the sucker ratio. In the new species, the oral:ventral sucker width ratio is 2.4–4.2 (average, 3.0), whereas in G. serpentum this ratio does not exceed 2.0.

Gogatea bijirrii is morphologically similar to G. mehri, although the oral sucker in these species differ in size (128–220 × 142–185 in G. bijirrii vs. 105–117 × 120–138 in G. mehri). Despite the morphological similarity, these species differ by 3.7% in 28S and 17.4% in COI (Table III).

Table III.

Divergence percentages among Gogatea spp. resulting from pairwise sequence comparisons of 431 bp long alignment of the partial COI gene (above diagonal), 1,259 bp long alignment of the partial 28S gene (below diagonal, before slash), and 1,205 bp long alignment of the ITS region (below diagonal, after slash). GenBank numbers for the COI sequences are provided in the top row. GenBank numbers for contiguous ITS region + partial 28S ribosomal sequences are provided in the first column.

 1. 2. 3. 4. 5. 6. 7.
Gogatea species PP991450 PP991442 PP991443 PP991444 PP991455 PP991453 PP991447
1. G. bijirrii n. sp. PP992061 — 5.3 5.3 5.1 14.8 17.4 15.3
2. G. acrochordi n. sp. PP992054 0.0/0.0 — 0.5 0.2 12.8 17.4 13.2
3. G. acrochordi PP992055 0.0/0.0 0.0/0.0 — 0.2 12.8 17.2 12.8
4. G. acrochordi PP992056 0.0/0.0 0.0/0.0 0.0/0.0 — 12.5 17.4 13.0
5. Gogatea sp. PP992066 2.2/38.3 2.2/38.3 2.2/38.3 2.2/38.3 — 17.6 13.0
6. G. mehri PP992064 3.7/6.8 3.7/6.8 3.7/6.8 3.7/6.8 2.9/35.3 — 15.5
7. G. anacetabulata n. sp. PP992058 2.9/5.7 2.9/5.7 2.9/5.7 2.9/5.7 2.9/40.7 3.6/7.7 —
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This new species and G. karachiensis most obviously differ in body shape (elongated in G. bijirrii vs. oval in G. karachiensis). The holdfast organ of G. karachiensis is large (420 × 400), occupying more than a third of the body length. In contrast, the holdfast organ of the new species is smaller (160–294 × 79–154), occupying less than a sixth of the body length. These species can be further differentiated based on oral sucker size (128–220 × 142–185 in G. bijirrii vs. 100 × 110 in G. karachiensis), ventral sucker size (36–69 × 36–71 in the new species vs. 70 × 60 in G. karachiensis), and pharynx size (50–75 in the new species vs. 30 in G. karachiensis).

Gogatea bijirrii and G. taiwanensis (Fischthal and Kuntz, 1975) n. comb. (= Szidatia taiwanensis (Fischthal and Kuntz, 1975); see discussion below) differ in prosoma shape (elongated prosoma in G. bijirrii vs. pyriform in G. taiwanensis). The ceca of the new species bifurcate in the anterior quarter of the prosoma, whereas those in G. taiwanensis bifurcate within the anterior third of the prosoma. The oral sucker of the new species (128–220 × 142–185) is generally larger than that of G. taiwanensis (90–119 × 99–144), whereas the ventral sucker is generally smaller in G. bijirrii (42–69 × 36–71) than in G. taiwanensis (62–95 × 85–112).

The new species and G. joyeuxi can be differentiated based on the anterior extent of cirrus sac (positioned at a level near the anterior margin of anterior testis in the new species vs. does not extend anterior to the level of posterior testis in G. joyeuxi). In the new species, the oral sucker (128–220 × 142–185) is much larger than the ventral sucker (42–69 × 36–71), whereas in G. joyeuxi the oral sucker (73–100 diameter) is similar in size or slightly larger than the ventral sucker (65–70 diameter).

