Asymmetrione tuxtlaensis, Romero-Rodriguez & Álvarez, 2023

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 : 146-153

Asymmetrione tuxtlaensis sp. nov.

urn:lsid:zoobank.org:act:BF09884B-55A7-4FE6-816B-1D890D42CC7C

Figs 1 , 2E , 7–8 , Tables 1–2

Diagnosis

Body outline oblong, right body side longer than left one, head rotated sinistrally, margin of second right pereomere at anterior end. All body regions and segments distinct, unpigmented. First pair of pereopods clearly different in size, pleopods 1–4 biramous, 5 uniramous, uropod uniramous ( Figs 2E , 7A ). Male with body unpigmented, elongated, all segments clearly separated dorsally and laterally, pleon of five pereomeres plus pleotelson, globose uniramous pleopods on all pleomeres and no uropods ( Fig. 8A–B )

Etymology

The specific name ‘ tuxtlaensis ’ refers to the region where more specimens of this species were registered, Los Tuxtlas, Veracruz.

Material examined

Holotype MEXICO • 1 ovigerous ♀ (dissected, 2.86 mm TL); Veracruz, Los Tuxtlas, Montepío ; 18º38′35.23″ N, 95º05′54.43″ W; 19 Feb. 1996; R. Robles leg.; host ♀ of Clibanarius antillensis (3.32 mm SL); C. Hernández det. host.; CNCR-36493-A1.

Allotype MEXICO • 1 ♂ (1.58 mm TL); same collection data as for holotype; CNCR-36493-A2.

Paratypes MEXICO • 1 ovigerous ♀ (3.07 mm TL), 1 ♂ (1.42 mm TL); same collection data as for holotype; same host data as for preceding (3.70 mm SL); CNCR-36493-B • 1 ♀ ovigerous (3.33 mm TL), 1 ♂ (1.33 mm TL); same collection data as for holotype; same host data as for preceding (3.40 mm SL); CNCR-36493-C • 1 juvenile ♀ (2.22 mm TL), 1 ♂ (1.16 mm TL); same collection data as for holotype; host ovigerous ♀ of same species as for preceding (3.50 mm SL); CNCR-36493-D • 1 ovigerous ♀ (3.20 mm TL), 1 ♂ (1.56 mm TL); same locality as for holotype; Jul. 2002; A. Argüelles and M. Maldonado leg.; host ♂ of C. antillensis (3.72 mm SL); A. Argüelles det. host; CNCR-36494 • 1 ovigerous ♀ (2.93 mm TL), 1 ♂ (1.64 mm TL); same locality; 14 Jun. 2016; J.L. Villalobos et al. leg.; host ♀ of same species as for preceding (3.13 mm SL); J. Romero det. hosts; CNCR-36497-A • 1 ovigerous ♀ (1.69 mm TL), 1 ♂ (1.25 mm TL); same collection data as for preceding; host ♂ of same species as for preceding (2.25 mm SL); J. Romero det. hosts; CNCR-36497-B • 1 juvenile ♀ (2.07 mm TL), 1 cryptoniscus larva (1.45 mm TL); same locality; 7 Feb. 2013; F. Álvarez and J.L. Villalobos leg.; right branchial chamber of Calcinus tibicen ♂ (3.84 mm SL); R. Robles det. host; CNCR-36498-A • 1 cryptoniscus larva (1.47 mm TL); same collection data as for preceding; left branchial of same for preceding host; CNCR-36498-B • 1 ♀ ovigerous (1.78 mm TL), 1 ♂ (0.98 TL); Veracruz, Isla Verde ; 19º11′59.18″ N, 96º04′01.28″ W; 26 Feb. 1959; A. Villalobos leg.; host ♀ of C. antillensis (2.90 mm SL); A.J. Provenzano det. host; CNCR-36490 • 1 cryptoniscus larva (1.20 mm TL); same locality as for preceding; 26 May 1969; I. Peña-Ramirez leg.; host ♀ of same species as for preceding (6.00 mm SL); T. Nates det. host; CNCR-36492-A • 1 bopyridium (1.49 mm TL); same collection data as for preceding; same host data as for preceding (4.75 mm SL); CNCR-36492-B • 1 ♀ (4.35 mm TL); same locality; 26 May 1969; I. Peña-Ramirez leg.; detached from host; CNCR-36500 • 1 ovigerous ♀ (2.51 mm TL), 1 ♂ (1.40 TL); Veracruz, La Blanquilla reef; 19º13′22.8″ N, 96º06′00.0″ W; 17 Apr. 1968; J. Cabrera leg.; host ♂ of same species as for preceding (5.53 mm SL); J.C. Nates det. host; CNCR-36491 • 1 ovigerous ♀ (4.85 mm TL), 1 ♂ (2.23 mm TL); Veracruz, Laguna de Tamiahua, Isla Lobos reef, 21º25′09″ N, 97º13′18″ W; 20 May 2005; J.L. Bortolini leg.; host ♀ of same species as for preceding (5.13 mm SL); G. Cervantes det. host; CNCR-36495 • 1 ovigerous ♀ (3.76 mm TL), 1 ♂ (2.02 mm TL); Veracruz, El Morro de la Mancha ; 19º35′22″ N, 96º22′45″ W; 20 Apr. 2006; J.L. Villalobos et al. leg.; host ♂ of same species as for preceding (4.35 mm SL); Y. de los Santos det. host; CNCR-36496 • 1 ♀ (3.33 mm TL), 1 ♂ (2.09 mm TL); Quintana Roo, Ensenada Lamcom, NE border of Isla Blanca ; 21º24′45.44″ N, 86º48′35.29″ W; 18 Jun. 2005; J.L. Villalobos et al. leg.; host ovigerous ♀ of same species as for preceding (5.00 mm SL); J. Romero det. host; CNCR-36499 .

