A new species of Caprella (Crustacea: Amphipoda) from the Mediterranean Sea
© Springer-Verlag and AWI 2011
Received: 11 November 2010
Accepted: 18 January 2011
Published: 4 February 2011
A new caprellid amphipod, Caprella tavolarensis n. sp., is described based on specimens collected from a Posidonia oceanica seagrass meadow at the Tavolara-Punta Coda Cavallo Marine Protected Area (Sardinia, Mediterranean Sea). The species is close to Caprella liparotensis, but can be clearly distinguished by smaller size, presence of a short rostrum, body elongate and dorsally smooth, absence of serrate carina on the basis of gnathopod 2 and pereopods, mouthparts scarcely setose, absence of fine setae on peduncle of antenna 1 and absence of swimming setae on antenna 2. The number of caprellid species reported from the Mediterranean Sea has increased from 23 (1993) to 41 (2010), consequently, further taxonomical studies should be addressed to properly estimate the total amphipod diversity in the Mediterranean Sea.
Seagrasses are distributed worldwide (600.000 km2 of the marine bottoms are covered by these spermatophytes) and play an important role in the general coastal dynamics and biology (Larkum et al. 1989; Templado 2004; González et al. 2008). When compared with neighbouring areas, the meadows reveal higher abundances and species richness (Edgar et al. 1994). The main factors contributing to this improvement in biodiversity are availability of microhabitat, protection from predators, trophic resources, sediment settling, hydrodynamic force reduction (see Pranovi et al. 2000). Seagrass beds of the temperate zone support large numbers of invertebrate species and individuals, thereby providing abundant food for fishes, compared to adjacent unvegetated areas (Nakamura and Sano 2005). Along the coasts of the Mediterranean Sea, five species occur: Posidonia oceanica (Linnaeus) Delile, Zostera marina Linnaeus, Zostera noltii Hornemann, Cymodocea nodosa (Ucria) Ascherson and a lessepsian species Halophila stipulacea (Forsskål) Ascherson (Buia et al. 2000). In spite of the abundance of these seagrass meadows in the Mediterranean, caprellid communities associated to these plants have been scarcely studied, and the only records of caprellids from these habitats come from general faunistic or ecological studies (see González et al. 2008).
As a part of a general project assessing the effects of protection status (totally, partially and non protected areas) on amphipod communities associated to Posidonia oceanica beds along the Sardinian coast (Italy), several specimens of the genus Caprella were collected. Detailed examination revealed that these specimens belonged to a new species close to Caprella liparotensis, here described as Caprella tavolarensis n. sp.
Materials and methods
Although the phylogeny and higher classification of the caprellids are still under debate (see Laubitz 1993; Takeuchi 1993; Ito et al. 2008), Myers and Lowry (2003) have recently proposed a new phylogeny and classification for the suborder Corophiidea Leach, 1814. Based on the hypothesis of the evolution of different feeding strategies, the Corophiidea are divided into two infraorders, the Corophiida and the Caprellida. In their new classification, the superfamily Caprelloidea contains five families: Caprellidae, Caprogammaridae, Cyamidae, Dulichiidae and Podoceridae. The Caprellidae are subdivided into three subfamilies: Caprellinae, Paracercopinae and Phtisicinae. In the present paper, we have adopted the classification of Myers and Lowry (2003) considering the family Caprellidae, and the subfamily Caprellinae.
The symbols used in the present work are: A1, 2 = Antenna 1, 2; UL = Upper lip; LL = Lower lip; LMd = Left mandible; RMd = Right mandible; Mx 1, 2 = Maxilla 1, 2; Mxp = Maxilliped; Gn 1, 2 = Gnathopod 1, 2; P5–7 = Pereopod 5–7; Ab = Abdomen. All the type material is deposited in the Museo di Storia Naturale di Verona, Italy (MVR).
Family Caprellidae Leach, 1814
Subfamily Caprellinae Leach, 1814
Holotype male (used for drawings) (MVRCr 500.0). Paratype female (used for drawings) (MVRCr 500.1). Paratypes dissected (used for drawing the mouthparts) (3 males and 3 females, MVRCr 500.2–500.7). Other paratypes (10 males, 8 females, 2 juveniles, MVRCr 500.8). All the material was collected from the type locality (July–August 2008).
Additional material examined
17 males, 13 females, 2 juveniles, collected from the type locality (July–August 2007)
All the material has been collected from a Posidonia oceanica meadow between 10 and 15 m depth at the Tavolara-Punta Coda Cavallo Marine Protected Area, A zone of Molarotto island (40°52′25″N, 9°46′35″E), NE Sardinia, Italy (Fig. 1).
