Anathelges hyptius ( Thompson, 1902 )

Romero-Rodriguez, Jesús & Álvarez, Fernando, 2023, Parasitic bopyrid isopods of hermit crabs (Anomura, Paguridae) from the Atlantic coast of Mexico, with notes on their reproduction and distribution, European Journal of Taxonomy 861, pp. 132-167 : 134-139

Anathelges hyptius ( Thompson, 1902)

Figs 1 , 2A , 3 , Table 1

Stegophryxus hyptius Thompson, 1902: 53–56 , pls. 9–10.

Stegophryxus hyptius – Richardson 1904: 59; 1905: 532–535, 537, figs 578, 579. — Rathbun 1905: 48. — Sumner et al. 1913a: 136; 1913b: 661. — Kunkel 1918: 236. — Reinhard et al. 1947: 70–72. — Reinhard 1949: 17, 18, 20, 21, 27, 29, 30; 1956: 101. — Caullery 1950: 97. — Reinhard & Buckeridge 1950: 131. — Caullery 1952: 76. — Reverberi 1952: 292. — von Brand 1952: 256, 271, table 41; 1966: 222, table 38. — Szidat 1959: 504. — Florkin 1960: 405. — Danforth 1963: 11, 20. — Bowman 1964: 105, 107–109, pl. 14, fig. 22. — Noble & Noble 1964: 392–393, figs XVI-5a, 5b, 5c. — Smith 1964: 105. — Oguro 1967: 67 (in table 3). — Bourdon 1968: 133. — Schultz 1969: 322, fig. 513. — Kaestner 1970: 463. — Gosner 1971: 476. — Markham 1972: 73; 1974: 33, 35, 38, 40, figs 1–3; 1978: 102, 111, 114, 116, table 1; 1988: 3, 45–46, 57, table 1; 2003: 73–74. — Adkison & Heard 1978: 408. — García-Gómez 1983: 22, 37. — Overstreet 1983: 225. — Adams et al. 1987: 127. — Greenwood & Adams 1987: 106. — Anderson 1990: 290. — Korpelainen 1990: 165. — McDermott 1998: 1042–1044; 2001: 629, 634–635; 2002: 39. — Boyko & Williams 2003: 796, 797, 798. — Meconcelli et al. 2015: 43.

Stegophrixus hyptius – Nierstrasz & Brender à Brandis 1931: 197–198.

Stegophryxus hyptias (sic) – Miner 1950: 450, 453, pl. 145.

Stegophryxus sp. – Baffoni 1953: 447. — Reinhard 1956: 93. — Kaestner 1967: 1161; 1970: 425, 463.

?”Male bopyrid isopod” – Lemaitre et al. 1982: 697, fig. 7C.

Anathelges hyptius – Boyko & Williams 2003: 798–800, figs 2–3; 2004: 361, 369; 2009: 203. — RománContreras & Martínez-Mayén 2011: 1145–1147, 1150. — Romero-Rodríguez & Román-Contreras 2013: 646 (in table 3). — Cericola & Williams 2015: 238 (in table 1). — Ewers-Saucedo 2019: 225. — Romero-Rodríguez & Álvarez 2020: 226 (in table 1). — Aguilar-Perera 2022: 115 (in table 1).

Anathelges hyptuis (sic) – Schotte et al. 2009: 981.

Anathelges cf. hyptius – Diaz & Roccatagliata 2006: 331–340, figs 1–6. — Pardo et al. 2009: 2041– 2042 , 2052–2053, table 1.