Description

Based on female holotype

MEASUREMENTS. Length 2.86 mm, maximal width 2.22 mm (at second pereomere), head length 0.51 mm, head width 0.56 mm, pleon length 0.42 mm, pleon width 0.73 mm. Body distortion 88º.

HEAD. Ovoid, surface smooth, distinct from first pereomere. Frontal lamina broad, bent upwards with medial notch and two semi-triangular lobes, anterolateral corners rounded. Eyes at ventral anterolateral edges of head, barely visible dorsally ( Fig. 7A ). Antennule 3-segmented, antennae 5-segmented, both with basal article wide and rounded, second article long and cylindrical, last article smaller, rounded, tipped with tiny setae ( Fig. 7B ). Maxilliped with anterior segment larger than posterior one, semi-rectangular of round margins without palp, posterior segment triangular in shape bearing thin and pointed spur ( Fig. 7C ). Barbula with two triangular projections on each side, outer one recurved and sharp, inner projection thicker and blunt, middle margin with medial notch and one rounded projection each side ( Fig. 7D ).

PEREON. Pereomeres dorsally and laterally distinct, similar in width and shape along left side, wider with variable outline along right side. Narrow coxal plates on pereomeres left 1–7 and right 1–4. On left side dorsolateral bosses rounded, occupying nearly entire margin of pereomeres 1–4, on right side, flat and ovoid at half margin of pereomeres 1–4, thick, directed forward and decreasing in size posteriorly on 5–7 ( Fig. 7A ). Oostegites fully enclosing brood pouch ( Fig. 8G ). First pair of oostegites similar in size and shape, anterior segment large and subtriangular, posterior one short, rectangular with rounded margins bearing thin and recurved posterolateral point ( Fig. 7E–G ); inner ridge slightly sinuate, medially thick with rounded projection on proximal portion ( Fig. 7G ); oostegites 2–5 relatively ovate, those on right side larger in size, bearing marginal fringe of setae on posterior edge ( Fig. 7H–O ). Pereopods similar in shape, rounded carina on superior margin of basis, ischium long and cylindrical, meri subqua-drate, carpi conical, propodi swollen distoventrally with deep socket for insertion of strongly recurved dactyli ( Fig. 7P–Q ). First pair of pereopods at both sides of head clearly different in size ( Fig. 7P–Q ). All pereopods on right side similar in size, left ones increasing in size backwards, 6–7 abruptly increasing in size ( Fig. 7A ).

