Crustacea:Amphipoda:Caprellidea - Universidad de Sevilla

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collected from sandy bottoms in the Strait of Gibraltar .... refers to the closest species Caprella rapax. ... cent molar flake. ... Penes rounded, situated laterally.

Hydrobiologia 448: 181–192, 2001. © 2001 Kluwer Academic Publishers. Printed in the Netherlands.

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Two new species of Caprella (Crustacea:Amphipoda:Caprellidea) collected from sandy bottoms in the Strait of Gibraltar J. M. Guerra-Garc´ıa, J. E. S´anchez-Moyano & J. C. Garc´ıa-G´omez Laboratorio de Biolog´ıa Marina, Departamento de Fisiolog´ıa y Biolog´ıa Animal, Facultad de Biolog´ıa, Universidad de Sevilla, Apdo. 1095, E-41080, Sevilla, Spain E-mail: [email protected] Received 6 July 2000; in revised form 16 January 2001; accepted 7 February 2001

Key words: Caprellidea, Caprella, new species, sandy bottoms, Strait of Gibraltar

Abstract Two new species of the genus Caprella (Crustacea:Amphipoda:Caprellidea) are described based on specimens collected from the Strait of Gibraltar (Southern Spain and Northern Africa). Both species were found living in sandy bottoms. Caprella pseudorapax n. sp. is very close to the species C. rapax (Mayer, 1890) and C. lilliput (Krapp-Schickel & Ruffo, 1987). Caprella sabulensis n. sp. resembles C. cavediniae (Krapp-Schickel & Vader, 1998).

Introduction During the last 10 years, the Laboratorio de Biología Marina of the University of Sevilla has been developing research programmes on benthic animal communities living in soft bottoms from the Strait of Gibraltar. The first research projects were conducted in Algeciras Bay, Southern Spain, where only 3 species of the Caprellidea were found living in sediment, i.e. Pariambus typicus (Kröyer, 1844), Phtisica marina (Slabber, 1769) and Pseudolirius kröyeri (Haller, 1897) (Estacio, 1996). The most recent studies have focused on the coastline Algeciras-Tarifa, Iberian side of the Strait of Gibraltar, and on the littoral of Ceuta, North African side of the Strait. The coastline Algeciras-Tarifa is the subject of a project leading to give this zone a protection status as a Natural Park. This coastal area exhibits an abundant biodiversity in both terrestrial and marine environments, with extensive well preserved areas. The topography of the seabottom provides a high diversity of environmental conditions (sand, rock, caves...), which allows the existence of many different species of plants and animals. The strong winds and currents

provide an important nutrient supply and renewal. The coast of Ceuta is also being studied to establish the current state of the marine biodiversity of this area. As a result of this monitoring programme, several specimens of the genus Caprella were collected from sandy bottoms of the Strait of Gibraltar. Detailed examination revealed that these specimens belong to two new species, here described as Caprella pseudorapax n. sp. and C. sabulensis n. sp.

Materials and methods Benthic sediment samples were collected with a Van Veen grab (0.05 m2 ). The samples were sieved through a 0.5 mm sieve and infauna was preserved in 5% buffered formalin containing Rose Bengal solution to ease sorting. Granulometry of the sediment was determined by Buchanan and Kain’s method (Buchanan & Kain, 1984). Sediment organic matter (%) was analysed by ashing to 500 ◦ C (mean value for 3 replicates per sample) of subsamples of sediment previously dried at 100 ◦ C during 24 h. For a microscopical study, caprellid specimens were dissected under a stereomic-

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Figure 1. Caprella pseudorapax n. sp. Lateral view: (a) male; (b) female. Scale bar: 1 mm.

roscope. Permanents mounts were made in polyvinyl lactophenol. All figures were drawn with the aid of a camera lucida.

Results Family Caprellidae White, 1847; Genus Caprella Lamarck, 1801 Caprella pseudorapax n. sp. (Figs 1–4). Type material: Holotype male, 4.47 mm in length, from sandy bottoms, found on Tarifa (36◦ 02.093 N, 5◦ 30.491 W), Cádiz, Spain, July 2000, 20 m in depth. Allotype female, 2.2 mm, from Tarifa (36◦ 01.781 N, 5◦ 30.630 W), July 2000, 30 m in depth. Paratypes: 1 male, 2.5 mm, collected together the holotype; 1 male, 2.3 mm, and 1 female, 2.1 mm, collected together the allotype. The holotype male and the allotype female has been deposited in the Museo Nacional de Ciencias Naturales de Madrid, Spain (holotype: MNCN 20.04/4657, allotype: MNCN 20.04/4658). Paratypes have been deposited in the Laboratorio de Biología Marina of the University of Sevilla, Spain.