Besides its congener from Australia described in the present work (see differentiation below), G. bijirrii differs from other Gogatea spp. sequenced so far by 2.2–3.7% in partial sequences of 28S, 5.7–38.3% in the ITS region, and 14.8–17.4% in COI (Table III). Gogatea sp. has a 375 bp long deletion in ITS1, which substantially increases the intrageneric variation. In addition, G. bijirrii is distributed in Australia and is parasitic in the Arafura file snake endemic to Australia and New Guinea.

No intraspecific variation was detected among 4 isolates sequenced for 28S and 4 isolates sequenced for the ITS region; no more than 0.2% variation was detected in the COI of 4 sequenced isolates.

Gogatea acrochordi n. sp. Achatz, Von Holten and Tkach (Figs. 20–25)

Figures 20–25.

Figures 20–25.

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Gogatea acrochordi n. sp. (20) Holotype, entire, ventral view. (21) Holotype, ventral view of posterior portion of opisthosoma with female reproductive system omitted. (22) Paratype, ventral view of posterior portion of opisthosoma with male reproductive system omitted. (23, 24) Arrangement of vitelline follicles in holotype and a paratype, respectively. (25) Paratype, entire, ventral view. Abbreviations: C, ceca; CS, cirrus sac; E, egg; GA, genital atrium; M, metraterm; O, ovary; T, testis; U, uterus; VR, vitelline reservoir.

Description (based on 6 adult specimens): Measurements of holotype in text (all measurements in micrometers); measurements of entire series given in Table II. Body 1,315 long, consisting of weakly separated prosoma and opisthosoma; prosoma oval, anterior margin concave, 907 long, usually widest at a point between level of holdfast organ and pharynx, 405; opisthosoma elongated, cylindrical, 408 × 300. Prosoma:opisthosoma length ratio 2.2. Forebody 46% of body length. Tegument of prosoma armed with spines. Oral sucker antero-ventral, 150 × 157. Ventral sucker 50 × 57. Oral sucker:ventral sucker width ratio 2.8. Pseudosuckers absent. Holdfast organ oval, with longitudinal opening, 237 × 273. Prepharynx absent. Pharynx subspherical, 50 × 51. Esophagus 161 long. Cecal bifurcation in anterior 35% of prosoma length. Ceca slender, extend to posterior margin of prosoma.

Testes 2, tandem, rounded, entire. Anterior testis 187 × 138; posterior testis 73 × 67. Short intertesticular space may be present, or posterior margin of anterior testis may be ventral to part of posterior testis. Cirrus sac extends to level of or slightly anterior to anterior testis, containing seminal vesicle and cirrus, 508 × 42, occupies 38% of body length. Genital pore slightly subterminal, dorsal.

Ovary subspherical, 75 × 66; opposite to anterior testis. Oötype and Mehlis’ gland intertesticular. Vitelline follicles large, distributed in 2 lateral elongated fields extending from level of ventral sucker to near prosoma–opisthosoma junction; vitelline follicle fields confluent or nearly confluent throughout their length on dorsal side and near anterior margin of holdfast organ only on ventral side. Vitelline reservoir primarily intertesticular, large. Uterus ventral to gonads, extends anteriorly beyond level of ovary before turning and extending posteriorly as metraterm, opening into genital atrium. Uterus contains 1 egg in holotype and no eggs in paratypes. Eggs 125–141 × 87–96. Excretory pore not observed.

Taxonomic summary

Type host:

Acrochordus arafurae McDowell (Squamata: Serpentes).

Site of infection:

Small intestine.

Type locality:

Leichardt Lagoon, Queensland, Australia; 17°51′00.6″S, 141°07′39.3″E.

Type material:

Holotype: HWML 217835, ex. Acrochordus arafurae, small intestine, Leichardt Lagoon, Queensland, Australia, 24 July 2007, coll. V. Tkach. Paratypes: HWML 217836 (5 specimens on 5 slides), labeled identical to the holotype.