PLEON. Comprised of five segments plus pleotelson, narrowing posteriorly, distinctly separated. Pleo-meres 1–2 with short and rounded lateral plates, triangular pleotelson with rounded edges ( Fig. 7A ). Five pairs of pleopods, biramous on pereomeres 1–4 and uniramous on pereomere 5, all decrease in size posteriorly, endopod and exopod of similar sizes, pleopods on pereomeres 1–3 foliaceus with sinuated margins, on 4–5 cylindrical with smooth borders ( Fig. 7R ). Long, smooth and uniramous uropods ( Fig. 7A, R ).

Female variations. Maxilliped with anterior segment rather quadrate in shape with anterior margin almost straight; the two pairs of projections on each side of the barbula ranged from both small and blunt in one female to both conspicuous and triangular in shape in most females, middle margin of one female with rectangular projection and another female with crenulations of different sizes on each side of the medial notch; the anterior segment of first oostegite ranged from triangular to ovoid, the oostegites’ inner ridge medially thick in most females ranged from slightly sinuous and lacking of projections to bearing one to four projections of different sizes and shape, this variability was recorded even in the first pair of oostegites of a same female ( Fig. 7E, G ); one female with pleopods on pereomere 5 biramous on sinistral and uniramous on dextral; most females bears tiny scales along frontal lamina, ventral side of head, dorsolateral bosses and pereomeres.

Male description (based on allotype)

MEASUREMENTS. Length 1.58 mm, maximal width 0.47 mm (at pereomeres 2–4), head length 0.16 mm, head width 0.31 mm, pleon length 0.45 mm, pleon width 0.27 mm.

HEAD. Ovoid with anterior margin straight, nearly fused to first pereomere medially, conspicuous eyes on posterolateral edges ( Fig. 8A ). Antennule 3-segmented, first one larger, quadrangular in shape, third segment small, rounded tipped with tuft of setae, barely reaches anterior margin of head. Antennae 5-segmented, distal one tipped with tuft of setae, exceeds head edges ( Fig. 8B–C ).

PEREON. Pereomeres with rounded lateral margins, separated by anterolateral indentations, tapering slightly backward ( Fig. 8A ). Midventral tubercles absent ( Fig. 8B ). Pereopods of similar size and shape, basis long, ischium about half size of basis, meri and carpi subquadrate, last one with cup-shaped distal margin for insertion of dactyli tip, propodi ovoid and strongly recurved dactyli; propodi and dactyli progressively smaller posteriorly ( Fig. 8D–E ).

PLEON. Comprised of five pleomeres plus pleotelson, first one narrower than final pereomere, others progressively narrower posteriorly, distinctly separated dorsal and laterally, lateral margins tapered, rounded and folded ventrally, resembling a conical pleon ( Fig. 8A ); globose uniramous pleopods on pleomere 1–5 ( Fig. 8F ). Pleotelson with two rounded posterolateral lobes bearing few tiny setae on each posterolateral corner, conspicuous medial anal cone. Uropods absent ( Fig. 8A–B, F ).

MALE VARIATIONS. Most variations of other examined males seem to be rather minor. One male with head rather rectangular, two males with pereomeres pigmented dorsally, pereomeres of five males slightly decrease in size backwards and pleotelson of one male with square lateral margins.

Juvenile stages

The two juvenile females examined (CNCR-36498-A and CNCR-36493-D) agreed with most characters described for the adult females but with the following traits poorly developed: body slightly asymmetrical since head is barely rotated to left side, frontal lamina wide but not bent up, barbula smooth lacking lateral projections or medial notches, flat dorsolateral bosses on pereomeres 1–4 ( Fig. 8H ), oostegites as small ovoid plates, in largest female barely reaching the midventral portion, first oostegite small but bearing a recurved posterolateral point and smooth inner margin, pereopods smooth or with poorly developed round carina at superior margin of basis, lateral plates in pleomeres 1–5 decreasing in size posteriorly. The individual classified as bopyridium (CNCR-36492-B) shows the following characteristics: body symmetric, all body regions and segments distinct, head rounded and small, frontal lamina wide bearing round bulges on each lateral margin and two more dorsally, conspicuous eyes at mid-lateral margin of head. Antennules and antennae similar to those described for adult females but exceeding head margin ( Fig. 8I ). Pereomeres laterally separate, rectangular in shape with slightly wider and rounded margins covered with tiny scales; middle portion raised as triangular projection decreasing in size posteriorly, on both sides of body large and thin pereopods of similar sizes and shape, propodi slightly swollen distoventrally with recurved dactyli, oostegites not developed. Five triangular pleomeres, first one of same size than last pereomere others decreasing in size posteriorly; five pairs of uniramous pleopods with thick and bifid tip, uropods uniramous with distal margin bifid ( Fig. 8I ).

