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Description of the first zoeal stage of Geograpsus crinipes (Dana, 1851) (Decapoda: Brachyura: Grapsidae) from the Red Sea.

INTRODUCTION

The study of crustacean systematics and phylogeny has from the very earliest times involved the recording of larval characters; and details of larval morphology reveal phylogenetic relationships among different brachyurans (Martin & Davis 2001). Consideration given to larval characters solves many of the existing problems of brachyuran taxonomy. Brachyuran larval culture and subsequent description will lead to correct identification of planktonic zoeae obtained from marine samples. Data on larval development and growth are poor for some brachyuran groups, and most larval descriptions deal only with the first zoeal stages because of the difficulties encountered in appropriately feeding the small late larval stages (Ingle 1987; Cuesta & Rodriguez 2000).

The family Grapsidae MacLeay, 1838, currently includes 40 species assigned to eight genera (Ng et al. 2008). The genus Geograpsus Stimpson, 1858, includes five species (Ng et al. 2008) and only one species, Geograpsus crinipes (Dana, 1851), is known from the Red Sea (Holthuis 1977). This species is widely distributed throughout the Indo-Pacific regions (Sakai 1976). The first grapsid zoeae can be distinguished from other grapsid larvae by the reduction of the antennal exopod to a small seta (Fransozo et al. 1998; Landeira & Cuesta 2012). At present, there are three descriptions of the larval stages of a species of Geograpsus, namely G. lividus (A. Milne Edwards, 1837). The first zoeal stage of this species was described from Panamanian waters (Cuesta & Schubart 1999) and the western Atlantic (Guerao et al. 2001). More recently, details of the complete larval development of G. lividus from Jamaican waters were published by Cuesta et al. (2011).

In the present study, larvae of G. crinipes were reared in the laboratory; and no larval stages could be obtained beyond the first zoeal stage. This is described and illustrated, and compared with the larvae of G. lividus.

MATERIAL AND METHODS

Ovigerous Geograpsus crinipes crabs were collected by hand from the rocky shore of Rabigh (22[degrees]79'N 39[degrees]03'E) on 12 July 2010. The females were held in aquaria (50* 20x25 cm), provided with a gravel base and rocky refuge, and fed fragments of fresh fish.

The seawater was changed every day until hatching took place. The eggs hatched on 15 July 2010. Approximately 250 larvae survived for four days. Soon after hatching, the healthy and actively swimming larvae were removed and separated in individual (each larva in 80 ml of filtered seawater) and mass bowls (20 larvae in 800 ml of filtered seawater). The temperature was kept constant at 27[degrees]C, salinity at 37 % and photoperiod at 12 h light and 12 h dark (Al-Aidaroos 2005; Cuesta et al. 2011). The larvae were fed the rotifer Brachionus sp., together with algae.

Larval specimens were dissected in polyvinyl lactophenol using a stereomicroscope and allowed to clear for 24 h. Coverslips were sealed with clear nail varnish. Appendages were drawn using an Olympus BH-2 microscope equipped with differential interference contrast (DIC) and which had a camera lucida. At least five replicates of each appendage were drawn in order to detect any variations (Clark & Al-Aidaroos 1996).

The first-stage zoea is described and fully illustrated. The sequence of the zoeal description is based on the malacostracan somite plan and described from anterior to posterior. Setal armature of appendages is described from proximal to distal segments and in order of endopod to exopod (Clark et al. 1998). The long antennular aesthetascs and the long plumose natatory setae of the first and second maxillipeds have been drawn truncated. Figures were drawn to scale with the aid of a camera lucida (Clark & Paula 2003).

Measurements are given to the nearest 0.01 mm and are based on a total of five larvae. A micrometer was used for measuring zoeal rostrodorsal length (RDL) from the tip of the rostral spine to the tip of the dorsal spine; carapace length (CL) from the base of the rostral spine to the posteriormost carapace margin; and carapace width (CW) as the maximum width of the carapace or the distance between the tips of the minute lateral spines. The pleon length (ABL) was measured from the first pleonite anterior margin to the posterior furca of the telson (Cuesta et al. 2011). Furcal length (fl) was deduced from an imaginary line across the base of the outer seta at the posterior margin of the telson to the furcal tip; and the basal telson length (bt) from a line across the anterior margin of the telson to the posterior margin (base of the outer seta) (Cuesta et al. 2011; Landeira & Cuesta 2012).

