Podocoryna martinicana, Galea, Horia R. & Ferry, Romain, 2013

Galea, Horia R. & Ferry, Romain, 2013, Podocoryna martinicana, a new species of athecate hydroid (Cnidaria: Hydrozoa: Hydractiniidae) from the Caribbean, Zootaxa 3710 (6), pp. 578-590 : 579-589

Podocoryna martinicana sp. nov.

(Pl. 1, 2; Fig. 1; Tables 1 , 2)

Material examined. Martinique, Case-Pilote, 14.638553°, -61.139591°, 18.ii.2013, 10 m: one shell carrying a fertile hydroid colony (holotype, MHNG-INVE-83148), about 50 newly released medusae (paratype, MHNG- INVE-83149), as well as 49 additional shells with hydroid colonies (paratype, MHNG-INVE-83150).

Description. Colonies live exclusively on gastropod shells inhabited by the hermit crab Iridopagurus caribbensis . The hydrorhiza is an encrusting, nearly continuous mat of perisarc-covered stolons, generally not overlaid by coenosarc externally, except for some rare instances in which the latter spreads for a limited extent around the base of some nutritive polyps. The perisarc is rather thin, translucent, straw-colored. Spines are absent. Zooids arise directly from hydrorhiza and are of three types: gastro-, gono-, and tentaculozooids.

Gastrozooids are stout, tall (1.0–5.0 mm high), columnar (0.4–0.8 mm wide), generally 1–6 in number (but up to 9 were observed2) in a linear row along the inner lip of the host shell (Pl. 1F–H). They are provided with up to 86 filiform tentacles with solid endodermal cores, arranged in 2–5 closely-set whorls, held in various attitudes, and irregularly bent or curved. Aberrant, two-headed polyps (Pl. 1I) were irregularly found among the colonies examined. The gastric cavity is lined with prominent longitudinal ridges and villosities, especially visible in polyps with the mouth open wide, or in those turned inside-out (Pl. 1L).

Gonozooids, more numerous (up to 48) and much smaller than their nutritive counterparts (0.5–1.7 mm high, but up to 2 mm in full extension, and 0.2–0.3 mm wide), occur typically on the rim of the upper lip of the host shell (Pl. 1E, G, H). Their dome-shaped hypostome, which does not open externally into a mouth, is encircled by a whorl of 4–9 tentacles reduced to globular, mere stumps (Pl. 2H). Aberrant, two- (Pl. 2I) or even three-headed polyps may be found among the common ones. Up to 30 gonophores are borne on short stalks arising from a budding zone

1. The role of the vents was to allow for the input of oxygenated water, carrying food items, and to prevent potential predators from reaching the hydroids.

2. Their number varies according to the age of the colony and the size of the inhabited shell.

proximal to the tentacular whorl (Pl. 2G). Young gonophores are more or less spherical, while the older ones become more pyriform. All are enveloped in a thin, transparent, membranous sheet ruptured by pulsation of the gonophore before release from the parent polyp. The gonophores are liberated as free-swimming medusae. Medusa buds are provided with four well-developed tentacles, coiled up in the subumbrellar cavity (Pl. 2J).

PLATE 1. Hermit crabs either resting burrowed in sand (A) or foraging (B). Ventral (C), lateral (D), and dorsal (E) views of three crabs, to show the position of gastro- and gonozooids. Encrusting hydrorhiza and gastrozooids on the inner lip of a shell (F). Shell apertures colonized by hydroids (G, H). Double-headed gastrozooid (I). Details of the insertion of tentacles (J) and their solid endodermal cores (K). Inside-out gastrozooids showing the characteristic longitudinal ridges lining their gastric cavity (L). Scale bars (in mm): 0.5 (J, K); 1.0 (F–I); 2.0 (C–E); 2.5 (L); 3.0 (A, B).

PLATE 2. Fertile gastrozooids (A–C). Tentacluzooids (D). Portions of outer lip of a shell showing gonozooids (E, F). Overview of a gonozooid (G) and detail showing its withered tentacles (H). Double-headed gonozooid (I). Young (J) and nearly liberable (K) medusa buds. Newly liberated medusa seen both laterally [with incident (L) and transmitted (M) light], and in oral view (N). Detail of the manubrium ( O). Aboral view of umbrella showing the four interradial pigmentary spots (P). Scale bars (in mm): 0.05 ( O, P); 0.1 (K–N); 0.3 (H, J); 0.5 (B, C, E–G, I); 1.0 (A, D).