Type locality

Veracruz, Los Tuxtlas, Montepío, (18º38′35.23″ N, 95º05′54.43″ W).

Distribution

Known from the north-central region of Veracruz and the NE coast of Isla Blanca, Quintana Roo, Mexico ( Fig. 1A ).

Calcinus antillensis Stimpson, 1859 had only been reported as host of A. clibanarii in Colombia ( Markham 1988) and C. tibicen had no previous records as host for any species of Asymmetrione (see McDermott et al. 2010). In Montepío, Veracruz, A tuxtlaensis sp. nov. co-occurred with the abdominal bopyrid P. atlantica , see above, and in Isla Blanca, Quintana Roo with the branchial bopyrid Bopyrissa wolffi . Asymmetrione tuxtlaensis is the fourteenth species of the genus but only the third one recorded from the west Atlantic.

Remarks

Based on the following morphological traits, the specimens examined were included in Asymmetrione Codreanu, Codreanu & Pike, 1965 : females with body extremely asymmetric, bilobed frontal lamina, pereopods with propodi distended distoventrally with deep ‛socket’ for insertion of recurved dactyli. Males with head not fully fused with first pereomere and pleon segmented, thin and bearing pleopods. According to Boyko et al. (2008 onwards), this genus currently comprises 13 species ( A. aequalis Pardo, Boyko & Mantelatto, 2009 ; A. ambodistorta Markham, 1985 ; A. asymmetrica ( Shiino, 1933) ; A. clibanarii Markham, 1975b ; A. dardani Bourdon, 1968 ; A. desultor ; A. foresti ( Bourdon, 1968) ; A. globifera An, Markham & Yu, 2010 ; A. harmoniae Williams, Boyko & Madad, 2019 ; A. imrai Kazmi & Khatoon, 2016 ; A. nossibensis Bourdon, 1976 ; A. sallyae Williams & Schuerlein, 2005 and A. shiinoi Codreanu, Codreanu & Pike, 1965 ), but since A. imrani is considered species inquirenda ( Williams et al. 2019) it is excluded from the following comparison.

A morphological comparison of some traits of the species of Asymmetrione is shown in Table 2 . The strong dextral body distortion (≥ 80º), two lateral projections on each side of the barbula and biramous pleopods suggest a close relationship to A. asymmetrica , A. clibanarii , A. globifera and A. shiinoi . However, the middle margin of the barbula of A. asymmetrica and A. globifera are branched and tuberculated, respectively, also both species have tuberculated pleopods which differ from those of the examined females. Based on the distribution of the species of Asymmetrione the material examined is close to A. clibanarii since, besides A. desultor , it is the only other member of Asymmetrione reported for the Western Atlantic ( Markham 1975b). However, traits described for A. clibanarii as the first oostegite with a more or less rectangular outline, internal ridge not ornamented and without pointed posterior border, five pairs of pleopods biramous with endopod somewhat smaller than exopod, uropods biramous and pereopods of similar size on both sides of body differ from those observed in the females examined. Females of A. shiinoi coincide with our material in the pereopods of dissimilar sizes, biramous pleopods and uniramous uropods but differ in that A. shiinoi has the inner ridge of the first oostegite with scaly tubercules as well as tubercules on the uropods. Therefore, A. tuxtlaensis sp. nov. can be distinguished by the first pair of oostegites with a more or less ovoid outline that bears round projections on the inner ridge and pointed posterior border, first pair of pereopods at both sides of head and clearly different in size, pleopods 1–4 biramous and fifth pair uniramous, and long and smooth uniramous uropod.

