NOTES AND NEWS

OCCURRENCE OF THE GUINEAN SPECIES NITIDA MANNING & HOLTHUIS, 1981 (, BRACHYURA) IN A MEDITERRANEAN SUBMARINE CAVE AND A COMPARISON WITH THE CONGENERIC H. CONDYLIATA (FABRICIUS, 1787)

BY

FRANCESCO DENITTO1,3), MICHELE PASTORE2) and GENUARIO BELMONTE1) 1) Laboratorio di Zoogeografia e Fauna, Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento, I-73100 Lecce, Italy 2) Istituto per l’Ambiente Marino Costiero, Sez. Talassografico, CNR, Taranto, Italy

INTRODUCTION Marine caves represent a peculiar habitat, characterized by particular environ- mental conditions that strongly affect the distribution of many species (Riedl, 1966; Bianchi et al., 1996). The reduced light intensity and the presence of many shel- ters on the rocky substrate over 360◦ (bottom, walls, and vault of the cave), make submarine caves an elective refuge for many benthonic that are tra- ditionally considered a sciaphylous group (Gili & Macpherson, 1987; Pessani & Manconi, 1994; Manconi & Pessani, 2003; Denitto et al., 2009). Among the vagile benthic fauna, many species of Decapoda are found in these habitats (for a recent review, see Manconi & Pessani, 2003) but from a general point of view, scientific literature referring to decapods that occur in submarine caves is still scanty. The present study focuses on Mediterranean belonging to the genus Herbstia, and describes the two species at issue coexisting in a shallow submarine cave in south-east Italy. One of these, H. nitida Manning & Holthuis, 1981, was originally described from coastal waters of the Gulf of Guinea (cf. Manning & Holthuis, 1981), and is a species only recently recorded from the Mediterranean basin (Pas- tore & Denitto, 2002).

MATERIAL AND METHODS The site under study is the shallow marine cave “Grotta di Ciolo”, located near Capo di Leuca (southern Apulia, S.E. Italy, Mediterranean Sea, 39◦5038N

3) Corresponding author; e-mail: [email protected] © Koninklijke Brill NV, Leiden, 2010 Crustaceana 83 (8): 1017-1024 Also available online: www.brill.nl/cr DOI:10.1163/001121610X513685 1018 NOTES AND NEWS

Fig. 1. Location of the submarine cave “Grotta di Ciolo” in the Puglia [= Apulia] Region, southeastern Italy.

18◦2311E) (fig. 1). This was explored by SCUBA divers to collect vagile fauna samples in April, May, and June 2002. The cave is a horizontal blind tunnel more than 120 m long (Onorato et al., 1999). The bottom near the entrance is covered with pebbles, while that at 40-120 m from the entrance is sandy-muddy. The cave system is constantly supplied by hypogean freshwater. Vertical profiles of irradiance, salinity, conductivity, and temperature were determined seasonally for one year by using a multiparameter portable probe at several locations inside the cave (at 0, 25, 50-75 m horizontal distance from the entrance). All decapods were collected with an aquarium net or by hand, preserved in 70% ethanol, and deposited at the I.A.M.C. Sezione Talassografico, CNR (Taranto, Italy). The specimens collected were measured and identified under a stereomicroscope. The abbreviation CL is used for carapace length. NOTES AND NEWS 1019

RESULTS

The temperature of the sampled water layer ranged from a minimum of 14.7◦C in winter to a maximum of 23.9◦C in summer. Depending on seasonal differences in runoff, salinity ranged from 35.6 ppt in winter to 39.3 ppt in summer. The innermost station was found to be the least variable for temperature, and the most for salinity. The progressive (from the entrance to the innermost part of the cave) light extinction is seen throughout all seasons and a dark zone exists starting from about 50 m from the lighted entrance (table I). A total of thirteen species of Decapoda was collected in the cave: Steno- pus spinosus Risso, 1826, Gnathophyllum elegans (Risso, 1816), Palaemon ele- gans Rathke, 1837, Palaemon longirostris H. Milne Edwards, 1837, Palaemon serratus (Pennant, 1777), Palaemon xiphias Risso, 1816, Lysmata seticaudata (Risso, 1816), Dromia personata (Linnaeus, 1758), Ilia nucleus (Linnaeus, 1758), Achaeus cranchii Leach, 1817, Macropodia rostrata (Linnaeus, 1761), Herbstia condyliata (Fabricius, 1787), H. nitida Manning & Holthuis, 1981, and Xantho pilipes A. Milne-Edwards, 1867. In the present study, we focused our attention on the two species belonging to the genus Herbstia.