Representative DNA sequences:

ITS region + 28S: PP992053; COI: PP991442.

ZooBank registration:

urn:lsid:zoobank.org:act:F8D009E1-991E-452F-BB6B-918A88E9976B.

Etymology:

The specific epithet refers to the Latin name of the host genus of the new species, file snakes of the genus Acrochordus.

Remarks

This new species belongs to Gogatea based on the same morphological features and phylogenetic placement as mentioned above for G. bijirrii. Gogatea acrochordi is extremely morphologically similar to G. bijirrii. All features that were used to distinguish G. bijirrii from other Gogatea spp. are the same, with only small changes to exact sizes and ratios (Table II). The ranges of most metric characteristics and ratios of G. acrochordi and G. bijirrii overlap, but most measurements of G. acrochordi are smaller on average. The most notable difference is that the relative length of the cirrus sac in G. acrochordi (35–39% of body length, average 37%) is substantially larger than that in G. bijirrii (23–31%, average 28%). Although G. acrochordi and G. bijirrii have identical 28S and ITS sequences, they differ by at least 5.1% in COI (Table III).

Gogatea acrochordi differs from other congeners sequenced so far by 2.2–3.7% in partial sequences of 28S, 5.7–38.3% in the ITS region, and 14.8–17.4% in COI (Table III). The high variation in the ITS region sequences is due to the large deletion in ITS1 of Gogatea sp.

No variation was detected among the 6 isolates sequenced for 28S and 5 isolates sequenced for the ITS region; no more than 0.6% intraspecific variation was detected in COI in 4 sequenced isolates.

Gogatea anacetabulata n. sp. Achatz, Von Holten, Binh and Tkach (Figs. 26–33)

Figures 26–29.

Figures 26–29.

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Gogatea anacetabulata n. sp. holotype. (26) Entire, ventral view. (27) Arrangement of vitelline follicles. (28) Ventral view of posterior portion of opisthosoma with female reproductive system omitted (ovary shown as outline). (29) Ventral view of posterior portion of opisthosoma with male reproductive system omitted (testes shown as outline). Abbreviations: C, ceca; CS, cirrus sac; E, egg; GA, genital atrium; M, metraterm; O, ovary; T, testis; VR, vitelline reservoir.

Figures 30–33.

Figures 30–33.

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Gogatea anacetabulata n. sp. paratype. (30) Entire, ventral view. (31) Arrangement of vitelline follicles. (32) Ventral view of posterior portion of opisthosoma with female reproductive system omitted (ovary shown as outline). (33) Ventral view of posterior portion of opisthosoma with male reproductive system omitted (testes shown as outline). Abbreviations: C, ceca; CS, cirrus sac; E, egg; GA, genital atrium; M, metraterm; O, ovary; T, testis; U, uterus; VR, vitelline reservoir.

Description (based on 29 adult specimens):

Measurements of holotype in text (all measurements in micrometers); measurements of entire series given in Table II. Body 1,617 long, consisting of distinct prosoma and opisthosoma; prosoma oval, 1,298 long, widest at level of holdfast organ, 631; opisthosoma cylindrical, 319 × 324. Prosoma:opisthosoma length ratio 4.0. Oral sucker terminal, 126 × 130. Ventral sucker and pseudosuckers absent. Holdfast organ oval, with longitudinal slit-like opening, 389 × 295. Prepharynx absent. Pharynx subspherical, 65 × 65. Esophagus 239 long. Cecal bifurcation in anterior 25% of prosoma length. Ceca slender, extend to level of anterior margin of ovary.

Testes 2, tandem, rounded. Anterior testis 198 × 191; posterior testis 162 × 196. Cirrus sac extends anteriorly beyond anterior testis to near level of middle of holdfast organ, contains seminal vesicle and cirrus, 755 × 54, occupies 47% of body length. Genital pore slightly subterminal, dorsal.

