J. Mar. Biol. Ass. U.K. (2003), 83,119^131 Printed in the United Kingdom

Phylogeny of the family Spongicolidae (Crustacea: Stenopodidea): evolutionary trend from shallow-water free-living to deep-water sponge-associated habitat

P O Tomomi Saito* and Masatsune Takeda O *Port of Nagoya Public Aquarium, Minato-ku, Nagoya 455-0033, Japan. National Science Museum, Shinjuku-ku, P Tokyo 169-0073, Japan. Corresponding author, e-mail: [email protected]

The phylogenetic relationships within the family Spongicolidae were examined based on a cladistic analysis of 38 adult morphological characters with reference to two outgroup species of the family .The strict consensus tree identi¢ed Microprosthema as the most basal , followed by Paraspongicola, Spongicola and the remaining genera. The Spongicoloides represents the most derived genus among spongicolids. The genera Spongicola, Spongicoloides and Spongiocaris should be rede¢ned, because they formed paraphyletic clades. The cladogram indicates that symbiosis with the hexactinellid sponges is coincident with the loss of gills, exopods on maxillipeds 2 and 3, and with the loss of spination on carapace, pereopods, abdomen, tail fan etc. These losses in the spongicolids are thought to be secondarily derived in relation to their sponge-associated habitat.

INTRODUCTION development and host association were obtained from pub- lished sources, museum collection records and examina- The family Spongicolidae is a relatively small group of tion of specimens, which are listed inTable 1. Comparative marine decapod . A total of 28 species and specimens were loaned from the following natural history two subspecies are recognized and at present assigned to museums: Natural History Museum and Institute, Chiba the following ¢ve genera: Microprosthema Stimpson, (CBM), Muse¤um National d’Histoire Naturelle, Paris Paraspongicola de Saint Laurent and Cleva, Spongicola de (MNHN), Te Papa National Museum of New Zealand Haan, Spongicoloides Hansen, and Spongiocaris Bruce & (NMNZ), National Science Museum, Tokyo (NSMT), Baba (see de Saint Laurent & Cleva, 1981; Holthuis, Northern Territory Museum of Arts & Sciences (NTM), 1994). The Microprosthema are free-living in Port of Nagoya Public Aquarium (PNPA), Nationaal shallow-water, but the others are well known for living as Natuurhistorisch Museum, Leiden (RMNH), Seto Marine a sexual pair entrapped in an internal cavity of deep-water hexactinellid sponges. In spite of the attention of many Biological Laboratory, Kyoto University (SMBL), Tokyo workers, a taxonomic grouping of the spongicolids has University of Fisheries (TUFIL), the University Museum, University of Tokyo (UMUTZ), National Museum of never been tested by a comprehensive analysis of the Natural History, Smithsonian Institution (USNM), Zoolo- relationships among all genera or species. gisches Museum, Christian Albrechts UniversitatZu It is di⁄cult to characterize these shrimps, ranging from ^ ^ « Kiel (ZMK), Zoologisk Museum, Copenhagen (ZMUC). those with well-developed mouthparts and a carapace The relationships of all known spongicolids were ana- with scattered spinules to those with reduced mouthparts lysed and evaluated by PAUP 4.0b8 (Swo¡ord, 2000). and a soft, relatively uncalci¢ed carapace without spines. Thirty-eight characters were used, all unordered and Spongicolid genera are still identi¢ed by characters of unweighted (Tables 6 & 7). Polarization decisions were maxillipeds 2 and 3. However, a detailed look at morpho- made using the outgroup method as laid out by Maddison logical features such as gills reveals even more diversity in the species of Spongicoloides and Spongiocaris than in the et al. (1984). Character states are indicated in the text by other genera. This case is similar to that of the pinnotherid numbers, giving the character and character state where 0¼presumed plesiomorphy; N40¼presumed apomor- (Pohle & Marques, 1998), which is known for sym- phy. For maximum parsimony, default settings included biosis with other invertebrates, mainly bivalve shells. ACCTRAN, and multistate taxa were treated as uncer- The present paper deals with evolutionary trends in tainties. Full heuristic searches were performed with the morphological characters of shallow-water free-living starting trees obtained by stepwise random addition. Tree to deep-water sponge-associated habitat and the phylo- bisection-reconnection branch swapping was performed genetic relationships among the species of the Spongi- with the MULTREES option to save all minimum-length colidae, with special reference to biogeography, larval trees. development and host association. The strict consensus tree calculated from the 208 equally parsimonious trees obtained from a heuristic analysis of MATERIALS AND METHODS the data matrix is shown in Figure 3. Two outgroup taxa 2 Data on external characters, gill formulae, biogeogra- genera, Odontozona and , were drawn from the phical and bathymetrical distributions, egg size, larval family Stenopodidae as the putative sister taxa of the