Specimens of Geograpsus crinipes have been deposited at the Senckenberg Natural History Museum in Frankfurt, catalogue number SMF 43574.

RESULTS

Family Grapsidae MacLeay, 1838 Genus Geograpsus Stimpson, 1858 Geograpsus crinipes Dana, 1851

Figs 1-3

First zoea.

Size (mm): RDL=0.89 [+ or -] 0.01, CW=0.52 [+ or -] 0.02, CL=0.43 [+ or -] 0.07, ABL=0.84 [+ or -] 0.02.

[FIGURE 1 OMITTED]

Carapace (Fig. 1A): Globose. Dorsal spine short and without setae. Rostral spine straight, shorter than dorsal spine. Lateral spine reduced to minute spine. There is a pair of dorsolateral setae. Anterodorsal, posterior and ventral margins without setae. Eyes: sessile.

Antennule (Fig. 1B): Uniramous. Endopod absent. Exopod unsegmented, with 2 long and 1 shorter unequal terminal aesthetascs, and 1 simple seta.

Antenna (Fig. 1C): Well-developed protopod process, longer than rostral spine, with 2 rows of 7 spinules of increasing size distally towards the tip. Endopod absent. Exopod reduced to a small bud with a simple terminal seta.

[FIGURE 2 OMITTED]

Mandible: Palp absent.

Maxillule (Fig. 2A): Coxal endite with 5 plumodenticulate setae. Basal endite with 5 setae and 2 minute spines. Endopod 2-segmented, proximal segment with 1 distal seta; distal segment with 1 subterminal and 4 terminal setae. Exopod setae absent.

Maxilla (Fig. 2B): Coxal endite bilobed, with 5+4 setae. Basal endite bilobed, with 5+4 setae. Endopod bilobed, with 4 (2 subterminal + 2 terminal) setae. Exopod (scaphognathite) margin with 4 plumose setae and a setose posterior stout process.

First maxilliped (Fig. 2C): Coxa without setae. Basis with 8 setae arranged 2+2+2+2. Endopod 5-segmented, with 1, 2, 1, 2 and 5 (1 subterminal + 4 terminal) setae. Exopod 2-segmented, distal segment with 4 terminal plumose natatory setae.

Second maxilliped (Fig. 2D): Coxa without setae. Basis with 4 setae arranged 1+1+1+1. Endopod 3-segmented, with 0, 1 and 5 (2 subterminal, denticulate + 3 terminal) setae, respectively. Exopod 2-segmented, distal segment with 4 terminal natatory setae. Third maxilliped: Absent.

Pereiopods: Absent.

Pleon (Figs 3A, B): Five somites, somite 2 with 1 pair of dorsolateral processes directed anteriorly. Somites 3-5 with 1 pair of dorsolateral processes directed ventrally, somites 2-5 with 1 pair of posterodorsal setae, also with posterolateral processes, these especially well-developed in somites 3-4. Pleopods absent.

Telson (Figs 3A, B): Forks short, slightly divergent; with a minute spine at base of each furcal arm, and lateral margins without spines. Posterior margin with 3 pairs of stout spinulate setae, medial setae shorter than the proximal ones; bt / fl > 1.

DISCUSSION

In many cases, only the first zoeal stage had been described for species in the family Grapsidae because of the difficulties in culturing larvae using techniques commonly employed in the laboratory for the later larval stages of various species of Brachyura (Guerao et al. 1999). Larval morphology is poorly documented in the Grapsidae, with the exception of the genus Metopograpsus (Cuesta et al. 2011, Table 2).

The morphological features of the first zoeal stages of Geograpsus lividus and G. crinipes correspond to those that define the zoeae of Grapsidae according to Fransozo et al. (1998), Cuesta et al. (1997), Cuesta and Schubart (1999) and Landeira and Cuesta (2012). Fransozo et al. (1998) distinguished zoeae of G. lividus on the Brazilian coast from other grapsid species on the basis of three characteristics: (a) telson furca with minute outer seta-like spines (type A); (b) fourth abdominal segment with minute medio-lateral process; and (c) fourth abdominal segment not laterally expanded. In the present study, G. crinipes was found to have somewhat similar characters to G. lividus. Only one important character is different and it can be used to distinguish between these species: lateral spines are not present on the telson of G. crinipes (there are 2-3 spines in G. lividus) (Table 1).