Ovary intertesticular, subspherical, 103 × 105. Oötype and Mehlis’ gland intertesticular. Vitelline follicles large, distributed in 2 lateral elongated fields extending from near anterior level of holdfast organ to near prosoma–opisthosoma junction; the fields may be confluent anteriorly. Vitelline reservoir intertesticular. Uterus ventral to gonads, extends anteriorly beyond level of ovary before turning and extending posteriorly as metraterm, opens into genital atrium. Uterus contains 1 egg in holotype and up to 6 eggs in paratypes. Eggs 84–188 × 43–110. Excretory pore not observed.

Taxonomic summary

Type host:

Fowlea piscator (Schneider) (Squamata: Serpentes).

Site of infection:

Small intestine.

Type locality:

Vicinities of Nha Trang, Khánh Hòa province, Vietnam.

Type material:

Holotype: HWML 217831 (along with 1 paratype on the same slide, clearly indicated), ex. Fowlea piscator, small intestine, vicinities of Nha Trang, Khánh Hòa province, Vietnam, 15 October 2016, coll. V. Tkach. Paratypes: HWML 217832 (27 specimens on 18 slides), labeled identical to the holotype.

Representative DNA sequences:

ITS region + 28S: PP992058; COI: PP991447.

ZooBank registration:

urn:lsid:zoobank.org:act:B39B8A25-A0DA-49F0-9136-C0E102BEABD2.

Etymology:

The specific epithet refers to the unique morphological feature of the new species, namely the lack of the ventral sucker.

Remarks

The new species belongs to Gogatea based on morphological characteristics, including the shape and relative size of the holdfast organ, the presence of a cirrus sac, the shape of the body including an elongated opisthosoma, and the horseshoe-like distribution of the vitellarium around the holdfast organ. It was also placed with other Gogatea sequences in our ribosomal molecular phylogenetic analysis.

This species is easily differentiated from all congeners by the lack of a ventral sucker. Gogatea anacetabulata is further distinguished from its congeners by a generally longer esophagus with similar body size (esophagus measures 157–297 in this new species vs. 106 in G. serpentum, 36–80 in G. mehri, 140 in G. karachiensis, 40 in G. joyeuxi, 67–149 in G. taiwanensis, 91–198 in G. bijirrii, and 111–161 in G. acrochordi) and longer cirrus sac (502–849 in G. anacetabulata vs. 300–473 in G. serpentum, 360–420 in G. mehri, 500 in G. karachiensis, 332–362 in G. taiwanensis, 300–400 in G. joyeuxi, 417–508 in G. bijirrii, and 402–508 in G. acrochordi).

Gogatea anacetabulata differs from other congeners sequenced so far by 2.9–3.7% of nucleotide positions in partial sequences of 28S, 5.7–40.7% in the ITS region, and 12.8–15.5% in COI (Table III). As with the other new species, the high level of variation in ITS region sequences is the result of the 375-bp-long deletion in ITS1 of Gogatea sp.

No variation was detected in 28S, ITS region, and COI sequences of 2 isolates of G. anacetabulata.