Material examined

MEXICO • 1 ovigerous ♀ (2.45 mm TL), 1 ♂ (1.64 mm TL); Campeche, Laguna de Términos, Estero Pargo ; 18º38′05.64″ N, 91º46′16.39″ W; 6 Jun. 1981; V. Solís et al. leg.; host ♀ of Pagurus maclaughlinae García-Gómez, 1982 (2.50 mm SL); J. Romero det. host; CNCR-36504 • 1 ovigerous ♀ (3.80 mm TL), 1 ♂ (1.98 mm TL); same locality as for preceding; 14 Nov. 1984; same collector; same host data as for preceding (2.97 mm SL); CNCR-36507 • 1 ovigerous ♀ (3.00 mm TL), 1 ♂ (1.31 mm TL), same locality as for preceding; 20 May 1987; same collector; host ♂ of same species as for preceding (2.25 mm SL); CNCR-36524-A • 1 ovigerous ♀ (3.70 mm TL), 1 ♂ (1.53 mm TL); same collection data as for preceding; same host data as for preceding (3.60 mm SL); CNCR-36524-B • 19 ovigerous ♀♀ (3.88 ± 0.62 mm TL), 19 ♂♂ (1.89 ± 0.28 mm TL), 2 cryptoniscus larvae (0.63 ± 0.07 mm LT); same locality; 8 Dec. 1987; same collector; host 10 ♀♀, 9 ♂♂ of same species as for preceding (3.47 ± 0.65 mm SL); CNCR-36525 • 1 ovigerous ♀ (3.17 mm TL), 1 ♂ (1.78 mm TL); Campeche, Laguna de Términos, La Bayoneta ; 18°46′42.0″ N, 91°29′14.7″ W; 3 Oct. 1981; same collector; host ♀ of same species as for preceding (3.17 mm SL); J. Romero det. hosts; CNCR-36505-A • 1 cryptoniscus larva (0.56 mm TL); same locality; same host data as for preceding (3.17 mm SL); CNCR-36505-B • 1 ♀ (4.25 mm TL), 1 ♂ (2.00 mm TL); same locality; 3 Nov. 1981; same collector; detached from host; CNCR-36527 • 1 ovigerous ♀ (2.13 mm TL), 1 ♂ (1.31 mm TL); Campeche, Laguna de Términos, Punta Zasnath ; 18º46′20.77″ N, 91º19′39.16″ W; 1 Aug. 1984; same collector; host ♀ of same species as for preceding (2.40 mm SL); CNCR-36506-A • 1 ovigerous ♀ (2.00 mm TL), 1 ♂ (1.30 mm TL); same locality; same host data as for preceding (2.03 mm SL); CNCR-36506-B • 1 ovigerous ♀ (4.00 mm TL), 1 ♂ (1.96 mm TL); Campeche, Laguna de Términos, Isla Pájaros ; 18º38′08.22″ N, 91º41′45.72″ W; 10 Mar. 1981; same collector; same host data as for preceding (3.33 mm SL); CNCR-36526 • 1 ♀ (3.40 mm TL), 1 ♂ (1.55 mm TL); Campeche, Laguna de Términos, Punta Gorda ; 18º43′18.34″ N, 91º33′50.17″ W; 14 Nov. 1984; same collector; detached from host; CNCR-36528 .

Distribution

Anathelges hyptius has one of the largest geographical ranges for any bopyrid species in the western Atlantic ( Fig. 1 ), from Massachusetts, USA, to Curaçao and the Bahamas ( Boyko & Williams 2004), which may be related to the eight species of pagurids used as hosts throughout its range ( Markham 1978; Boyko & Williams 2004): Iridopagurus caribbensis (A. Milne-Edwards & Bouvier, 1893; I. margaritensis García-Gómez, 1983 ; Pagurus annulipes (Stimpson, 1860) ; P. brevidactylus (Stimpson, 1859) ; P. longicarpus Say, 1817 ; P. maclaughlinae ; P. provenzanoi Forest & de Saint Laurent, 1968 and P. stimpsoni (A. Milne-Edwards & Bouvier, 1893). It has been suggested that its geographical distribution extends to Argentina and Chile parasitizing two more hosts ( Diaz & Roccatagliata 2006; Pardo et al. 2009): P. comptus (White, 1847) and P. villosus Nicolet in Gay, 1849, respectively.

In Mexico it has only been recorded in Laguna de Términos parasitizing a single female of P. longicarpus ( Román-Contreras & Martínez-Mayén 2011) , so this record does not represent a new locality for this bopyrid but P. mclaughlinae is recorded as new host in the area.

Remarks

Our material ( Figs 2A , 3A, F ) conforms well with the characters proposed for A. hyptius by Thompson (1902), but some variations were observed. The barbula of adult females consists of a single slightly acute and curved projection on each side and two foliaceus plates in the medial margin ( Fig. 3B ). The barbula of this species was described with three curved processes on each side but only two lateral projections were illustrated ( Thompson 1902: plate 9, fig. 7). However, the observed specimens agree

with the subsequent illustrations and description of the barbula provided by Markham (1974: fig. 1d) and Diaz & Roccatagliata (2006: fig. 4b).