Diagnosis (based on adult males): Body smooth, eyes reduced to 6–8 ocelles. Antenna 1 a little shorter than a half body-length. Basis of gnathopod 2 with the same length than pereonite 2. Palm with 1 large acute tooth, followed by a deep concavity filled with a membranous sac, defined distally by another tooth. Dactylus distally widened. Branchial lobes with serrated margin in anterior half. Pereopods 5–7 carring 1 smooth grasping spine situated on the anterior half of the propodus palm. Abdominal appendages 2-articulate, distal article about 4 times longer than proximal one. Description Holotype male Body length 4.47 mm Lateral view: Body smooth. Head lacking rostrum. Eyes reduced to eight ocelles. Pereonites 3 and 4 with pleura. Gills elongated, with serrated margin in anterior half. Peduncle short. Antennae: Antenna 1 shorter than half bodylength. Flagellum 4-articulate. Antenna 2 with the same length than the first 2 peduncular articles of antenna 1.

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Figure 2. Caprella pseudorapax n. sp. (a–d) Male: (a) antenna 1; (b) antenna 2; (c) gnathopod 1; (d) gnathopod 2. (e) Female gnathopod 2. Scale bars: A: 0.3 mm (a, b); B: 0.2 mm (c); C: 0.2 mm (d); D: 0.2 mm (e).

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Figure 3. Caprella pseudorapax n. sp. (a–e) Male: (a) pereopod 5; (b) pereopod 7; (c) gill 3; (d) gill 4; (e) abdomen. (f) Female abdomen. Scale bars: A: 0.3 mm (a, b); B: 0.3 mm (c, d); C: 0.1 mm (e, f).

Mouthparts: Upper lip semicircular, symmetrically bilobed, pubescent apically. Outer lobes of the lower lip with a medial cleft. Incisor 5-toothed, lacinia mobilis 4-toothed. A row of 3 plumose setae on left mandible and 2 on the right one. Maxilla 1 outer lobe with 5 forked spines distally. Palp with 2 articles, the distal one with 4 spines on end and 2 on the ventral surface. Maxilla 2 inner and outer lobes subequal, both of them carrying simple setae on end. Inner lobe, also, with 1 plumose setae. Inner and outer plates of maxilliped with the same length. Inner plate carrying 3 teeth and 4 plumose setae on apical margin. Outer plate carrying 1 big tooth and 2 simple setae. Palp 4-articulate, not very setose. Gnathopods: Basis of gnathopod 1 shorter than ischium to carpus combined. Propodus 2 times longer than carpus, length ca. 2 times width, palm defined by one long spine. Dactylus distally bifid. Gnathopod 2 inserted in the posterior half of pereonite 2. Basis, with

the same length than pereonite 2, provided with a little serrated carine on proximal dorsal margin. Ischium cylindrical, merus slender proximally, wide distally. Palm of propodus with 1 large acute tooth, followed by a deep concavity filled with a membranous sac, defined distally by another tooth. Dactylus distally widened. Pereopods 5–7 (pereopod 6 missing in holotype but present in paratypes) increasing in length but with the same morphology, carrying 1 smooth grasping spine on the anterior half of the propodus palm. Penes situated laterally. Abdomen with a pair of appendages, a pair of lateral lobes and a single dorsal lobe. Abdominal appendages 2-articulate. Distal article ca. 4 times longer than proximal one.

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Figure 4. Caprella pseudorapax n. sp. Male: (a) upper lip; (b) lower lip; (c) maxilliped; (d) left mandible; (e) right mandible; (f) maxillae 1; (g) maxillae 2. Scale bars: 0.1 mm. A (a, b); B (c); C (d, e, f, g).

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Figure 5. Caprella sabulensis n. sp. Lateral view: (a) male; (b) female. Scale bar: 1 mm.

Allotype female Body length 2.2 mm. Gnathopod 2 inserted in the middle of pereonite 2. Propodus palm of gnathopod 2 straight, with 3 teeth. Dactylus curved. Carpus and merus subequal. Abdomen with a pair of lateral lobes and a single dorsal lobe. Etymology: The specific name, pseudorapax, refers to the closest species Caprella rapax.