Journal of the Marine Biological Association of the United Kingdom (2003) 120 T. Saito and M. Takeda Phylogeny of spongicolid mez & Lalana, 1994] ¤ 1981; CBM, NSMT, NTM, USNM, ZMK] MNHN, NSMT, PNPA, SMBL, TUFIL, UMUTZ] CL range (mm) Source (Richters, 1880) 4 2.0^3.5 [Richters, 1880; CBM, PNPA, ZMK] Rathbun, 1906 4 2.4^6.6 [Rathbun, 1906; de Saint Laurent & Cleva, 1981; NTM, UMUTZ, USNM] de Saint Laurent & Cleva, 1981 8 2.2^4.3 [de Saint Laurent & Cleva, 1981; CBM, MNHN, USNM] Baba, 1979 4 7.7^12.7 [Baba, 1979; NMNZ, USNM] Berggren, 1993 3 5.8^8.9 [Berggren, 1993; RMNH, USNM] Goy, 1980 ^ ^ [Goy, 1980] (Richters, 1880) ^ ^ [Richters, 1880] Criales, 1997 1 3.5 [Criales, 1997; USNM] Manning & Chace, 1990 1 1.8 [Manning & Chace, 1990; USNM] Baba, 1983 ^ ^ [Baba, 1983] Goy, 1987 2 3.8^5.2 [Goy, 1987; USNM] Goy & Felder, 1988 9 2.9^5.9 [Goy & Felder, 1988; USNM] (von Martens, 1872) 4 3.8^4.5 [von Martens, 1872; USNM] Stimpson, 1860 TYPE SPECIES 26 1.8^4.9 [Stimpson, 1860; Holthuis, 1946; Baba et al., 1968; de Saint Laurent & Cleva, Hansen, 1908 TYPE SPECIES 3 5.0^7.0 [Hansen, 1908; ZMUC] Goy & Felder, 1988 1 4.3 [Goy & Felder, 1988; USNM] Alcock, 1901 ^ ^ [Alcock, 1901] (Bouvier, 1905) 2 6.2^6.9 [Bouvier, 1905a; MNHN] (Caullery, 1896) ^ ^ [Caullery, 1896; Kemp, 1910] de Saint Laurent & Cleva, 1981 TYPE SPECIES 2 3.1^3.2 [MNHN] Bruce & Baba, 1973 5 6.3^9.9 [Bruce & Baba, 1973; NMNZ, USNM] (Bouvier, 1905) ^ ^ [Bouvier, 1905b] Bruce & Baba, 1973 TYPE SPECIES 2 5.3^6.2 [Bruce & Baba, 1973; RMNH, NMNZ, USNM] Zarenkov, 1990 ^ ^ [Zarenkov, 1990] Stimpson, 1860 de Saint Laurent & Cleva, 1981 Ortiz, G¢mez & Lalana, 1994 ^ ^ [Ortiz, Go de Saint Laurent & Cleva, 1981 3 3.0^5.6 [de Saint Laurent & Cleva, 1981; CBM, MNHN] Kubo, 1942 443 1.6^8.8 [Kubo, 1942; PNPA, TUFIL] Hansen, 1908 Hayashi & Ogawa, 1987 12 2.3^3.2 [Hayashi & Ogawa, 1987; USNM] de Haan, 1844 TYPE SPECIES 56 2.0^10.5 [de Haan, 1844; Bate, 1888; Holthuis, 1946; de Saint Laurent & Cleva, 1981; Bruce & Baba, 1973 de Saint Laurent & Cleva, 1981 2 1.6^2.5 [de Saint Laurent & Cleva, 1981; MNHN] de Haan, 1844 List of examined species, number, size range (mm), and source of specimens. Spongicola Paraspongicola Spongicoloides Spongiocaris Microprosthema Paraspongicola pusilla Spongicola andamanica Spongicola cubanica Spongicoloides evolutus Spongicoloides hawaiiensis Spongicoloides inermis Spongicoloides novaezelandiae Spongicola henshawi henshawi Spongicola henshawi spinigera Spongicola holthuisi Spongicoloides galapagensis Spongicoloides koehleri Spongicoloides profundus Microprosthema semilaeve Microprosthema validum Spongicola in£ata Spongicola levigata Microprosthema scabricaudatum Spongicola japonica Spongicola parvispina Spongicola venusta Spongiocaris hexactinellicola Spongiocaris semiteres Spongiocaris yaldwyni Microprosthema inornatum Microprosthema manningi Microprosthema plumicorne Microprosthema emmiltum Microprosthema granatense Microprosthema looensis Genus Genus Genus Genus Genus Table 1. Species N N, number of examined specimens.

Journal of the Marine Biological Association of the United Kingdom (2003) Phylogeny of spongicolid shrimp T. Saito and M. Takeda 121

Table 2. Egg sizes and hatched larvae in the Spongicolidae.