DISCUSSION

Gogatea is a small genus of cyathocotylids that before this study included only 2 recognized nominal species: the type species G. serpentum and G. mehri. Members of the genus were reported in the Indomalayan realm, from eastern Pakistan to Thailand and Vietnam (Farooq, 1973; Dubois, 1989). Our study revealed the presence of 3 additional species, including the first representatives of the genus from Australia, parasitic in file snakes. The file snakes (order Acrochordoidea McDowell, family Acrochordidae Bonaparte) are an ancient lineage of snakes containing only a single genus, Acrochordus Hornstedt. The exact relationships between acrochordoideans and other snake groups are still unclear (Pyron et al., 2013; Figueroa et al., 2016; Zheng and Weins, 2016; Zaher et al., 2019). Our phylogenetic analysis based on the 28S gene placed the sequences from acrochordoideans in a clade weakly separated from 2 other congeners parasitic in more derived colubrids (yellow-spotted keelback Fowlea flavipunctata Hallowell and F. piscator). All other reports of Gogatea, lacking molecular data, have come from colubrid hosts, i.e., Chinese water snake Enhydris chinensis Gray (Fischthal and Kuntz, 1975; Curran et al., 2001), rice paddy snake Enhydris plumbea Boie (Curran et al., 2001), F. piscator (Gogate, 1932; Mehra, 1947; Dwivedi and Chauhan, 1969), viperine water snake Natrix maura L. (Joyeux and Baer, 1934; Dollfus, 1953), grass snake Natrix natrix L. (Hughes, 1929; Joyeuxi and Baer, 1934), and oriental rat snake Ptyas mucosa L. (Bhutta and Khan, 1975), or from a homalopsid such as Cerberus rynchops Schneider (Farooq, 1973). With the present limited data (Fig. 1), 2 contrasting hypotheses can be suggested regarding the directionality of the host switching between Gogatea spp. parasitic in acrochordid and in more recently derived groups of snakes. The first possibility is that the parasites switched from the older group of hosts (Acrochordidae) into the more recent one (Colubridae); the second possibility is that these digeneans switched from colubrid to acrochordid snakes. Although our phylogeny may weakly indicate possible cophylogenetic patterns between these parasites and their hosts, more data are necessary to further explore this interesting question.

Combined with the notable fact that colubrids are distributed worldwide but cyathocotylids from snakes are known in only the Old World, the pattern of snake cyathocotylid distribution poses interesting questions regarding the dispersal and historical biogeography of these parasites. Only 2 species, G. acrochordi and G. bijirrii, are found in the Australasian realm, whereas others are found in Indomalaya, including the unidentified specimen from the Elephant trunk file snake Acrochordus javanicus Hornstedt from Thailand sequenced by Achatz et al. (2019), which formed a clade with G. acrochordi and G. bijirrii. Based on the current knowledge of the fossil record and molecular phylogenetic data on file snakes (Sanders et al., 2010), a dispersal event likely occurred between Indomalaya and Australasia, potentially within the file snake hosts rather than as a result of 2 independent host-switching events between colubrids and acrochordids.

Gogatea sp. had a much shorter ITS region sequence than did its congeners (377–414 bp shorter). This species has a 375-bp-long deletion in ITS1; the sequences were of high quality and verified through amplification and sequencing with 3 different pairs of primers. This deletion dramatically increases the pairwise differences between Gogatea sp. and its congeners to 38.3–40.7% compared with only 6.0–9.3% excluding it.

The taxonomic history of the previously accepted Gogatea spp. is complex and includes substantial disputes on the synonymy of species and between genera. Gogatea serpentum was originally described as Prohemistomum serpentum Gogate, 1932 from the intestine of an F. piscator Schneider in Myanmar (referred to as Burma at the time) and later transferred to Gogatea, which was erected for the species (Lutz, 1935). Mehra (1947) split G. serpentum into 2 subspecies: G. serpentum serpentum (Gogate, 1932) and G. serpentum indicum Mehra, 1947 based on specimens from F. piscator in India. Later, Dwivedi and Chauhan (1969) elevated G. s. indicum to species status as G. mehri. Dubois (1975b) rejected G. mehri and restored it to G. s. indicum. More recently, Achatz et al. (2019) restored G. mehri based on a study of new materials. Baugh (1958) described Gogatea incognitum Baugh, 1958; however, Dubois (1975b) synonymized it with G. mehri (referred to as G. s. indicum). Farooq (1973) described 2 additional species: Gogatea kalrii Farooq, 1973 and G. karachiensis Farooq, 1973 from the bockadam snake C. rynchops in Pakistan, but Dubois (1980, 1989) synonymized both species with G. mehri (referred to as G. s. indicum).