Caprella sabulensis n. sp. (Figs 5–8). Type material: Holotype male, 5.35 mm in length, from sandy bottoms, found on Tarifa (36◦ 02.093 N, 5◦ 30.491 W), Cádiz, Spain, July 2000, 20 m in depth. Allotype female, 3.93 mm, collected together with the holotype. Paratypes: 2 males, 3.83 and 4 mm; 1 female, 3.5 mm; 2 juveniles, 2.83 and 3.16 mm, collected together the holotype; 1 premature female, 3.29 mm, found on Tarifa (36◦ 01.781 N, 5◦ 30.630 W), Cádiz, Spain, July 2000, 30 m in depth; 1 male, 4.22 mm, found on Ceuta (35◦ 53.5 N, 5◦ 19 W), Spain, August 2000, 5 m in depth.

The holotype male and the allotype female has been deposited in the Museo Nacional de Ciencias Naturales de Madrid, Spain (MNCN 20.04/4659). Paratypes have been deposited in the Laboratorio de Biología Marina of the University of Sevilla, Spain. Diagnosis (based on adult males): Body smooth. Pereonite 3 the longest. Propodus palm of gnathopod 2 straight or slightly concave, defined by a tooth and a pair of strong proximal spines. Dactylus thickened medially. Pereopod 5 without grasping spines. Abdominal appendages 1-articulate. $ESCRIPTION Holotype male Body length 5.35 mm Lateral view: Body smooth. Head lacking rostrum. Pereonite 3 the longest. Gills elongated, length ca. 3 times width. Antennae: Antenna 1 about 2/3 of body length. Flagellum 12-articulate. Antenna 2 shorter than a half of antenna 1.

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Figure 6. Caprella sabulensis n. sp. (a–d) Male: (a) antenna 1; (b) antenna 2; (c) gnathopod 1; (d) gnathopod 2. (e) Female gnathopod 2. Scale bars: A: 0.5 mm (a, b); B: 0.3 mm (c); C: 0.5 mm (d); D: 0.23 mm (e).

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Figure 7. Caprella sabulensis n. sp. (a) Female pereopod 5; (b) Female pereopod 7; (c) Male abdomen; (d) Female abdomen. Scale bars: A: 0.5 mm (a, b); B: 0.2 mm (c, d).

Mouthparts: Upper lip symmetrically bilobed, densely pubescent apically. Lower lip densely pubescent. Proximal projections of outer lobe slender, well-marked. Incisor 5-toothed, lacinia mobilis 4toothed. A row of 3 plumose setae on left mandible and 2 on the right one. Rigth mandible with a pubescent molar flake. Maxilla 1 outer lobe with 6 forked spines distally. Palp with 2 articles, the distal one with 4 spines on end and 4 longer ones on ventral surface. Maxilla 2 outer lobe, a little longer than inner lobe, carrying simple setae on distal end. Inner lobe with simple setae distally and 5 plumose setae laterally. Inner plate of maxilliped, wider than outer plate, carrying 2 small teeth and several plumose setae. Outer plate with 1 tooth. Palp 4-articulate. Gnathopods: Basis of gnathopod 1 with the same length than ischium to carpus combined. Propodus 3 times longer than carpus, length ca. 3 times width. Palm minutely serrated, carrying 2 proximal grasping spines. Dactylus distally bifid. Gnathopod 2 inserted in the middle of pereonite 2. Basis ca. 0.6 times pereon-

ite 2 in length. Palm of propodus slightly concave defined by a tooth and a pair of strong proximal spines. Dactylus thickened medially. Pereopods missing in holotype. Penes rounded, situated laterally. Abdomen with a pair of appendages, a pair of lateral lobes and a single dorsal lobe which carries 2 plumose setae. Abdominal appendages 1-articulate, smooth. !LLOTYPE FEMALE Body length 3.93 mm. Gnathopod 2 inserted in the anterior half of pereonite 2. Propodus palm of gnathopod 2 straight with 3 spines proximally. Dacylus not thickened. Pereopod 5 without grasping spines. Pereopod 7 with a pair of grasping spines. Perepod 6 missing in allotype female. Abdomen with a pair of lateral lobes and a single dorsal lobe carrying 2 long plumose setae and 2 short simple ones.

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Figure 8. Caprella sabulensis n. sp. Male: (a) upper lip; (b) lower lip; (c) maxilliped; (d) right mandible; (e) left mandible; (f) maxillae 1; (g) maxillae 2. Scale bars: A: 0.2 mm (a, b); B: 0.2 mm (c); C: 0.1 mm (d, e, f, g).