FIGURE 1. Hermit crab inhabited shell colonized by hydroid (A). Shells with removed hermits to show the arrangement of the various polyps around their apertures (B, C). Group of gastrozooids (D), of which one (left) bears medusa buds. Gastrozooids with medusa buds (E, F), gonozooids (G, H). Newly-liberated (I, J), 1-day (K), 2-day (L, M), and 3-day-old (N–Q) medusae. Cnidome (R) of the gastro- (R1), gono- (R2), and tentaculozooid (R3), as well as of the medusa bud (R4). Scale bars: 10 µm (R), 300 µm (H–Q), 1 mm (D–G), 3 mm (A–C). Drawings by H.R.G. (B–G, I–R) and R.F. (A, H).

Tentaculozooids (Pl. 2D) are present in about 45% of the specimens inspected. Up to 16 of these slender structures may be scattered among each colony, though they differentiate mostly on their edges. They are very extensible (0.5–5.0 mm long) and arise from a broadened base given off from the perisarc meshwork, then taper gradually toward tips.

Newly liberated medusae are bell-shaped, approaching the globular, about 0.3 mm high and wide (Pl. 2L, M). The mesoglea is uniformly thin. An umbilical canal is present, but it is soon lost during growth. The exumbrella displays a moderate number of scattered nematocysts, and there is sometimes a slight apical depression (Fig. 1K). The manubrium is fusiform to tubular, extending to about halfway to velar aperture, and there is no peduncle. The mouth is simple, square when open wide (Fig. 1J), provided with four perradial, short lips crowded with fusiform nematocysts (PL. 2 O). There are four moderately narrow radial canals, a rather inconspicuous ring canal, and four perradial bulbs, each bearing a single filiform tentacle of equal development (Pl. 2N). Ocelli are absent and the velum is broad (Fig. 1L). No signs of gonad formation could be noted at this stage. Medusae raised for three days in natural conditions did not develop much compared to the newly-released ones. They attained about 0.5 mm in height and width, and their gonads were still not formed3.

In life, the body of gastrozooids is generally orange in color (Pl. 1G), though about 3% of the inspected colonies had polyps that exhibited various shades, ranging from dark brown to purple. However, their distal part, including an area below the origin of tentacles, these structures, and the hypostome, are always of a bright, white tinge (Pl. 1J, K). The gonozooids harbor the same colors as their feeding counterparts (Pl. 2F). The medusa buds are rendered conspicuous through the bright white coloration of the distal part of their tentacles, marginal bulbs, and the four interradial white spots on the manubrium (Pl. 2L–N, P). The tentacles of both the hydroid (Pl. 1K) and medusa exhibit a very characteristic, closely set, alternating light and dark banding pattern.

Nematocysts4: the categories of capsules occurring in the hydrorhiza, the various polyps and the medusa buds, together with their dimensions, are summarized in Table 1 . There are 3 size classes of microbasic euryteles in the polyps (small, medium sized, and large capsules), as well as an isorhiza5. The medusa buds are provided with medium sized microbasic euryteles (comparatively wider then those of the gastrozooids), large microbasic heteronemes6 (more fusiform than the euryteles of polyps), and desmonemes.

Remarks. One of the most striking features of Podocoryna martinicana is found in its gastrozooids, whose considerable number of tentacles, arranged in multiple closely set whorls, is rather uncommon within the family Hydractiniidae . Only a few taxa exhibit such a feature: up to 40 tentacles were reported in both Hydractinia minoi (Alcock, 1892) (see Hirohito 1988) and Hydractinia proboscidea (Hincks, 1868) (see Bouillon et al., 1997, as Hydractinia calderi sp. nov.); up to 50 in Schuchertinia epiconcha (Stechow, 1907) and Hydractinia spiralis (Goto, 1910) (for both, see Hirohito 1988); up to 60 in Hydrissa sodalis (Stimpson, 1858) (see Hirohito 1988); and up to 91 in Hydractinia multitentaculata Millard, 1975 (see original description). However, the gonozooids of H. sodalis bear fixed sporosacs, while those of S. epiconcha , H. multitentaculata , H. proboscidea , and H. spiralis produce medusoids. In contrast, H. minoi grows in association with scorpaeonid fishes, and its medusa buds are devoid of mouth and its associated appendages.