Herbstia condyliata (Fabricius, 1787) (figs. 2-3)

Material examined. — Three  (22.5-40.0 mm CL), 1  (17.0 mm CL), 1  ovigerous (29.0 mm CL), 2  juv. (12.5; 12.8 mm CL), 4  juv. (11.0-13.8 mm CL). Deposited in the I.A.M.C. Sez. Talassografico, CNR — Taranto (Italy).

TABLE I Seasonal variation of the physico-chemical parameters of the water at the three stations investigated (average data, ENT = cave entrance (0 m); INT = intermediate position (25 m); INN = the inner portion of the cave (50-75 m)). From Moscatello & Belmonte (2007), modified

Abiotic parameters Autumn Winter Spring Summer ENT INT INN ENT INT INN ENT INT INN ENT INT INN ◦ Temp. [ C] 18.618.818.814.714.815.015.815.916.023.923.923.5 Conductivity − [mS cm 1]49.749.649.245.344.943.547.547.445.957.557.556.8 pH 8.38.28.18.38.28.08.28.28.18.28.28.1 Salinity [ppt] 37.737.537.237.437.135.638.438.336.939.337.137.4 Photosynthetically Active Radiation − [μWcm 2] 2322 658 0 2441 1072 0 2060 595 0 2755 1116 0 1020 NOTES AND NEWS

Fig. 2. Herbstia nitida Manning & Holthuis, 1981, male, CL 13.0 mm (adult, at right) and an H. condyliata (Fabricius, 1787) female, CL 13.8 mm (juv., at left).

Remarks. — Herbstia condyliata is apparently the most common European species of the genus (Guerao et al., 2008). It can readily be distinguished from its two Atlantic congeners, H. nitida and H. rubra A. Milne-Edwards, 1869 by its larger size, prominently spinulose carapace with the regions well defined, and the presence of a trilobate projection on the posterior margin of the carapace. The smaller specimens collected in the “Grotta di Ciolo”, both male and female (figs. 2, 3) have the characteristic three posterior lobes, though the spinulation of the carapace is rudimentary like in the specimen figured by Manning & Holthuis (1981) (specimen from Spain, CL 10.8 mm, their fig. 79c). There are many previous records of H. condyliata collected inside Mediter- ranean submarine caves (Ledoyer, 1968; Gili & Macpherson, 1987; Grippa, 1993; Pessani & Manconi, 1994; Arko-Pijevac et al., 2001). Finally, Manconi & Pessani (2003) reported its presence in a recent review from seven Italian marine caves on the Tyrrhenian coast. NOTES AND NEWS 1021

Fig. 3. Herbstia nitida Manning & Holthuis, 1981, male, CL 13.0 mm (adult, at right) and an H. condyliata (Fabricius, 1787) female, CL 12.5 mm (juv., at left).

Our adult specimens were collected while they were walking on the cave walls, 100 m from the entrance (sector “INN” in table I), while the juveniles were collected under pebbles, at 20-35 m from the entrance (“INT” in table I).