190 Table 1. Comparison of selected characteristics between C. lilliput (Krapp-Schickel & Ruffo, 1986), Caprella rapax (Mayer, 1890) and Caprella pseudorapax n. sp. Features are taken from Krapp-Schickel & Ruffo (1986) for C. lilliput and Mayer (1890), Cavedini (1982) and Krapp-Schickel (1993) for C. rapax. Comparison is based on male specimens except female gnathopod 2

Body length Eyes Antenna 1 Antenna 2 Basis of gnathopod 2 Gills Pereopods

Inner lobe of maxilliped Abdominal appendages

Female gnathopod 2

C. lilliput

C. rapax

C. pseudorapax

2 mm Reduced to 3 ocelles Longer than half body length Same length as peduncular articles 1–2 of antenna 1 Shorter than pereonite 2 Smooth margin. Large and wide peduncle 2 grasping spines in pereopod 5, the long harpoon-shaped. Spines are lacking in pereopod 6 and 7 Not described Distal article ca. 4 times longer than proximal one

3.7–7 mm Not very reduced Longer than half body length Shorter than peduncular articles 1–2 of antenna 1 Longer than pereonite 2 Smooth margin. Short peduncle 2 smooth grasping spines in pereopod 5, lacking in pereopod 6 and 7

2.3–4.47 mm Reduced to 6–8 ocelles Shorter than half body length Same length as peduncular articles 1–2 of antenna 1 Same length as pereonite 2 Serrated margin in anterior half. Short peduncle 1 smooth spine in pereopods 5, 6 and 7

2 teeth Distal article 1.5 times longer than proximal one

2 grasping spines

2 grasping spines

3 teeth Distal article more than 4 times longer than proximal one 3 grasping spines

Etymology: The specific name sabulensis is from Latin Sabulum that means ‘sand’, referencing to the habitat of this species which lives in sandy bottoms.

Discussion Since Mayer’s monograph on the world Caprellidea from the Siboga Expedition (Mayer, 1903) little work has been done with caprellids living in sediments from the Strait of Gibraltar. The caprellid fauna in this area is of special taxonomic interest since the Strait is situated between the Mediterranen Sea and the Atlantic Ocean. In general, the studies of the Caprellidea from this zone have focused mainly on caprellid species collected from algae and hydroids (Sánchez-Moyano et al., 1995a, b) and specific researches on caprellids from soft bottoms were lacking. This is clearly demonstrated by the fact that general sediment sampling programmes lead to the discovery of such new species as Caprella pseudorapax n. sp. and C. sabulensis n. sp., described in the present paper. Caprella pseudorapax n. sp. is very close to the species C. rapax (Mayer, 1890). But it also shares several characteristic with C. lilliput (Krapp-Schickel & Ruffo, 1986). Detailed figures of the mouthparts from C. lilliput and C. rapax are lacking so a complete com-

parison between C. pseudorapax and these two close species is not possible. Nevertheless, C. pseudorapax can be easily differentiated from these species by the presence of a single grasping spine in pereopods 5–7. In C. rapax and C. lilliput, the grasping spines, a pair, are present only in pereopod 5 (see Table 1). The three species, C. rapax, C. lilliput and C. pseudorapax are, so far, Mediterranean endemisms. Caprella rapax and C. lilliput have been found in the Tyrrhenian Sea, Italy [C. rapax: Napoli (Mayer, 1890), Livorno (Cavedini, 1982); C. lilliput: Ischia (KrappSchickel & Ruffo, 1986)] while C. pseudorapax lives in the Strait of Gibraltar (Fig. 9). Further studies of the Caprellidea from soft bottoms could, however, modify this distribution. Caprella sabulensis, n. sp. has been found on both sides of the Strait of Gibraltar, Southern Spain and Northern Africa. This species is very close to Caprella cavediniae (Krapp-Schickel & Vader, 1998). Although 9 specimens have been collected in total, pereopods were absent in all of adult males. Caprellids from soft bottoms usually lose the pereopods during the treatment (sieving, sorting out...) of the sediment samples (obs. pers.). Despite this, several differences have been found between the males of the two species (Table 2).

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Figure 9. Location of the Strait of Gibraltar and comparative distribution of Caprella lilliput (Krapp-Schickel & Ruffo, 1986), C. rapax (Mayer, 1890) and C. pseudorapax n. sp.