The specific name refers to the area where the species was found.
Head with very short rostrum. Pereonites 2, 3 and 4 with anterolateral projections. Body dorsally smooth. Peduncular articles of antenna 1 not setose. Antenna 2 without swimming setae. Basis of gnathopod 2 without serrated carina but with inner projection.
Holotype male (MVRCr 500.0)
Body length 5.8 mm.
(Fig. 2). Head with a short rostrum (almost absent in subadult males), suture between head and pereonite 1 present. Body dorsally smooth, without tubercles. A pair of anterolateral projections on pereonites 2, 3 and 4.
(Fig. 2). Present on pereonites 3–4, elongate, length about twice width.
(Fig. 3, figured from paratype 1). Upper lip symmetrically bilobed, small setulae apically. Mandibular molars process strong; incisor and lacinia mobilis 5-toothed; left mandible with three pectinated setae, right mandible with only two; small molar flake present on right mandible. Lower lip with inner lobes poorly demarcated and outer lobes scarcely setose. Maxilla 1 outer lobe with six robust and stout setae; distal article of palp with six setae distally and eight lateral setae. Maxilla 2 inner lobe oval and outer lobe rectangular, about 1.5 times as long as the inner lobe. Maxilliped inner plate with three robust and short setae (similar to “teeth”) and five plumose setae; outer plate with long, plumose setae and three robust setae (like “teeth”); palp four-articulate, with long plumose setae, article 4 with rows of setulae on its grasping margin.
(Fig. 4). Antenna 1 about half of the body length; peduncle scarcely setose; flagellum 9-articulate. Antenna 2 flagellum two-articulate, with scarce setae; swimming setae absent.
(Fig. 4). Gnathopod 1 basis as long as ischium, merus and carpus combined; propodus palm with two proximal grasping spines, grasping margin smooth; dactylus elongate. Gnathopod 2 inserted near distal end of pereonite 2; basis short, about one-sixth of pereonite 2 in length, provided with a ventral projection and lacking serrate carina; propodus elongate, length about 3 times width; palm concave with one proximal projection provided with grasping spine; another projection one-quarter length from distal end, followed by “U” notch distally.
(Fig. 5). Short, length about 1.2 times the width. Abdomen with a pair of two-articulate appendages, a pair of lateral lobes and a single dorsal lobe.
Paratype female (MVRCr 500.1)
Body length 3.5 mm. Similar to male, except for the following characters: flagellum of antenna 1 eight-articulate (Fig. 2); oostegites present (Fig. 2), being slightly setose on pereonite 3; gnathopod 2 (Fig. 4) inserted on the anterior half of pereonite 2, basis about one-fourth of pereonite 2 in length, length of propodus about 2 times width, U-notch lacking; abdomen without appendages, only the lateral lobes and dorsal lobe present.
Length varied from 2.8 to 6.3 mm (males) and 2.0–4.3 mm (females). Most of the morphological characters studied in the present paper were rather constant. All the specimens examined had the body smooth dorsally, lacking tubercles. The rostrum was very short in both males and females, being extremely reduced (almost absent) in subadult specimens. Insertion of gnathopod 2 was near distal end of pereonite 2, although the insertion could vary from half to distal end of pereonite 2, depending on the maturation stage of the specimen. Length of pereonite 1 and 2 vary also according to the stage of development (Figs. 6b, 8d). All the specimens were lacking serrate carina on the basis of gnathopod 2 and basis of pereopods. Carpus of pereopods 5–7 was provided by tiny teeth (Figs. 7f, 9e), although the number of these internal teeth could vary between 1 and 3. Six paratype specimens (3 males and 3 females) were dissected for examination of mouthparts. The structure of mouthparts is very constant, except for the following: (a) the number of strong setae (similar to “teeth”) in the outer lobe of the maxilliped could vary between 1 and 3; (b) the number of lateral setae of distal article of the palp of maxillae varied also from 4 to 8.
The specimens of Caprella tavolarensis n. sp. were collected from a well-preserved Posidonia oceanica bed between 10 and 15 m depth, located in a totally protected area. The meadow under investigation occurs on sandy bottoms and granitical rocks, and extends to a lower limit of about 27–30 m in depth. At sampling depth, mean meadow density reached 259 ± 98 shoots m−2 (mean ± standard deviation of 16 measurements).