Egg size Egg CL of ovigerous Species Hatched larva (mm long axis) number female (mm)

Microprosthema emmiltum zoea (?) 0.5 37^82 3.8^5.2 Microprosthema looensis ? large 20 4.3 Microprosthema manningi zoea (?) 0.5 1592 5.9 Microprosthema scabricaudatum zoea (?) 0.6 22 2.0^2.7 Microprosthema semilaeve zoea 0.5 828 3.9^4.1 Paraspongicola pusilla zoea 0.7^1.0 ? 3.1 Spongicola henshawi henshawi zoea (?) 0.6^0.7 631 6.2^6.6 Spongicola henshawi spinigera zoea (?) 0.6 ? 3.2 Spongicola holthuisi zoea (?) 0.8 ? 3.0 Spongicola japonica 1st juvenile 1.9 3^46 5.8^8.8 Spongicola levigata zoea or postlarva (?) 0.4^0.6 few 2.3^2.9 Spongicola parvispina zoea (?) 0.6^0.7 ? ? Spongicola venusta zoea 0.9 240 7.5 Spongicoloides galapagensis postlarva or 1st juvenile (?) 2.0 20 ? Spongicoloides koehleri 1st juvenile 2.0 62 ? Spongicoloides novaezelandiae postlarva or 1st juvenile (?) 2.2^2.4 23 9.4 Spongicoloides profundus postlarva or 1st juvenile (?) 1.5 few 7.0 Spongiocaris hexactinellicola postlarva or 1st juvenile (?) 2.5 30^33 7.6^8.5 Spongiocaris semiteres postlarva or 1st juvenile (?) 1.7 8 6.5 Spongiocaris yaldwyni postlarva or 1st juvenile (?) 2.4 97 9.9

CL, carapace length. Table 3. Geographical distribution of the Spongicolidae.

Japan Indo-West Paci¢c East Paci¢c West Atlantic East Atlantic

Genus Microprosthema emmiltum [ granatense [ inornatum [ looensis [ manningi [ plumicorne [ scabricaudatum [[ semilaeve [ validum [[ Genus Paraspongicola pusilla [ Genus Spongicola andamanica [ cubanica [ henshawi henshawi [ henshawi spinigera [ holthuisi [ in£ata [ japonica [[ levigata [[ parvispina [ venusta [[ Genus Spongiocaris hexactinellicola [ semiteres [ yaldwyni [ Genus Spongicoloides evolutus [ galapagensis [ hawaiiensis [ inermis [ koehleri [ novaezelandiae [ profundus [

[, observed.

Journal of the Marine Biological Association of the United Kingdom (2003) 122 T. Saito and M. Takeda Phylogeny of spongicolid shrimp

Table 4. Vertical distribution of the Spongicolidae.

Depth (m) 0^100 100^200 200^500 500^1000 1000^

Genus Microprosthema emmiltum [ granatense [ inornatum [ looensis [ manningi [ plumicorne [ scabricaudatum [ semilaeve [ validum [ Genus Paraspongicola pusilla [ Genus Spongicola andamanica [[ cubanica [ henshawi henshawi [[ henshawi spinigera [[ holthuisi [ in£ata [[ japonica [ levigata [ parvispina [ venusta [[[ Genus Spongiocaris hexactinellicola [ semiteres [ yaldwyni [ Genus Spongicoloides evolutus [[ galapagensis [ hawaiiensis [ inermis [ koehleri [[ novaezelandiae [[ profundus [

[, observed.

Spongicolidae (Holthuis, 1946; Dounas & Koukouras, S. henshawi h., S. h. spinigera, S. holthuisi and S. parvispina 1989). Nine of 32 taxa in this analysis have incomplete are also considered to be a similar pattern (Bate, 1888; data sets (Table 7), and therefore many of the contentious de Saint Laurent & Cleva, 1981; Zarenkov, 1990). Larvae taxa also fall into this category.The average percentage of in this group have extended larval development and missing data in the matrix is only 3.5%, but in some presumably wide dispersal. On the other hand, Spongicola species this percentage is as high as 31.6%. The placement japonica, Spongiocaris and Spongicoloides bear a comparably of taxa with high proportions of missing data should be small number of large eggs that hatch as postlarvae or viewed with some reservation. decapodids without wide dispersal (Bruce & Baba, 1973; Goy, 1980; Berggren, 1993; Saito & Konishi, 1999).