Consistent morphological differences could also be observed between the first zoeal stages of the two populations of G. lividus. The abdomen of the larvae from the Atlantic coast of Mexico has dorsolateral processes on somite 5, which are absent in the Pacific population (Cuesta & Schubart 1999). However, according to Schubart (2011), G. lividus from the Pacific could be G. occidentalis, based on mtDNA data. The same processes on somite 4 are more developed in Atlantic specimens than in their Pacific and Jamaican counterparts (Guerao et al. 2001). This variation may follow a temperature gradient rather than necessarily being indicative of geographic separation (Cuesta et al. 2011).

When these zoeae with are compared with those from Jamaica, differences in size are seen to be a prominent feature, with the Jamaican larvae being the smallest and those from the Gulf of Mexico the largest. According Guerao et al. (2001), Atlantic zoeae of G. lividus have three minute outer spines on the furcal arms of the telson, while there are only two in the Pacific population. The zoeal stage of G. lividus of the Pacific coast of Panama and that from the Gulf of Mexico could be distinguished from each other by the morphological features of the antennae, furcal arms of the telson, and abdomen (Cuesta et al. 2011).

[FIGURE 3 OMITTED]

As in the case of G. lividus, geographical differences may exist between the larvae of G. crinipes, also due to the temperature gradient and other factors. Therefore, further research is required on the larval stages of G. crinipes from different regions in order to understand geographical variation as well as to enable keys to the zoeae of this species to be formulated confidently. This, in turn, will facilitate accurate plankton identification from marine collections.

ACKNOWLEDGMENTS

Sincere thanks are due to Prof. Meachil Turkay for identification of the berried female crabs. We also thank King Abdul Aziz City for Science and Technology for providing financial support to the research project [P-S-(10-0029)].

REFERENCES

AL-AIDAROOS, A.M. 2005. The first three zoeal stages of the crab Metopograpsus messor (Forskal, 1775) (Crustacea: Brachyura: Grapsidae). International Journal of Biology and Biotechnology 2 (1): 29-36.

CLARK, P.F. & Al-Aidaroos, A.M. 1996. The first zoeas of Actaeodes hirsutissimus (Ruppell, 1830) and A. tomentosus (H. Milne Edwards, 1834) (Crustacea: Decapoda: Brachyura: Xanthidae: Actaeinae). Journal of King Abdulaziz University - Marine Sciences 7: 207-214.

CLARK, P.F. & Paula, J. 2003. Descriptions of ten xanthoidean (Crustacea: Decapoda: Brachyura) first stage zoeas from Inhaca Island, Mozambique. The Raffles Bulletin of Zoology 51 (2): 323-378.

CLARK, P.F., Calazans, D.D. & Pohle, G.W. 1998. Accuracy and standardization of brachyuran larval descriptions. invertebrate Reproduction and Development 33 (2-3): 127-144.

CUESTA, J.A. & Rodriguez, A. 2000. Zoeal stages of the intertidal crab Pachygrapsus marmoratus (Fabricius, 1787) (Brachyura, Grapsidae) reared in the laboratory. Hydrobiologia 436: 119-130.

CUESTA, J.A. & Schubart, C.D. 1999. First zoeal stages of Geograpsus lividus and Goniopsispulchra from Panama confirm consistent larval characters for the subfamily Grapsinae (Crustacea: Brachyura: Grapsidae). Ophelia 51 (3): 163-176.

CUESTA, J.A., Gonzalez-Gordillo, J.I. & Rodriguez, A. 1997. First zoeal stages of Grapsus adscensionis (Osbeck) and Planes minutus (Linnaeus) (Brachyura: Grapsidae) described from laboratory hatched material, with notes on larval characters of the Grapsinae. Journal of Natural History 31 (6): 887-900.

CUESTA, J.A., Guerao, G., Schubart, C.D. & Anger, K. 2011. Morphology and growth of the larval stages of Geograpsus lividus (Crustacea, Brachyura), with the descriptions of new larval characters for the Grapsidae and an undescribed setation pattern in extended developments. Acta Zoologica 92 (3): 225-240.

FRANSOZO, a., Cuesta, J.A. & Negreiros-Fransozo, M.L. 1998. The first zoeal stage of two species of Grapsidae (Decapoda, Brachyura) and a key to such larvae from the Brazilian coast. Crustaceana 71 (3): 331-343.

GUERAO, G., Abello, P & Torres P. 1999. Morphology of the first zoea of the shamefaced crab Calappa granulata (Linnaeus, 1758) Crustacea, Brachyura, Calappidae), obtained in the laboratory. Graellsia 55: 157-162.