Although we do not dispute the synonymy of G. incognitum and G. kalrii with G. mehri, we disagree with the synonymization of G. karachiensis due to the presence of several distinguishing morphological characteristics. The body shape of G. karachiensis is more rounded or circular than the elongated body of G. mehri (and other nominal Gogatea spp.). Gogatea karachiensis has a noticeably longer prosoma compared with the opisthosoma (prosoma:opisthosoma ratio of 3.23 in G. karachiensis vs. 1.67 in G. mehri based on the original measurements of each species) and a lower oral sucker:ventral sucker length ratio (1.4 in G. karachiensis vs. greater than 2.0 based on original measurements). The holdfast organ of G. karachiensis (420 × 400) is about twice as large as that in G. mehri (210–270 × 180–225) despite both species having similar body lengths (1,270 in G. karachiensis vs. 1,134–1,176 in G. mehri). Based on these differences, we reject the synonymy of G. karachiensis with G. mehri and restore G. karachiensis. The description of G. karachiensis does not mention or show tegumental spines, and we believe that this species should have spines based on the fact that all other members of this digenean group have them.

Four other cyathocotylid genera are known to parasitize snake definitive hosts: Serpentostephanus Sudarikov, 1961 in Tunisia; Mesostephanoides Dubois, 1951 in Rangoon; Szidatia Dubois, 1938 in Tunisia, Morocco, Vietnam, and Thailand; and Prohemistomum Odhner, 1913 in experimentally infected snakes (Yamaguti, 1971; Niewiadomska, 2002). The validity of Mesostephanoides and Szidatia has been questioned by previous authors based on morphological data (Chatterji, 1940; Curran et al., 2001). Dubois (1951) erected Mesostephanoides and transferred Gogatea burmanicus Chatterji, 1940 to Mesostephanoides as its type species. Dwivedi and Chauhan (1969) returned G. burmanicus to Gogatea and synonymized the genera. Yamaguti (1971) and Dubois (1989) considered Mesostephanoides valid. Fischthal and Kuntz (1975) described Mesostephanoides taiwanesis Fischthal and Kuntz, 1975. Curran et al. (2001) redescribed the species based on new material and transferred it to Szidatia. These authors also disputed the validity of the features used to distinguish Mesostephanoides from Gogatea (i.e., prosoma:body length ratio and the length of spined cirrus) proposed by Dubois (1951). Both Gogatea and Mesostephanoides spp. have a vitellarium that is confluent anteriorly. Therefore, due to the lack of meaningful morphological characteristics differentiating between these 2 genera, we synonymize Mesostephanoides with Gogatea.

Multiple authors (Chatterji, 1940; Mehra, 1947; Baugh, 1958; Agrawal, 1966) and Dwivedi and Chauhan (1969) have rejected Szidatia and considered it to be a synonym of Gogatea. Dubois (1951), Dollfus (1953), and Yamaguti (1958, 1971) maintained Szidatia as a separate genus. Dubois (1975a) also rejected the synonymization of Neogogatea Chandler and Rausch, 1947 with Gogatea proposed by Dwivedi and Chauhan (1969) but did not directly comment on the synonymization of Szidatia with Gogatea. Instead, Dubois (1975a) simply stated in a footnote that Gogatea and Szidatia are morphologically different. In his system of the Cyathocotylidae, Dubois (1987) considered Szidatia to be a valid genus.