Overall, the first pair of oostegites of the adult females examined ( Fig. 3C–D ) are similar to those described by Thompson (1902), although this author did not define the internal ridge. Markham (1974: fig. 1e) illustrated it smooth and almost straight, contrasting with the inner ridge thickened in the middle portion and bearing one small digitation proximally recorded in our adult females ( Fig. 3D ), which coincides with what Diaz & Roccatagliata (2006: fig. 5g) reported for an adult female of A. cf. hyptius parasitizing the abdomen of P. comptus in Argentina. Likewise, an ovigerous female (36525-Q) had no uropods thus the last segment of pleon had a round appearance. The maxilliped was similar to that noted by Thompson (1902: pl. 9, fig. 5) but the anterior segment was somewhat rectangular in outline when the external lateral margin, that tends to bend inwards, is extended; the surface of both anterior and posterior segments has a rough appearance ( Fig. 3E ).

Reproduction

Sizes of the two adult females without embryos in the marsupium were 3.40 and 4.25 mm TL, both paired with a male but detached from the host. Average TL of the ovigerous females (n = 23) was 3.65 ± 0.73 mm and ranged from 2.13 to 5.53 mm TL ( Table 1 ), which are smaller than the range of females carrying embryos (5.98–6.56 mm long) reported by McDermott (1998); however, the overall average fecundity calculated (1906.67 ± 1021.51 embryos) is close to the average number of embryos (2462.33 ± 1,181, calculated from original data) reported by McDermott (1998). The lowest (480 embryos) and highest (4572 embryos) fecundities were recorded from the ovigerous females with the minimum and maximum TL, respectively. The latter could be explained by the significant (τ 16 = 5.74, p <0.05) and positive (r = 0.67) relationship calculated between fecundity and the size of the ovigerous females: fecundity = 1808 + 1031.10 (TL). The highest number of embryos recorded ( Table 1 ) was higher than the maximum fecundity (3437 embryos) reported by McDermott (1998) in a 6.56 mm female.

The average length and width of embryos of A. hyptius by stage of development and epicaridium larvae are shown in Table 1 . Sizes of embryos in egg stage ranged from 0.11 to 0.15 mm of length and between 0.09 and 0.13 mm of width, whilst the length of embryos in stage I varied from 0.13 to 0.16 mm and their width was between 0.09 and 0.15 mm. These sizes are smaller than those reported by McDermott (1998) for embryos in an early stage (0.172 ± 0 mm long and 0.144 ± 0.4 mm wide), this difference may be due to the low number of embryos examined by the latter author (n = 10). Volumes of embryos in egg stage ranged from 0.0005 to 0.0013 mm 3, and for embryos in stage I varied between 0.0006 and 0.0019 mm 3. The average volume of both stages of development ( Table 1 ) is similar to those reported for other bopyrids of comparable sizes (see Romero-Rodríguez & Álvarez 2020). The epicaridium larvae length ranged from 0.15 to 0.20 mm and the width between 0.09 and 0.15 mm.

The three cryptoniscus larvae recorded, one attached dorsally to the posterior limit of the host’s cephalothorax and two more attached to the female’s marsupium (see below), matched well the

description but were smaller (0.63 ± 0.07 mm TL, 0.25 ± 0.02 mm width) than the length of 0.7 mm provided by Thompson (1902).

The average TL of males was 1.80 ± 0.30 mm, and varied from 1.33 to 2.25 mm TL which is similar to that recorded by McDermott (1998) and Boyko & Williams (2003), but smaller than the 3 mm males reported by Thompson (1902). Except for one male, that was attached transversally between pleomeres 1–2 of the female, all males were inside the females’ brood pouch between pereomeres 6–7, transversely aligned with their head directed towards the right side of the female and attached to the last oostegites. Although this is the typical position reported for males of A. hyptius, Markham (1974) registered during live observations that males can get out from the brood pouch and crawl all over the female’s body.

The number and average size by sex of individuals of P. mclaughlinae parasitized by A. hyptius were rather similar, 14 females (3.28 ± 0.58 mm SL) and 13 males (3.32 ± 0.72 mm SL) were recorded. No statistical differences by sex were found (χ 2 = 0.08, df = 1; P <0.05).