RESULTS Egg size and larval development Geographical and vertical distribution There is little information available about the larval Tables 3 and 4 show the geographical and vertical dis- development of the family Spongicolidae. Table 2 shows tributions of the Spongicolidae, respectively. Even though the egg size and type of hatched larvae of selected species their occurrence is concentrated in deep water, the dis- in the Spongicolidae and outgroups. is tribution of the Spongicolidae is restricted to tropical and known to bear an abundance of eggs that hatch as zoea temperate waters. The northernmost and deepest record with over nine developmental stages (Lebour, 1941). Most for this family is that of Spongicoloides profundus from a of Microprosthema have a large number of small sized eggs depth of 1480 m o¡ Iceland (Hansen, 1908). that hatch as zoea with over four stages (Raje & Except for the Paraspongicola, for which little distribution Ranade, 1978). Paraspongicola pusilla and Spongicola venusta, data are available, the widely distributed species are found

Journal of the Marine Biological Association of the United Kingdom (2003) Phylogeny of spongicolid shrimp T. Saito and M. Takeda 123 7e] 7e] 7e] 7e] 6e] 2e] 3e] 3e] 3e] 3e] 7e] 3e] 3e] þ þ þ þ þ þ þ þ þ þ þ þ þ exopod) (excluding Gill formula 3451 2 3 12345 11^1 1 1 ^^^^^ [19 11^1 1 r ^^^^^ [19 11^1 r ^ ^^^^^ [19 11^1 1 ^ ^^^^^ [19 1^^1 1 ^ ^^^^^ [19 ^^^1 1 ^ ^^^^^ [19 ^^^1 ^ ^ ^^^^^ [18 ^^^1 ^ ^ ^^^^^ [19 ^^^1 ^ ^ ^^^^^ [12 ^^^1 ^ ^ ^^^^^ [13 11^1 ^ ^ ^^^^^ [19 ^^^1 ^ ^ ^^^^^ [19 ^^^1 ^ ^ ^^^^^ [14 12312 11111 11111 11111 11111 11111 11^^^ 111^^ 111^^ 111^^ 111^^ 11111 111^^ 111^^ 2345 ^^^^ ^^^^ ^^^^ ^^^^ ^^^^ ^^^^ ^^^^ ^^^^ ^^^^ ^^^^ ^^^^ ; e, epipods; r, rudimentary form; ^, not observed. 1231 ^1^^ ^1^^ ^1^^ ^1^^ ^1^^ ^1^^ ^1^^ ^1^^ ^1^^ ^1^^ St, Stenopous ; 2345 222^ 222^ 222^ 222^ 222^ 222^ 222^ 111^ 222^^ r ^ ^^^^^ 222^ 222^ So, Spongicoloides ; 1231 1122 1122 1122 1122 1122 1122 1112 ^^11 1122 ^11111r^^r^^ 1122 1122 Sa, Spongiocaris ; Pleurobranch Arthrobranch Podobranch Epipod Exopod S, Spongicola ; Maxilliped Pereopod1 2 3 12345 Maxilliped Pereopod Maxilliped Pereopod Maxilliped Pereopod Maxilliped Pereopod ^ ^ 1 11111 ^ ^ 1 11111 ^ ^ 1 11111 ^ ^ 1 11111 ^ ^ 1 11111 ^ ^ 1 11111 ^ ^ 1 11111 ^ ^ 1 11111 ^ ^ 1 11111 ^ ^ 1 11111 ^ ^ 1 11111 ^ ^ 1 11111 ^ ^ 1 11111r r 1 1111^^ r ^ ^^^^^ P, Paraspongicola ; Gill formulae of the Spongicolidae and outgroup. M. inornatum, M. looensis, M. manningi, M. plumicorne, M. scabricaudatum, M. semilaeve, M. validum, P. pusilla, S.St. in£ata, hispidus henshawi, S. henshawi spinigera, S. holthuisi, S. venusta, S. levigata Table 5. Taxa M. emmiltum, M. granatense, S. andamanica, S. henshawi S. japonica Sa. semiteres Sa. hexactinellicola Sa. yaldwyni So. evolutus So. galapagensis So. hawaiiensis So. inermis So. koehleri So. novaezelandiae So. profundus M, Microprosthema

Journal of the Marine Biological Association of the United Kingdom (2003) 124 T. Saito and M. Takeda Phylogeny of spongicolid shrimp

Table 6. List of characters and their states used in the parsimony analysis. Numeric character labels correspond with those in Table 7.