Gogatea and Szidatia are differentiated based on the size and shape of the holdfast organ (large in Gogatea vs. small in Szidatia) and distribution of the vitellarium (confluent in the shape of a horseshoe in Gogatea vs. nonconfluent bands in Szidatia) (Niewiadomska, 2002). However, Mehra (1947), Agrawal (1966), and Curran et al. (2001) suggested that these characters may vary within Gogatea spp., e.g., due to different methods of fixation. Based on our materials and prior descriptions, the holdfast organ shape and size of Gogatea spp. is variable (Gogate, 1932; Chatterji, 1940) (Figs. 5, 6, 12, 23, 24, 27, 31). The holdfast organ of S. taiwanensis and Szidatia joyeuxi Hughes, 1929 occupies a large proportion of the prosoma, similar to some reports of G. serpentum (Mehra, 1947). The holdfast organ of diplostomoideans can differ dramatically in size based on the level of eversion in individual specimens (T. J. Achatz and V. V. Tkach, pers. obs.) (everted in Fig. 24 and not everted in Fig. 23) and congeners (for instance, see variation among Crassiphiala spp. in Achatz et al., 2023b). The size of the holdfast organ should not be strongly relied upon as a critical feature to distinguish between genera or species.

Figures 8–12.

Figures 8–12.

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Gogatea bijirrii n. sp. paratype. (8) Entire, ventral view. (9) Ventral view of posterior portion of opisthosoma with all structures shown. (10) Ventral view of posterior portion of opisthosoma with male reproductive system omitted (testes shown as outline). (11) Ventral view of posterior portion of opisthosoma with female reproductive system omitted (ovary shown as outline). (12) Arrangement of vitelline follicles. Abbreviations: C, ceca; CS, cirrus sac; E, egg; GA, genital atrium; M, metraterm; O, ovary; T, testis; U, uterus; VR, vitelline reservoir.

Likewise, the vitellarium of S. taiwanesis was shown to vary between confluent and nonconfluent in these digeneans based on the method of fixation (Curran et al., 2001). According to these authors, cold-fixed specimens had a confluent vitellarium, whereas heat-killed specimens had a nonconfluent vitellarium. Likewise, the vitellarium of G. anacetabulata and G. acrochordi appears to be confluent (as in Gogatea) or practically non-confluent (similar to Szidatia) in our heat-killed specimens. Considering extremely vague morphological differences between these genera and the variable nature of the characters used for their differentiation, we synonymize Szidatia with Gogatea and transfer both currently recognized species of Szidatia into Gogatea as G. joyeuxi and G. taiwanensis.

The monotypic genus Serpentostephanus was erected by Sudarikov (1961) for Prosostephanus natricis Dubois, 1958 based on the lack of a “caudal process” (cf. distinct opisthosoma) and more weakly developed groove of the holdfast organ compared with those of other Prosostephanus spp. Sudarikov (1961) also noted that P. natricis parasitizes snakes in Africa, whereas in Asia mammals are the typical hosts of Prosostephanus spp. Dubois (1987) and Niewiadomska (2002) also considered Serpentostephanus and Prosostephanus Lutz, 1935 to be distinct genera. Based on the original description by Dubois (1958), we agree with this opinion. However, DNA sequences from Serpentostephanus natricis (Dubois, 1958) are necessary to determine its phylogenetic relationships with other cyathocotylids. We hypothesize that this genus is closely related to other cyathocotylids from snakes.

Specimens of G. bijirrii and G. anacetabulata exhibited mirror symmetry in the position of gonads. Although this phenomenon is not rare in other digeneans (Achatz et al., 2018 and references therein; Fernandes et al., 2021), it has not been previously stated for Gogatea spp. However, the illustration of G. taiwanensis published by Fischthal and Kuntz (1975) shows symmetry mirroring specimens of Curran et al. (2001).

The loss of a ventral sucker in G. anacetabulata is unusual but not unique among cyathocotylids. For instance, Cyathocotyle bushiensis Khan, 1962 secondarily lost its ventral sucker, whereas most of its congeners still possess it. Likewise, some representatives of Prosostephanus Lutz 1935, Holostephanus Szidat 1936, and Duboisia Szidat 1936 each lack a ventral sucker, whereas their congeners possess it (Niewiadomska, 2002). However, Gogatea is the only cyathocotylid genus in which this phenomenon has been confirmed by use of DNA sequences.