The amphipod fauna of this meadow is dominated by the species Caprella tavolarensis n. sp. (37.2%), Apherusa chiereghinii Giordani-Soika (17.4%), Aora spinicornis Afonso (12.1%) and Phtisica marina Slabber (11.3%). Caprella tavolarensis mean density was 64 ± 75 individuals m−2 (mean ± standard deviation of 16 samples) and reached maximum density of 271 individuals m−2. The examination of horizontal spatial variability patterns, using a hierarchical nested design with spatial scales ranging from metres to hundred of metres, revealed that C. tavolarensis density exhibited the larger variation at the small spatial scale (~1 m). Although the existence of small-scale patchiness in density within P. oceanica meadows has long been recognised (Panayotidis et al. 1981), no correlation has been found between C. tavolarensis abundance and meadow density. Previous studies revealed that there is no correlation between parameters of the vagile fauna such as number of individuals and features of the P. oceanica meadow such as density (Scipione et al. 1996). In the same area, several experiments dealing with fish predation have been conducted. This species is little predated in comparison with other accompanying species such as Caprella acanthifera. Probably, the small size could let the specimens camouflaged among Posidonia leaves and escape from predators. Three caprellid species were found living in P. oceanica bed together with Caprella tavolarensis: Caprella acanthifera, Phtisica marina and Pseudoprotella phasma.
The new species Caprella tavolarensis n. sp. is close to Caprella liparotensis Haller, 1879, and Caprella wirtzi Krapp-Schickel and Takeuchi 2005. Caprella liparotensis was described based on specimens collected from Lipari, Italy and has since been reported from Portugal to the whole Mediterranean, including the Adriatic and Black Seas (Krapp-Schickel and Takeuchi 2005). Additional descriptions of this species have been provided by Chevreux and Fage (1925), Krapp-Schickel (1993) and Guerra-García and Takeuchi (2002). Krapp-Schickel and Takeuchi (2005) described Caprella wirtzi from Cape Verde Islands (Atlantic), close to C. liparotensis, but showing differences on antenna 2, gnathopod 2 and pereonites.
The new species Caprella tavolarensis clearly differs from C. liparotensis and C. wirtzi on the following characters: (1) smaller size in C. tavolarensis (males 3–6 mm, females 2–4 mm) than in C. liparotensis (males 7–12 mm, females 4–7 mm) and C. wirtzi (males 8–12 mm, females 4–6 mm); (2) body more elongate and dorsally smooth in C. tavolarensis, while dorsal tubercles or acute projections are present on pereonites 5–7 on the other two species; (3) very short rostrum in C. tavolarensis, while well developed in C. liparotensis and C. wirtzi; (4) maxilliped less setose in C. tavolarensis; (5) peduncle articles 2 and 3 of antenna 1 lacking dense setae in C. tavolarensis; (6) antenna 2 lacking swimming setae in C. tavolarensis; (7) basis of gnathopod 2 and pereopods lacking serrate carina in C. tavolarensis and C. wirtzi, while a developed serration is present in C. liparotensis.
The elongate shape of the body together with the scarcely setose antennae and very short rostrum make C. tavolarensis to resemble the species Caprella mitis and C. paramitis. However, the gnathopod 2 is totally different in these species.
Based on the considerable degree of intraspecific morphological variation in C. liparotensis, Krapp-Schickel and Takeuchi (2005) already doubted about the wide distribution of C. liparotensis within the Mediterranean and north-east Atlantic and pointed out that careful checking of rich series taken from many different localities should shed more light on what is variable and what are small but constant differences. Probably, the new species described in the present paper may have been misidentified as C. liparotensis in the past. So far, C. liparotensis had been recorded from different species of algae and hydroids (Krapp-Schickel 1993; Guerra-García 2001; Guerra-García and Takeuchi 2002), and also from P. oceanica seagrass beds (Scipione and Fresi 1984; Zakhama-Sraieb et al. 2006). The most common caprellid species recorded from seagrasses at Mediterranean sites are Caprella acanthifera Leach, 1814, Caprella rapax Mayer, 1890, Phtisica marina Slabber, 1769, Pseudoprotella phasma Montagu, 1804 and Pariambus typicus Krøyer, 1844 (Scipione 1998; Sánchez-Jerez et al. 1999; Luque et al. 2004; González et al. 2008). However, these caprellid species are not exclusive of these habitats since they have been collected from many different substrates (Guerra-García 2001). During the present study, the new species Caprella tavolarensis was found together with Caprella acanthifera, Pseudoprotella phasma and Phtisica marina. Probably, further studies on Posidonia oceanica beds of other Mediterranean areas could reveal the presence of C. tavolarensis, although we cannot exclude that the species could be an endemism of the area, and this would explain that the species has not been reported so far in the Mediterranean. Monitoring of the amphipod fauna in other comparable partially protected localities (B and C zones) of the Tavolara-Punta Coda Cavallo Marine Protected Area (Fig. 1) showed that specimens of Caprella tavolarensis have been found in only very rare cases, while it is the dominant species in the A zone with 37.2% of the total amphipod fauna. We cannot exclude a possible role of the protection status of this locality, highlighting the importance of totally protected areas in species conservation.