Based on the list of valid species of hydractiniid hydroids compiled by Schuchert (2013), and upon a thorough search of the relevant literature, it appears that only 22 taxa7 reproduce through free-living, feeding medusae. For comparisons of both their hydroid and medusa stages, see Table 2. Since only young, sexually immature medusae were obtained for P. martinicana , the differences to other species described exclusively from their pelagic stage are sometimes difficult to establish, mainly due to the scarcity of morphological features displayed, further confounded by the lack of data on their cnidome composition. However, the comparison is made easier when the hydroid is known and well documented.

3. An attempt to rear the medusa proved unsuccessful, as a significant decay was observed after three days.

4. The cnidome composition was examined in fixed material upon measurements of ca. 30 capsules of each type. The sizes given in Table 1 correspond to undischarged capsules. Only a few discharged nematocysts were seen, and no reliable size range could be provided for them at this time.

5. The extremely rare occurrence of isorhizas in the gastrozooids did not allow their type to be determined with certainty. Their presence in the cnidome recalls Bouillonactinia carcinicola (Hiro, 1939) . According to Namikawa (1997), up to 10 atrichous isorhizas could be found in each polyp of the Japanese hydroid. Spines on the shaft of the single discharged capsule observed in P. m art ini ca na were either absent or too inconspicuous to be noted, leading us to suspect that the nematocyst might be an atrichous isorhiza. However, the shape of undischarged capsules matches better the holotrichous isorhizas illustrated by Namikawa (1997) for the planula of B. carcinicola . The study of additional living material of the new species is expected to solve this issue.

6. Capsules with similar morphology were observed by Schuchert (2008) in the oral appendages of Podocoryna exigua (Haeckel, 1880) , and were identified as microbasic euryteles. No discharged nematocyst of this type could be found in our material, and their precise identification is pending.

7. Three of these, originally placed in Hydractinia van Beneden, 1841, viz. H. guangxiensis Huang et al., 2010 , H. moniliformis Huang et al., 2010 , and H. spiralis Lin et al., 2010 , are excluded from the following discussion, on account of several peculiar morphological features that contrast with the present concept of Podocoryna M. Sars, 1846 , as well as on the absence of data on their hydroid stages. Thus, H. guangxiensis has the tentacle tips crowded with 14–28 large nematocysts of unreported type (Li et al. 2010). The second and third species have moniliform (Li et al. 2010) and spirally twisted (Lin et al. 2010) tentacles, respectively, thus differing from the strictly filiform condition displayed by all species of Podocoryna medusae described so far. In addition, the occurrence of all three nominal species in the Taiwan Strait, set them apart from P. martinicana .

Unlike P. dubia (Mayer, 1900) , P. ocellata (Agassiz & Mayer, 1902) , P. uniformis (Stampar et al., 2006) , and P. vacuolata (Xu & Huang, 2006), the medusae of P. martinicana are devoid of ocelli. When set free, they always bear four well developed marginal tentacles, in contrast to the following species, in which their number is increased: P. americana (Mayer, 1910) , P. anechinata 8 Ritchie, 1907, P. areolata (Alder, 1862) , P. australis Schuchert, 1996 , P. b e l l a Hand, 1961, P. borealis (Mayer, 1900) , P. carnea M. Sars, 1848 , P. hayamaensis Hirohito, 1988 , and P. tenuis (Browne, 1902) 9. In addition, a number of differences in their hydroid stage (when known) are listed in Table 2.

Three species, namely P. a p i c a t a Kramp, 1959b, P. dongshanensis (Xu & Huang, 2006), and P. exigua (Haeckel, 1880) , possess medusae that are liberated and retain, during their whole life, only four tentacles10. The former, whose hydroid stage is unknown, is characterized by the presence of a distinct gastric peduncle and of a mouth provided with four simple arms. No such structures were observed in our 3-day old medusae of P. martinicana , though they may possibly develop subsequently. However, the remote geographical distribution of Kramp's species suggests that it is most probably distinct from ours. The hydroid of P. dongshanensis is equally unknown to allow establishing a comparison with that of P. martinicana , though the occurrence of its medusa in the Taiwan Strait, together with the presence of a black pigment in its tentacle bulbs, set it apart from the Caribbean species. Finally, the colonies of the European P. e x i g u a may occasionally form spines and spiral zooids (neither observed in our species), its gastrozooids are provided with only 10–13 tentacles, and the cnidome of the polyp includes desmonemes instead of isorhizas (Schuchert 2008).