The abdomen of a P. mclaughlinae male of 3.36 mm SL was simultaneously parasitized by A. hyptius and an undetermined rhizocephalan; one externa with two lobes of different sizes; were located below the bopyrid female, this last one was tightly attached to the host abdomen, with its head directed towards the host pleon, while one of its pereomeres was holding the largest externa. The male of A. hyptus was inside the marsupium of this female, additionally two cryptoniscus larvae were observed attached to the inner side of the oostegites of this bopyrid female, one on the lateral margin of the left oostegite 5 and another one on the anterior margin of the oostegite 3 of the right side.

A total of 475 hermit crabs were counted in the samples, of which 29 were parasitized by A. hyptius , this represents a prevalence of 6.11 %.

Figures

Fig. 1. Distribution along the American continent of five bopyrid species that parasite hermit crabs recorded in the Mexican Atlantic. A. Detail of the Atlantic coast of Mexico.

Fig. 2. Dorsal view of ovigerous females of bopyrid isopods that parasites hermit crabs in Atlantic Mexican coasts.A. Anathelges hyptius (Thompson, 1902) (CNCR-36525-C). B. Pseudostegias atlantica Lemos de Castro, 1965 (CNCR-36483). C. Stegias clibanarii Richardson, 1904, stained with methylene blue (CNCR-36487). D. Asymmetrione desultor Markham, 1975 (CNCR-36488). E. Asymmetrione tuxtlaensis sp. nov., with male ventrally attached to pleon (CNCR-36495). F. Bopyrissa wolffi Markham, 1978 (CNCR-36502-A). Scale bars: A–E = 1.0 mm; F = 0.5 mm.

Fig. 3. Anathelges hyptius (Thompson, 1902). A. Ovigerous ♀, dorsal view (CNCR-36525-F). B. Barbula. C. First oostegite, external view. D. Same, internal view. E. Maxilliped. F. ♂, dorsal view (CNCR-36525-E). Scale bars: A = 1.0 mm; B–F = 0.5 mm.

Tables

Table 1. Some reproductive traits of the bopyrid isopods that parasitize hermit crabs at SW Atlantic coasts of Mexico.

Species	TL female (mm)	Fecundity (embryos)	Stage of development	Average sizes (± standard deviation) Length (mm) Width (mm) Volume (mm 3)
Anathelges	2.13 – 4.00	480 – 2615	Egg	0.128 ± 0.010	0.116 ± 0.009	0.0009 ± 0.0002
hyptius
	3.60 – 4.65	1566 – 2516	I	0.146 ± 0.010	0.117 ± 0.013	0.0011 ± 0.0003
	3.00 – 5.53	1092 – 4572	epicaridium	0.172 ± 0.014	0.123 ± 0.012	–
Asymmetrione	4.90	741	I	0.231 ± 0.017	0.200 ± 0.009	0.0049 ± 0.0006
desultor
Asymmetrione	1.69 – 4.85	110 – 606	Egg	0.146 ± 0.016	0.167 ± 0.11	0.0019 ± 0.0005
tuxtlaensis
sp. nov.
	3.20	762	I	0.162 ± 0.16	0.193 ± 0.015	0.0027 ± 0.0007
	2.93 – 3.07	293 – 811	epicaridium	0.115 ± 0.15	0.253 ± 0.014	–
Bopyrissa	3.32 – 4.95	1601 – 4507	Egg	0.127 ± 0.009	0.118 ± 0.0012	0.0009 ± 0.0002
wolffi
	4.90 – 4.50	3917	I	0.158 ± 0.010	0.140 ± 0.10	0.0016 ± 0.0003
	2.18 – 4.10	1305 – 1543	epicaridium	0.180 ± 0.009	0.126 ± 0.008	–
Pseudostegias	3.92	177	Egg	0.214 ± 0.010	0.200 ± 0.011	0.0045 ± 0.0007
atlantica
	3.30 – 4.00	205 – 267	I	0.192 ± 0.015	0.163 ± 0.017	0.0027 ± 0.0007
Stegias	3.80	1892	Egg	0.137 ± 0.009	0.131 ± 0.009	0.0012 ± 0.0002
clibanarii