Caprellids cited in Mediterranean waters
Name of species
Caprella acanthifera Leach, 1814
Caprella andreae Mayer, 1890
M, A, P
Caprella caulerpensis Guerra-García, Sánchez-Moyano and García-Gomez, 2002
Caprella cavediniae Krapp-Shickel and Vader, 1998
Caprella ceutae Guerra-García and Takeuchi, 2002
Caprella danilevskii Czerniavski, 1868
M, A, P, I
Caprella dilatata Krøyer, 1843
Caprella equilibra Say, 1818
M, A, P, I
Caprella erethizon Mayer, 1901
Caprella fretensis Stebbing, 1878
Caprella grandimana Mayer, 1882
Caprella hirsuta Mayer, 1890
Caprella lilliput Krapp-Shickel and Ruffo, 1987
Caprella linearis Linnaeus, 1767
Caprella liparotensis Haller, 1879
Caprella mitis Mayer, 1890
Caprella monai Guerra-García, Sánchez-Moyano and García-Gómez, 2001
Caprella paramitis Guerra-García, Sánchez-Moyano and García-Gómez, 2001
Caprella penantis Leach, 1840
M, A, P, I
Caprella pseudorapax Guerra-García, Sánchez-Moyano and García-Gómez, 2001
Caprella rapax Mayer, 1890
Caprella sabulensis Guerra-García, Sánchez-Moyano and García-Gómez, 2001
Caprella santosrosai Sánchez-Moyano, Jiménez-Martín and García-Gómez, 1995
Caprella scaura Templeton, 1836
M, A, P, I
Caprella takeuchii Guerra-García, Sánchez-Moyano and García-Gómez, 2001
Caprella tavolarensis n.sp.
Caprella telarpax Mayer, 1890
Caprella tuberculata Bate and Westwood, 1868
Caprella sp (armata-group) (see Krapp-Shickel and Vader, 1998)
Deutella schieckei Cavedini, 1982
Liropus elongatus Mayer, 1890
Liropus minimus Mayer, 1890
Pariambus typicus Krøyer, 1844
Parvipalpus linea Mayer, 1890
Parvipalpus major A. Carausu, 1941
Pedoculina bacescui A. Carausu, 1940
Pedoculina garciagomezi Sánchez-Moyano, Carballo and Estacio, 1995
Phtisica marina Slabber, 1769
M, A, P
Pseudolirius kroyerii Haller, 1879
Pseudoprotella inermis Chevreux, 1927
Pseudoprotella phasma Montagu, 1804
Summarising, in spite of the amphipod fauna from the Mediterranean can be considered as very well studied, still new species are being described. Further sampling, especially from sediments, maerl bottoms and corraligène (below 40–50 m) should be conducted to complete our knowledge about Mediterranean caprellids.
We are very grateful to A. Navone and P. Panzalis (Consorzio di Gestione Area Marina Protetta Tavolara-Punta Coda Cavallo, Olbia, Italy) for their hospitality and field assistance. Many thanks to A. Pérez-Perera for valuable help during field work. Thanks are also due to G. Lepoint and S. Gobert for their help in advices and the staff of the Laboratoire d’Océanologie (Université de Liège, Belgium), as well as P. Compère for help and advices with SEM pictures (Laboratoire de Morphologie Fonctionnelle et Evolutive, Université de Liège). This study was supported by the Belgian Fund for Research for the Industry and Agriculture (FRIA, grant nr. FC77010), by a Special Research Fund of the University of Liège (FSR) and by the Belgian National Fund for Scientific Research (FNRS: FRFC 2.4.502.08.F). Additional financial support of this work was provided by the Ministerio de Educación y Ciencia (Project CGL2007-60044/BOS) co-financed by FEDER funds, by the Consejería de Innovación, Ciencia y Empresa, Junta de Andalucía (Project P07-RNM-02524). This paper is MARE publication number 205.
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