GUERAO, G., Schubart, C.D. & Cuesta, J.A. 2001. The first zoeal stages of Grapsus grapsus (Linnaeus) and Geograpsus lividus (H. Milne Edwards) (Decapoda, Brachyura, Grapsidae) from the western Atlantic. Nauplius 9 (2): 111-121.

HOLTHUIS, L.B. 1977. The Grapsidae, Gecarcinidae and Palicidae (Crustacea: Decapoda: Brachyura) of the Red Sea. Israel Journal of Zoology 26 (3-4): 141-192.

INGLE, R.W. 1987. The first zoea of three Pachygrapsus species and of Cataleptodiusfloridanus (Gibbes) from Bermuda and Mediterranean (Crustacea: Decapoda: Brachyura). Bulletin of the British Museum (NaturalHistory), Zoology Series 52 (1): 31-41.

LANDEIRA, J.M. & Cuesta, J.A. 2012. Morphology of the second zoeal stage of Grapsus adscensionis (Osbeck, 1765) (Crustacea, Decapoda, Grapsoidea) confirms larval characters of the family Grapsidae. Zootaxa 3540: 59-64.

MARTIN, J.W. & Davis, G.E. 2001. An updated classification of the recent Crustacea. Natural History Museum of Los Angeles County Science Series 39: i-vii+1-124.

NG, P.K.L., Guinot, D. & Davie, PJ.F. 2008. Systema Brachyurorum: Part I. An annotated checklist of extant brachyuran crabs of the world. The Raffles Bulletin of Zoology, Supplement series 17: 1-286.

SAKAI, T. 1976. Crabs of Japan and the adjacent seas. Vol. 1. Tokyo: Kodansha.

SCHUBART, C.D. 2011. Reconstruction of phylogenetic relationships within Grapsidae (Crustacea: Brachyura) and comparison of trans-isthmian versus amphi-atlantic gene flow based on mtDNA. Zoologischer Anzeiger 250 (4): 472-478.

Ahmed E. Al-Haj and Ali M. Al-Aidaroos *

Department of Marine Biology, Faculty of Marine Sciences, King Abdul Aziz University, Post Box 80207, Jeddah, 21589 Saudi Arabia

* Corresponding author: aaidaroos@kau.edu.sa
TABLE 1

Morphological differences among first zoeas of the genus Geograpsus.
Abbreviations: A-aesthetascs, CL--carapace length, CW--carapace
width; nd--no data, P--pleonites, RDL--rostradorsal lengh, S--setae.

                                                G. lividus

References                                       Cuesta &
                                              Shubart (1999)

Carapace       RDL (mm)                     0.75 [+ or -] 0.03
               CW (mm)                      0.32 [+ or -] 0.01
               CL (mm)                      0.42 [+ or -] 0.02
Antennule                                         2A, 1S
Antenna        Small spines in protopod            6-7
Maxilliped 1   Coxa (S)                             nd
Telson         Outer spines                         3
Pleon          Dorsolateral processes (P)          2-4

                                                G. lividus

References                                        Guerao
                                               et al. (2001)

Carapace       RDL (mm)                      0.81 [+ or -] 0.02
               CW (mm)                       0.34 [+ or -] 0.01
               CL (mm)                       0.45 [+ or -] 0.01
Antennule                                          3A, 1S
Antenna        Small spines in protopod             5-6
Maxilliped 1   Coxa (S)                              1
Telson         Outer spines                          2
Pleon          Dorsolateral processes (P)           2-5

                                                G. lividus

References                                        Cuesta

                                               et al. (2011)

Carapace       RDL (mm)                      0.67 [+ or -] 0.02
               CW (mm)                       0.36 [+ or -] 0.03
               CL (mm)                       0.50 [+ or -] 0.02
Antennule                                          3A, 1S
Antenna        Small spines in protopod             5-6
Maxilliped 1   Coxa (S)                              1
Telson         Outer spines                          2
Pleon          Dorsolateral processes (P)           2-4

                                               G. crinipes

References                                    Present study

Carapace       RDL (mm)                     0.89 [+ or -] 0.01
               CW (mm)                      0.52 [+ or -] 0.02
               CL (mm)                      0.43 [+ or -] 0.07
Antennule                                         3A, 1S
Antenna        Small spines in protopod             7
Maxilliped 1   Coxa (S)                             0
Telson         Outer spines                         0
Pleon          Dorsolateral processes (P)          2-5
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Publication:African Invertebrates
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Date:Jun 1, 2014
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