The specimens of Caprella pseudorapax and C. sabulensis were collected in gross and medium sand (according to Buchanan & Kain, 1984) with low values of the organic matter (lower than 1%). The sandy bottoms from the Tarifa coast, Iberian side of the Strait of Gibraltar, where the new species were collected, are characterised by the abundance of the mollusc species Gouldia minima (Montagu, 1803), Digitaria digitaria (Linnaeus, 1758), Calyptraea chinensis (Linnaeus, 1758), the crustacean Bathyporeia sp. and several annelid species of the familly Syllidae. Caprella sabulensis n. sp. was also collected in sediment samples from Ceuta, North African side of the Strait of Gibraltar, dominated by the bivalve Ervilia castanea (Montagu, 1903), the annelids Hyalonecia bilineata Baird, 1870 and Marphisa belli (Audouin &

Milne-Edwards, 1833), and the crustaceans Apseudes latreillei (Milne-Edwards, 1828) and Leptocheirus hirsutimanus (Bate, 1862). Other caprellids found living together C. pseudorapax and C. sabulensis on sandy bottoms were Phtisica marina (Slabber, 1769) and Pariambus typicus (Kröyer, 1844). Acknowledgements We express our thanks to Compañía del Mar and Club Calypso from Ceuta for assistance in the field. We also thank Asamblea de Ceuta and a grant “Programa de Formación de Profesorado Universitario y Personal Investigador AP98 28617065”, from the Ministry of Education and Culture of Spain for financial support.

192 Table 2. Comparison of some morphological characters in Caprella cavediniae (Krapp-Schickel & Vader, 1998) and C. sabulensis n. sp. Features of C. cavediniae are taken from Krapp-Schickel & Vader (1998). Comparison is based on male specimens except pereopod 5, missing in male specimens studied C. cavediniae

C. sabulensis

Body length Surface body Pereonites length Propodus palm of gnathopod 2

4–7 mm Few rounded humps 2=3>4>5>6=7 Deeply excavated defined by a big tooth

Inner margin of gnathopod 2 dactylus Upper lip Lower lip

Thickened distally Scarcely pubescent Scarcely pubescent. Proximal projections of outer lobes short, not well-marked A pair of grasping spines 2-articulate Shallow depth (1.5–5 m), algae, hydroids, no detritus

3.8–5.3 mm Smooth 24>5>6=7 Straight or slightly concave defined by a tooth and a pair of strong proximal spines Thickened medially Densely pubescent Densely pubescent. Proximal projections of outer lobes slender, well-marked Without grasping spines 1-articulate Sandy bottoms (5–30 m)

Female pereopod 5 Abdominal appendages Ecology

Appreciation is extended to Consejería de Medio Ambiente (Junta de Andalucía) for financial support and the crewmembers of the ship AMA8 for assistance during the sampling programme in Tarifa coast.

References Buchanan, J. D. & J. M. Kain, 1984. Measurement of the physical and chemical environment. In Holme, N. L. & A. D. McIntyre (eds), Methods for the Study of Marine Benthos. Blackwell Scientific Publications, Oxford: 30–50. Cavedini, P., 1982. Contributo alla conoscenza dei Caprellidi del Mediterraneo. Bolletino del Museo Civico di Storia Naurale, Verona 8: 493–531. Estacio, F., 1996. Distribución y variación espacio-temporal de las comunidades macrobentónicas del sedimento en la Bahía de Algeciras. Implicaciones en la evaluación ambiental del medio marino. Tesis Doctoral, Universidad de Sevilla: 482 pp. Unpublished.

Krapp-Schickel, T., 1993. Suborder Caprellidea. In Ruffo, S. (ed.), The Amphipoda of the Mediterranean. Mémoires de l’Ínstitute Oceanographique, Monaco 13 (3): 773–809. Krapp-Schickel, T. & S. Ruffo, 1986. A new Caprella of the Mediterranean Sea (Crustacea: Amphipoda). Bolletino di Museo Civico di Storia Naturale, Verona, 13: 437–441. Krapp-Schickel, T. & W. Vader, 1998. What is, and what is not, Caprella acanthifera Leach, 1814 (Amphipoda, Caprellidea)? Part 1: the acanthifera-group. J. nat. Hist. 32: 949–967. Mayer, P., 1890. Die Caprelliden des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Fauna und Flora des Golfes von Neapel 17: 1–55. Mayer, P., 1903. Die Caprellidae der Siboga-Expedition. SibogaExpeditie 34: 1–160. Sánchez-Moyano, J. E., J. L. Carballo & F. J. Estacio, 1995a. Pedoculina garciagomezi (Amphipoda: Caprellidea), new species from Bahía de Algeciras (Southern Spain). Crustaceana 68: 418–427. Sánchez-Moyano, J. E., J. A. Jiménez-Martín & J. C. GarcíaGómez, 1995b. Caprella santosrosai n. sp. (Amphipoda: Caprellidea) from the Strait of Gibraltar (Southern Spain). Ophelia 43(3): 197–204.