Herbstia nitida Manning & Holthuis, 1981 (figs. 2-3)

Material examined. — Two  (13.0; 13.2 mm CL), 2  (10.0; 13.0 mm CL). Deposited in the I.A.M.C. Sez. Talassografico, CNR — Taranto, Italy. Descriptive notes. — Carapace pyriform, smooth, and cream-coloured, mottled with rust. Two short rostral spines, pre-orbital and post-orbital spines also short. Hepatic region with three or four sharp tubercles, gastric region with three low tubercles in transverse line, cardiac and intestinal regions each with a single low dorsal tubercle. Posterior median margin of carapace with a single projection. Cheliped, as long as carapace, not greatly enlarged in males, merus and carpus 1022 NOTES AND NEWS with many low tubercles, chela smooth. Meri of walking legs bristly, with orange- coloured transversal bands. Posterior margin of dactyli with 1-4 triangular teeth. Remarks. — Manning & Holthuis (1981), reported the male CL in the range of 5.9-8.8 mm, and female CL as 6.1-10.0 mm, but the specimens of the present study are larger. The specimens collected in the submarine cave “Grotta di Ciolo” represent the first occurrence of H. nitida in the Mediterranean basin. Its discovery was already reported in the CIESM Atlas (Galil et al., 2002) but without any information on its identification and/or discussion on the presence outside of its type area. However, scanty information on its distribution is available. It is known from its type locality, Annobon Island, and other islands in the Gulf of Guinea, where it was found at depths between 9 and 55 m, among calcareous algae (Manning & Holthuis, 1981). We found the four specimens at the semi-dark zone of the cave (“INT” in table I), 20-35 m from the entrance, under the pebbles on the bottom, 3 m below sea level, together with juveniles of H. condyliata.

DISCUSSION Herbstia nitida and H. condyliata both have a pyriform carapace. Nevertheless, H. nitida differs from H. condyliata by its smaller size, smoother carapace, its single median posterior lobe on the carapace, and through the less prominent lateral spines. In addition, in H. nitida the walking legs are slender and long; the fifth leg is longer than the carapace. Finally, in H. nitida, the adult male chelipeds are not greatly enlarged. Besides all other morphological differences, and according to Manning & Holthuis (1981), H. nitida would occur at its type-locality (Annobon Island), at 9-55 m below sea level, in beds of calcareous algae and elsewhere in the Gulf of Guinea (eastern Atlantic Ocean) in such beds on offshore islands, while H. condyliata is typical for the continental shelf. Although the decapod Crustacea of Mediterranean marine caves have been studied by several authors (Gili & Macpherson, 1987; Grippa, 1993; Pessani & Manconi, 1994; Arko-Pijevac et al., 2001; Manconi & Pessani, 2003; Denitto et al., 2009), literature about the crabs inhabiting these biotopes is very scattered and scanty. As regarding the presence of H. nitida in the Mediterranean Sea, after the recent first record (Pastore & Denitto, 2002), the species has been included in the “list of exotic species” in the CIESM Atlas of exotic species in the Mediterranean (Galil et al., 2002). Accordingly, it should be considered an invader species coming from the western tropical Atlantic, where it was previously found (Manning & Holthuis, 1981). Its introduction into the Mediterranean Sea could NOTES AND NEWS 1023 be the result of recent human activities. Shipping appears to be the major vector of introduction (excluding Lessepsian migration, Onofri et al., 2009), and zoobenthos appears to be, by far, the dominant group, comprising about 57% of the newcomers (Streftaris et al., 2005). Finally, we cannot exclude the alternative hypothesis that Herbstia nitida was simply missed in the past. The small size of the adults may have led to confusion with juvenile specimens belonging to the congeneric and well known H. condyliata. This could be the main reason why it has been overlooked in the Mediterranean basin, until now.

ACKNOWLEDGEMENTS We would like to thank Prof. B. S. Galil (Oceanographic and Limnological Research, Haifa, Israel), and Prof. M. Türkay (Senckenberg Natural History Museum and Research Institute, Frankfurt am Main, Germany) for their valuable comments to improve this paper. We would also like to thank the divers of the Speleological Submarine Centre “Apogon” (Nardò, Italy) for their assistance during cave diving.

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First received 24 July 2009. Final version accepted 27 May 2010.