CARAPACE 1 Scattered spinules on surface: (0¼p, 1¼a). 2 Antennal spine: (0¼p, 1¼a). 3 Spines on hepatic region: (0¼p, 1¼a). 4 Postmarginal spines on pterygostomial angle: (0¼p, 1¼a). 5 Spines on rostral base: (0¼p, 1¼a). 6 Rostral length to distal end of segment 2 of antennular peduncle: (0¼overreaching, 1¼short). EYES & ANTENNA 7 Stalk length against cornea: (0¼larger, 1¼smaller or nearly equal). 8 Spinules on ophthalmic peduncle: (0¼p, 1¼a). 9 Shape of scaphocerite: (0¼lance shaped, 1¼semicircular, 2¼quadrangular, 3¼small & narrow). ABDOMEN 10 Scattered spinules on surface: (0¼p, 1¼a). 11 Posterior dorsal margin of segment 3: (0¼covers most of dorsal forth segment, 1¼not elongate). GILLS 12 Arthrobranchs on maxilliped 1: (0¼1, 1¼rudimentary, 2¼a). 13 Arthrobranchs on maxilliped 2: (0¼1, 1¼rudimentary, 2¼a). 14 Arthrobranchs on maxilliped 3: (0¼2, 1¼1, 2¼a). 15 Arthrobranchs on pereopod 1: (0¼2, 1¼1, 2¼a). 16 Arthrobranchs on pereopod 2: (0¼2, 1¼1, 2¼a). 17 Arthrobranchs on pereopod 3: (0¼2, 1¼1, 2¼a). 18 Arthrobranchs on pereopod 4: (0¼2, 1¼1, 2¼rudimentary). 19 Podobranchs on maxilliped 2: (0¼1, 1¼rudimentary). 20 Epipod on pereopod 1: (0¼p, 1¼a). 21 Epipod on pereopod 2: (0¼p, 1¼a). 22 Epipod on pereopod 3: (0¼p, 1¼a). 23 Epipod on pereopod 4: (0¼p, 1¼a). MOUTHPARTS 24 Exopod on maxilliped 2: (0¼well developed, 1¼rudimentary, 2¼a). 25 Exopod on maxilliped 3: (0¼well developed, 1¼rudimentary, 2¼a). 26 Spines on ischium of maxilliped 3: (0¼many, 1¼few, 2¼a). 27 Spines on merus of maxilliped 3: (0¼p, 1¼a). 28 M3-P brush: (0¼de¢nite, 1¼rudimentary or absent). PEREOPODS 29 P1^CP brush: (0¼de¢nite, 1¼rudimentary or absent). 30 Spines on merus of pereopod 2: (0¼p, 1¼a). 31 Dorsal margin of palm of pereopod 3: (0¼spinous with crista, 1¼spinous, 2¼grained or setae, 3¼a). 32 Ventralmarginofpalmofpereopod3:(0¼spinous or denticlate, 1¼grained or setae, 2¼a). 33 Carpi of pereopods 4 and 5: (0¼distinctly more than 6-segmented, 1¼sometimes faintly below 6-segmented, 2¼not segmented). 34 Propodi of pereopods 4 and 5: (0¼distinctly more than 3-segmented, 1¼sometimes faintly below 3-segmented, 2¼not segmented). 35 Dactyli of pereopods 4 and 5: (0¼bi¢d, 1¼bi¢d with teeth or tri¢d). TELSON & UROPODS 36 Shape of telson: (0¼lance shaped, 1¼triangular, 2¼quadrangular). 37 Spines on outer margin of uropodal exopod: (0¼1^9, 1¼more than 10). 38 Spines on outer margin of uropodal endopod: (0¼p, 1¼a). a, absent; p, present. in Microprosthema and Spongicola, especially Spongicola venusta, old group, which originated in the tropical Tethys and which is known from several areas of the Indo-West Paci¢c highly specialized to comply with particular requirements. waters (de Haan, 1844; Bate, 1888; Holthuis, 1946; de Saint The vertical distribution of the Spongicolidae is also Laurent & Cleva, 1981). Spongiocaris and Spongicoloides are interesting. The shallowest genus is the Microprosthema. widely distributed as genera, but each of their species is The average habitat depth of spongicolids then becomes endemic to a speci¢c region with no overlap in geographical deeper in Paraspongicola, followed by Spongicola, Spongiocaris ranges. and ¢nally Spongicoloides, the genus recorded from the Distributions of the Spongicolidae seem strictly limited deepest bottom for the family at 500^1500 m. by the presence of suitable temperature ranges and sub- strate habitats within available current regimes. The latter ensures that their larvae do not disperse far on their own Morphological characters but are highly dependent on where the currents take them. Table 6 shows the characters and their states for 32 Schram (1986) estimated that the Spongicolidae is a very taxa used in the phylogenetic analysis, and Table 7 shows

Journal of the Marine Biological Association of the United Kingdom (2003) Phylogeny of spongicolid shrimp T. Saito and M. Takeda 125

Table 7. Data matrix.

Character number #0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 1 1 1 1 1 2 2 2 2 2 2 2 2 2 2 3 3 3 3 3 3 3 3 3 Character number 0# 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8

Microprosthema emmiltum 00000000111000000000000000000111120110 Microprosthema granatense 10000000210000000000000001000100000100 Microprosthema inornatum 10000100210?00000000000001000100000100 Microprosthema looensis 00000001101000000000000001000121220100 Microprosthema manningi 00000000111000000000000000000000220100 Microprosthema plumicorne 0000000?2110000000000000010??112000200 Microprosthema scabricaudatum 00000000301000000000000000000?1?220100 Microprosthema semilaeve 00000000111000000000000001000000220110 Microprosthema validum 00000000111000000000000000000000110110