Podocoryna meteoris Thiel, 1938 , described from a single medusa caught in Cape Verde, is provided with eight marginal tentacles, its manubrium buds off young medusae, and ends in twelve oral arms. No medusa budding was ever noted in the rather young medusae of P. martinicana , and the differences related to the marginal tentacles and the number and type of oral appendages may be diagnostic.

8. The tentacle number was not clearly stated by Ritchie (1907). On one hand, he explained that "During the earlier stages the tentacles appear as four blunt knobs, but these develop considerably ere the medusoid is set free". On the other hand, six tentacles are visible in his Pl. 23 Fig. 9. Rees & Thursfield (1965) hypothesized that Ritchie's material might belong to Podocoryna carnea M. Sars, 1848 , though they were unable to demonstrate it unambiguously.

9. Several Chilean specimens described earlier by one of us (Galea 2007) were reexamined for this study. Their tentacle number varies between 4 and 8, and all bear medusa buds on their manubria. Although quite difficult to observe in fixed material, the more developed medusa buds appear provided with 5–8 tentacles. Consequently, we assume that the newly liberated medusae produced either sexually or asexually must bear 4–8 tentacles.

10. This situation is not excluded from occurring in P. martinicana , taking into account that its tentacles are already well developed at liberation, and no signs of additional, interradial marginal bulbs and tentacles are present.

In addition, mainly due to geographical reasons, P. martinicana is most probably assumed to be different from P. polytentaculata (Xu & Huang, 2006), and P. recurvata (Lin et al., 2010) 11, both from the Taiwan Strait. Furthermore, the former species has the endoderm of the marginal bulbs crowded with a dark pigment, while the tentacle tips of the latter are reportedly swollen.

Last but not least, the conspicuous bright pigmentation of the tentacles and hypostome of polyps, and that of the distal half of marginal tentacles of the medusa, together with the four white, interradial, manubrial spots, were never reported, to our knowledge, in any other hydractiniid described so far.

Biology. Colonies of P. martinicana were exclusively found on gastropod shells inhabited by Iridopagurus caribbensis (A. Milne-Edwards & Bouvier, 1893) . Examination of more than 100 shells gathered at 7 distinct stations (some up to 40 km distant), showed that about 5% of them were not colonized by the hydroid, being very small (apertures less than 2.5 mm high) and inhabited by young crabs.

Unlike other hydractiniid species, in which the colonies recover most of the host shell surface and have the various polyps scattered more or less homogenously throughout, the organizational pattern of both gastro- and gonozooids of P. martinicana is unique and invariant amongst specimens, regardless the origin of the shell inhabited by the hermit. Thus, a few gastrozooids are lined up along the inner lip of the shell. Their size is in accordance with their position along the lip: the centrally placed polyps are the tallest, while those placed laterally are gradually smaller (Pl. 1F, G, Pl. 2A). In contrast, all gonozooids exhibit a uniform height, and they dress a line nearly exclusively on the outer lip of the shell (Pl. 1G, H, L, Fig. 1B). Due to the numerous gonophores they carry, they are most often bent alternately forward and backward, thus optimizing the availability of space between them. In addition, it is likely that the specific occurrence of the gonozooids on the outer lip of the shell prevents potential damage of the fragile medusa buds when the crab burrows in sand (see also below and Pl. 1A).

New hydroid colonies develop first on the inner lips of recently acquired shells, regardless their shape and size. They are composed of a few gastrozooids, of which those placed more laterally may occasionally develop medusa buds (Pl. 2A, Fig. 1D). These fertile zooids are provided with fewer, almost normally developed tentacles (Pl. 2B, C), and represent an intermediate stage between the truly feeding polyps and their generative counterparts. During the growth of the hydroid colony, the stolonal web progresses from a periderm-covered, more or less reticulate hydrorhiza, to a nearly fully coalescent plate investing the inner lip of the host shell (Pl. 1F, Fig. 1B). In only a few instances, the ectoderm at the base of polyps was observed to grow, to a varied extent, over the net of stolons, producing a sheet of naked coenosarc. Otherwise, the perisarc is practically never overlaid with coenosarc. On the other hand, the basal stolonal network extends towards the edge of the outer lip, forming a mat-like expansion beyond the shell aperture, the stolons there being mostly parallel and adnate. Consequently, the aperture of the shell may be increased, up to a couple of millimeters, providing a broader surface area to protect the hermit.