Reproduction

Sizes of the two adult females of A. tuxtlaensis sp. nov. without embryos in the marsupium were 3.33 and 4.35 mm TL, the former was paired with a male of 2.09 mm TL. Average TL of ovigerous females (n = 10) was 3.00 ± 0.92 mm and ranged from 1.69 to 4.85 mm TL ( Table 1 ). The overall average fecundity from the four ovigerous females examined was 455 ± 313 embryos, the minimum (110 embryos) was recorded in the smallest ovigerous female whilst the maximum (811 embryos) fecundity was recorded in a female of 2.93 mm TL ( Table 1 ). The average length and width of embryos by stage of development and epicaridium larva are shown in Table 1 . Sizes of embryos in egg stage ranged from 0.118 to 0.182 mm of length and between 0.145 and 0.182 mm of width, whilst the length of embryos in stage I varied from 0.145 to 0.182 mm and their width between 0.164 and 0.218 mm. Volumes of embryo in egg stage ranged from 0.0012 to 0.0031 mm 3, and for embryos in stage I between 0.0018 and 0.0038 mm 3. The average volume of both stages of development ( Table 1 ) is similar to the range calculated for other bopyrids ( Romero-Rodríguez & Álvarez 2020). The epicaridium larvae length ranged from 0.127 to 0.182 mm and the width between 0.218 mm and 0.273 mm.

Asymmetrione tuxtlaensis sp. nov. parasitized more females (n = 10) than males (n = 4) of Calcinus antillensis , though no statistical differences were found (χ 2 = 0.6, df =1; P <0.05) and both host sexes were of similar average sizes 4.05 ± 1.09 mm SL and 3.96 ± 1.37 mm SL, respectively. Two host females were ovigerous, a female of 3.50 mm SL carried 40 embryos rather circular in shape and yellowish in color with an average length, width and volume of 0.329 ± 0.013 mm, 0.314 ± 0.013 mm and 0.017 ± 0.002 mm 3, respectively. The second female of 5.00 mm SL carried 206 embryos attached on the abdomen, which were ovoid in shape and showed a thin eye line, their average length, width and volume were 0.362 ± 0.025 mm, 0.335 ± 0.013 mm and 0.021 ± 0. 002 mm 3, respectively. The number of embryos of both females was less than the average fecundity reported for C. antillensis ( Turra & Leite 1999) but embryo size was in the range reported for this species by Turra & Leite (2007).

The 16 parasitized hosts examined were found in a 694 hermit crab sample, this represents a prevalence of 2.31%.

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. 7. Asymmetrione tuxtlaensis sp. nov. (CNCR-36493-A). A. Ovigerous ♀, dorsal view, holotype (CNCR-36493-A). B. Antennule and antennae. C. Maxilliped. D. Barbula. E. First oostegite right, internal view. F. First oostegite left, external view. G. Same, internal view. H. Second oostegite right, with second pereopod, external view. I. Second oostegite left, external view. J. Third oostegite right, external view. K. Third oostegite left, external view. L. Fourth oostegite right, external view. M. Fourth oostegite left, external view. N. Fifth oostegite right, external view. O. Fifth oostegite left, external view. P. First pereopod right. Q. First pereopod left. R. Pleon, ventral view. Scale bars: A = 1.0 mm; C, E–N, R = 0.5 mm; B, D, O–Q = 0.1 mm.

Fig. 8. Asymmetrione tuxtlaensis sp. nov. A. Dorsal view, holotype ♂ (CNCR-36493-A). B. Ventral view. C. Antennule and antennae ♂. D. First right pereopod of ♂, paratype (CNCR-36495). E. Seventh left pereopod of same ♂ paratype. F. Pleon of same ♂ paratype, ventral view. G. Adult ♀, paratype (CNCR-36499), ventral view. H. Juvenile ♀ (CNCR-36498-A), dorsal view. I. Bopyridium (CNCR- 36492-B), dorsal view. Scale bars: A–B, G–I = 1.0 mm; C–E = 0.1 mm; F = 0.5 mm.