Paraspongicola pusilla 10100000111000000000000001100010221110

Spongicola andamanica 1000010011100000000000001???01?0220110 Spongicola cubanica 11111100111???????0????0221?1132220200 Spongicola henshawi henshawi 10100000111000000000000010000110121110 Spongicola henshawi spinigera 10000000111000000000000010000110121110 Spongicola holthuisi 10000100111000000000000011010110121110 Spongicola in£ata 10000000111000000000000001000110221110 Spongicola japonica 11101111211000000000000122111131221211 Spongicola levigata 10111100111000000000000012111110120100 Spongicola parvispina 10001000111???????0????0121?1110220101 Spongicola venusta 10000100111000000000000012111110221110

Spongicoloides evolutus 11100100211001000001111222111132221201 Spongicoloides galapagensis 10000101211221111101111221111131221211 Spongicoloides hawaiiensis 11111?1121100000001111122211113222?211 Spongicoloides inermis 10111111211211111211111222111132221201 Spongicoloides koehleri 111011012110000000000002221?11322212?? Spongicoloides novaezelandiae 10001101211000000001111222111132221211 Spongicoloides profundus 11100111211111111111111222111132220211

Spongiocaris hexactinellicola 10101111211000000000001022011131221211 Spongiocaris semiteres 11111111211000000000000022111132221210 Spongiocaris yaldwyni 10001011211000000001111022111132221211

Odontozona minoica 10000010010012????00000000000110000000 Stenopus hispidus 00000000000000000000000000000010000010 the data matrix, summarizing the character states. This outgroup as shown in Table 6: antennal spine (2), spines includes characters 1^6 related to carapace, characters on the hepatic region (3), postmarginal spines on the 7^9 related to eyes and antenna, characters 10 and 11 pterygostmial angle (4), and spines on the rostral base (5). related to abdomen, and characters 12^23 related to the For the Stenopodidea, almost all free-living shrimp have gill formula. Additional characters 24^28 are related to scattered spinules on the body, such as on the carapace mouthparts, and characters 29^35 to pereopods. Finally, and abdomen. Thus, those spongicolids with sponge asso- three characters listed as 36^38 related to telson and ciations represent derived taxa. The carapace multistate uropods are analysed. character is left unordered, since it is uncertain whether evolution to a membranous carapace proceeded through Carapace. Figure 1A^C shows the spongicolid carapace, an intermediate stage with a less pliant carapace in all which is distinctive in spination, and the of taxa. Rostral length to distal end of second segment of various genera is mostly based on its appearance (Hansen, antennular peduncle (6) is overreaching in the outgroup 1908; Bruce & Baba, 1973; de Saint Laurent & Cleva, 1981; (i.e. all Microprosthema except for M. inornatum, Paraspongicola Holthuis, 1994). In the present study, six characters are pusilla, S. in£ata, S. henshawi h., S. h. spinigera, S. parvispina and found to be phylogenetically informative, with an out- Spongiocaris yaldwyni), but is short in all Spongicoloides and the group comparison suggesting the presence of each of others. these characters to be plesiomorphic. Scattered spinules on the carapace surface (1) are observed in Stenopus and Eyes and antenna. The characters 7^9 relating to the state of most of Microprosthema, while they are not present in eyes and antenna are also phylogenetically informative. M. granatense, M. inornatum and the others. The numbers Stalk length against cornea (7) is related to visual ability, of spines associated with some speci¢c parts of the cara- and spinules on the ophthalmic peduncle (8) are also pace are also useful and polarized by comparison to the found to be useful. The outgroup comparison suggests

Journal of the Marine Biological Association of the United Kingdom (2003) 126 T. Saito and M. Takeda Phylogeny of spongicolid shrimp

Figure 1. Schematic representations of Microprosthema validum (A,D,G,J),Spongicola venusta (B,H,K),S. japonica (C, E), and Spongicoloides profundus (F,I,L).A^C, Carapace; D^F, exopod of maxilliped 2; G^I, exopod of maxilliped 3; J^L, pereopod 3.

that the larger cornea and presence of spinules on a stalk maxillipeds 1^3 (12^14) and pereopods 1^4 (15^18), podo- are plesiomorphic states. The shape of the scaphocerite (9) branch on maxilliped 2 (19), and epipods on pereopods is informative, lance shaped in the outgroup, semicircular in 1^4 (20^23), considered plesiomorphic from outgroup most Microprosthema and Spongicola. However, it is quadran- comparison. Particular gills also show a reduced state by gular in M.granatense, M. inornatum, M. plumicorne, S. japonica, lacking one of the usual states, or by being reduced to a Spongiocaris and Spongicoloides. rudimentary axis.The data for the three resulting character states provided ordered, developmental evidence (Hong, Abdomen. The abdomen in all taxa examined is invariant 1988), indicating that a loss of gills is preceded by reduc- with no phylogenetic useful characters. Transverse ridges tion. Table 5 shows gill formulae among the Spongicolidae. seen frequently in Microprosthema are not used in this Microprosthema, Paraspongicola and Spongicola represent the study, as they are sometimes unusable in the deposited maximum number of gills. Gill formulae are relatively condition of specimens. Scattered spinules on surface (10) consistent within these genera, but there are slight varia- were recognized in only outgroup and M. scabricaudatum. tions in Spongiocaris and Spongicoloides, where some species Posterior dorsal margin of third abdominal segment (11) have lost gills. is elongated in outgroup, M. granatense and M. inornatum. Mouthparts. The Spongicolidae possess a number of syna- Gills. Characters 12^23 relating to the state of the gills pomorphies associated with the maxillipeds, which are are phylogenetically informative, with arthrobranchs on distinctive, and taxonomy of various genera is based