As to the characteristic position of the gastrozooids in the closest vicinity of the buccal apparatus of the crab (Pl. 1D, Fig. 1A), preliminary observations suggest that it might potentially reflect a two-way relationship. On one hand, the crab lays pieces of food12 on the polyp's hypostome, allowing it to take and ingest them. On the other hand, the crab gently "squeezes" the hydroid body, pushing it to regurgitate the digested food that, in turn, is ingested at once by the crab. It therefore appears that, at least in some circumstances, the hydroid serves as a food storage device for the hermit crab. In addition, there is evidence that the gastrozooids are possibly not capable of catching food by themselves. Indeed, hydroid colonies deprived of their pagurid host and cooped up in perforated jars, totally disappeared after three days in natural conditions.

Compared to other congeners (see Table 2), the absence of desmonemes from the cnidome of gastrozooids of P. martinicana is striking. Indeed, these nematocysts were shown to play an important role in the adhesion to, and the entanglement of prey (Östman et al. 1991). In our case, their absence could be correlated with the nearly permanent contact between the gastrozooids and the hermit, thus possibly preventing their tentacles from adhering to the host. On the other hand, the numerous euryteles from the tentacles seem to not have any deleterious effect on the crab, in contrast with those species of hermits that avoid acquiring shells invested by hydroid colonies due to their apparent sensitiveness to the sting (Brooks & Mariscal 1985).

Upon stressful situations for the crab (e.g. voluntary mechanical perturbation), it characteristically leaps up 11. Podocoryna is a feminine noun, and the original specific epithet recurvatus should be replaced by the correctly spelled recurvata .

12. Since the crabs exhibit very often a quarrelsome behavior, especially when several specimens occur together (as it usually happened during the sampling), pieces of chelipeds and legs are often procured from their defeated congeners, and offered to the hydroid. Large pieces of ingested food may be seen through the body of gastrozooids (Pl. 1H), and are clearly revealed upon dissection of the polyps.

backwards, making considerable jumps, up to 10 times its size. Upon a prolonged stress, it adopts two choices: it either draws into its shell, the gastrozooids forming a gate obstructing the shell aperture, or it buries in sand, leaving only its eyes, antennae, and the gonozooids protruding at surface. There is no actual evidence for an active role for the gastrozooids of P. martinicana in the defense of its host crab from potential predators. Within some symbioses, however, hydroids have been shown to either protect their host by deterring predators of hermits, or by deterring other crab species from using the same shells in order to minimize interspecific shell competition (summarized by Damiani 2003). Additional observations are therefore needed in order to document in a more comprehensive manner the nature of the symbiosis between P. martinicana and its host.

Etymology. The specific name refers to Martinique, the Caribbean island from which the material described herein originates.

Tables

TABLE 1. Cnidome of Podocoryna martinicana sp. nov. (dimensions are given in µm). The occurrence of nematocysts ranges from rare (+), to average (++), to abundant (+++).

	Small microbasic euryteles	Medium sized microbasic euryteles	Large microbasic euryteles	Isorhizas	Fusiform microbasic heteronemes	Desmonemes
Gastrozooid	(7.4–8.7) × (2.7–3.6) [+++, tentacles, hypostome]	absent	(11.7–12.9) × (4.1– 4.5) [+++, tentacles, hypostome]	(5.3–5.5) × (2.6– 2.9) [+, column]	absent	absent
Gonozooid	absent	absent	(11.0–12.2) × (3.7– 4.4) [+++, tentacles, column]	(5.3–5.7) × (2.7– 3.0) [++, column]	absent	absent
Tentaculozooid	absent	(9.4–10.3) × (3.6–3.9) [+++]	(11.7–12.9) × (4.5– 4.8) [+++]	(5.3–5.7) × (2.6– 2.9) [+++]	absent	absent
Gonophore	absent	(8.3–9.0) × (3.9–4.5)	absent	absent	(11.5–13.1) × (2.9–3.2)	(6.5–6.9) × (4.1–4.5)
Stolon	absent	absent	(11.3–13.3) × (4.0– 4.8) [+++]	absent	absent	absent