DNA sequences of several digeneans identified as Cyathocotyle Mühling, 1896 are available in GenBank and included in our analysis (Fig. 1). Only 2 of these taxa have been identified to the species level (Cyathocotyle prussica Mühling, 1896 and Cy. bushiensis); the remainder were only identified as Cyathocotyle sp. (Schwelm et al., 2020). Moreover, only the data from Cy. bushiensis originated from morphologically identified adults, whereas the remaining sequences came from larval stages. Cyathocotyle was found to be non-monophyletic in our analysis due to the inclusion of H. dubinini, another digenean sequenced and identified as an adult (Fig. 1). It is clear that at least 1 of the 2 clades currently identified as Cyathocotyle must represent a different genus. We consider the clade consisting of Cy. bushiensis, Cyathocotyle sp. (GenBank accession MN726943), and Cyathocotylidae sp. (GenBank accession OR592546) to represent Cyathocotyle in our analysis, whereas the larval stages identified as Cy. prussica and Cyathocotyle sp. (GenBank accessions MN726941 and MN726942) represent an unknown genus. More DNA sequence data from adult Cyathocotyle spp. are necessary to explore the relationships within the genus and the phenomenon of the secondary loss of the ventral sucker in Cy. bushiensis.

Recently Grano-Maldonado et al. (2024) sequenced a variety of metazoan parasites from Pacific silverstripe halfbeak Hyporhamphus naos Banford and Collette, 2001 in Mexico. These authors included several 28S sequences from metacercariae of Mesostephanus microbursa Caballero, Grocott, and Zerecero, 1953 (GenBank accessions OR4826501, OR4826521, OR4826551), which were similar but not identical to sequences from morphologically identified adult stages of the species (GenBank accessions MF398325, MK650446) (Fig. 1). Considering that diplostomoideans often demonstrate low (or no) interspecific variation in 28S (see Achatz et al., 2023a and references therein) (Table III) and rarely any intraspecific variation in this gene (up to 1 base), these new sequences likely represent 1 or 2 additional distinct species. However, Grano-Maldonado et al. (2024) did not provide COI sequences of these specimens and made several erroneous statements regarding diplostomoideans, e.g., referring to them as heterophyids. Additional data are required to confirm the identities of these digeneans. The sequences of adult Me. microbursa demonstrate substantial genetic divergence (2.7% in 28S and 16.4% in COI) and certainly represent different species (Hernández-Mena et al., 2017; Achatz et al., 2019). DNA sequences of adult stages from the type host, brown pelican Pelecanus occidentalis L., remain necessary to determine which lineage may represent the true Me. microbursa.

Although the family Cyathocotylidae is globally distributed and members parasitize fish, reptilian, avian, and mammalian definitive hosts, only a few studies have been conducted to explore the phylogenetic interrelationships of cyathocotylids using ribosomal DNA sequences (Blasco-Costa and Locke, 2017; Achatz et al., 2019; Schwelm et al., 2020; Grano-Maldonado et al., 2024). Additional sequencing of adult cyathocotylids is necessary to investigate the interrelationships between and within most cyathocotylid genera. In the case of Gogatea spp., the remaining nominal species need to be sequenced to properly reconstruct the evolutionary history of this interesting cyathocotylid genus. We also anticipate that more members of the genus will be discovered with the expansion of geographic and host coverage of parasitological investigations of snakes and other hosts.

ACKNOWLEDGMENTS

We sincerely thank Dr. Scott Snyder and Dane Trembath for their invaluable help with collecting specimens in Australia. This research was supported by the National Science Foundation (grant DEB-1120734 to V.V.T.; REU Site award 1852459 to the University of North Dakota School of Medicine and Health Sciences), the National Institutes of Health (grant R15AI092622 to V.V.T.; Institutional Development Award grant P20GM103442 to University of North Dakota School of Medicine and Health Sciences), the Midwestern Association of Parasitologists, and the University System of Georgia Stem Initiative IV (Middle Georgia State University).

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