Journal of the Marine Biological Association of the United Kingdom (2003) Phylogeny of spongicolid shrimp T. Saito and M.Takeda 127

Figure 2. Schematic representations of Microprosthema validum (A, D), Spongicola japonica (B, E), and Spongicoloides profundus (C, F). A^C, Setiferous organ of maxilliped 3 (arrow); D^F, setiferous organ of pereopod 1 (arrow). on their appearance (Figures 1D^I&2A^F). Spongi- maxilliped 3 (Figure 1H). Spongicola japonica has a reduced colids except for Microprosthema di¡er from other exopod on maxilliped 2 (Figure 1E), but lacks one on stenopodideans in that some lack exopods on the maxilli- maxilliped 3. Spongicola cubanica represents the characteris- peds. For this character, an outgroup polarization showed tics in maxillipeds 2 and 3 of Spongiocaris, showing a well- the presence of exopod on all maxillipeds to be in a plesio- developed exopod on maxilliped 2, but lacking one on morphic state.The states of exopods on maxillipeds 2 and 3 maxilliped 3. Spongicoloides lacks it on both maxillipeds 2 (24, 25) are consistent within genera; Microprosthema and and 3 (Figure 1F, I). Spines on the ischium and merus of Paraspongicola have well-developed ones on each maxilliped maxilliped 3 (26, 27) are informative, recognized mainly (Figure 1D, G). Most Spongicola members have a well- in the outgroup, Microprosthema and some species of Spongi- developed exopod on maxilliped 2, but a reduced one on cola. The maxilliped 3 propodal brush (M3^P brush) (28)

Journal of the Marine Biological Association of the United Kingdom (2003) 128 T. Saito and M. Takeda Phylogeny of spongicolid shrimp [ [ [ [

Figure 3. The strict consensus tree based on 38 characters of [[ 30 spongicolid and 2 outgroup taxa. Tree length¼114 steps, CI¼0.4649, RC¼0.3697. Synapomorphies are indicated below branches; characters 11, 14, 15, 16, 17, 20, 21, 22, and , observed. [

28 are unique in the taxa examined and unreversed; character ; state numbers in parentheses are shown only for multi-state or [ reversed characters. So, Spongicoloides ranges from rudimentary or absent in Spongiocaris and ; Spongicoloides to well developed in the outgroup, Microprosthema, Paraspongicola and some Spongicola (Figure 2A^C). This character is used for grooming antennule in Stenopus hispidus (Bauer,1989). Sa, Spongiocaris ;

Pereopods. The form of the spongicolid pereopod is well documented.Variations in the pereopod 1 carpal-propodal

joint brush (P1^CP brush) (29) are also found. It ranges S, Spongicola from rudimentary or absent in Spongiocaris and Spongicoloides ; to well-developed in the others (Figure 2D^F). This char- acter is also used for grooming the antenna in Stenopus [[[ [[[ hispidus (Bauer, 1989). Spines on the merus of pereopod 2 R, Regadrella

(30) are present in Stenopus hispidus, M. manningi, ; M. semilaeve, M. validum,andP. pusilla. Dorsal and ventral E. aspergillum E. curvistellata E. imperialis E. jovis E. marshalli E. oweni H. sieboldi D. pumiceus R. phoenix R. okinoseana marginal states of pereopod 3 (31, 32) are also informative, ranging from spinous with crista, spinous, grained, with setae to absent (Figure 1J^L). Subdivisions of the carpi E, Euplectella ;

and propodi of pereopods 4 and 5 (33, 34) are of phy- Records of host species and their spongicolid symbionts. logenetic use, as outgroup comparison suggesting the subdivision to be plesiomorphic. In the outgroup, M. granatense, M. inornatum and M. plumicorne, these char- Sa. hexactinellicola S. japonica S. levigata S. venusta Sa. yaldwyni So. koeleri D, Dactylocalyx acters are distinct. However, they are equivocal in the Table 8. Host species S. cubanica

Journal of the Marine Biological Association of the United Kingdom (2003) Phylogeny of spongicolid shrimp T. Saito and M. Takeda 129 other Microprosthema and some Spongicola species, and not [29(1)]. The monophyly at clade G is supported by two at all divided in the rest of Spongicola, Spongiocaris and synapomorphies, all of which multistate: no exopod on the Spongicoloides.The dactyli of pereopods 4 and 5 (35) are bi¢d maxilliped 3 [25(2)] and the quadrangular shape of the in the outgroup, Microprosthema and Spongicola andamanica, telson [36(2)]. Results from the strict consensus tree indicate S. cubanica, S. levigata and S. parvispina, while they are bi¢d that Spongicola japonica, Spongiocaris hexactinellicola, S. semiteres with accessory teeth or tri¢d in most Spongiocaris and Spon- and Spongicoloides koehleri are sister taxa at clade H, which is, gicoloides. however, poorly de¢ned and not supported by any synapo- morphies. Spongiocaris yaldwyni, Spongicoloides hawaiiensis and Telson and uropods. The forms of telson and uropods are S. novaezelandiae are sister taxa at clade I, which is supported used to distinguish spongicolid genera. However, a ridge by three unique and unreversed synapomorphies: the on the surface used as de¢nitive genera is not employed epipods on the pereopods 1^3 (20^22). The monophyly at in this study, since it is sometimes unrecognizable due to clade J is supported by a unique and unreversed synapo- the deposited condition of the specimens. Shape of the morphy: arthrobranchs on the maxilliped 3 (14).The mono- telson (36) ranges from lance-shaped in the outgroup to phyly at clade K is supported by ¢ve synapomorphies, three triangular in most Microprosthema and Spongicola, and to of which are unique and the others multistate: no arthro- quadrangular in M. plumicorne, S. cubanica, S. japonica, branchs on maxilliped 1 [12(2)] and arthrobranchs on Spongiocaris and Spongicoloides. Spines on the outer margins pereopods 1^4 [15^17,18(1)]. of uropodal exopod and endopod (37, 38) are informative. A trend seen in both characters is to be spinous in the out- DISCUSSION group, most Microprosthema and Paraspongicola, and absent in most Spongicola, Spongiocaris and Spongicoloides. Decapod crustaceans spend much time and energy in grooming or cleaning their bodies using a variety of appendages and processes while under constant exposure Host association to a variety of microbial and macroscopic fouling org- Others than Microprosthema occurring in tropical anisms that can interfere with feeding and locomotion if shallow-waters, the spongicolid genera are associated with not removed. Many studies have indicated that various deep-water hexactinellid sponges. The host species for specialized setal areas, located on the posterior maxilli- each symbiont of Spongicola, Spongiocaris and Spongicoloides peds and pereopods, are used to brush, comb, scrape, and are given inTable 8. Spongicola venusta has a wide selection, pick other appendages, gills, and general body surfaces, being associated not only with Euplectella but also with keeping them free of fouling organisms and debris. Hyalonema, while the others are mostly reported only from Numerous grooming structures and behaviours have the Euplectella species. evolved in decapod crustaceans in response to the selective pressure of fouling. Bauer (1989) reviewed the grooming behaviour and characteristics in many species of decapod Phylogenetic analysis crustaceans, and stated that the grooming characters The strict consensus of the 208 most parsimonious trees might have contributed to our understanding of certain based on the analysis of 38 characters with a total of 94 aspects of decapod phylogeny. character states (Table 7), is shown in Figure 3. Seventeen In the coral banded shrimp Stenopus hispidus, the long clades are apparent, but in the following section, selected antennular £agellum is groomed by a cup-shaped setal clades necessary to our discussion are labelled in alpha- brush located at the distal end of the maxilliped 3 betical order. Numbers below the branches correspond to propodus (M3^P brush). The specialized brushes of setae characters inTable 6 and show where derived states evolved; on either side of the carpal-propodal joint of pereopod 1 character state numbers in brackets are shown only for (P1^CP brush) are also used for grooming the long multistate characters and characters with reversals. chemotactile antennal £agellum (Bauer, 1989).The spongi- The monophyly of clade A is supported by two synapo- colids characteristically reveal diversity in such setiferous morphies of multistate: the semicircular or quadrangular organs as those on maxilliped 3 and pereopod 1, and even shape of the scaphocerite [9(2)] and the triangular shape in the exopods of maxillipeds 2 and 3, which are also used of the telson [36(1)]. Clade B is supported by a unique for gill grooming. Several caridean shrimps use the post- and unreversed synapomorphy: not elongate posterior erior pereopods for grooming the abdomen and posterior dorsal margin of the third abdominal segment (11). A parts of cephalothoraxes. Stenopodidean shrimps have no polytomy at clade C is supported by a multistate synapo- setal brushes or combs on pereopods 4 and 5; however, a morphy: unsegmented propodi of the pereopods 4 and 5 sub-division of each propodus and carpus on pereopods 4 [34(2)]. Although Microprosthema forms the most basal taxon and 5 provides £exibility, which may be related to cleaning within the Spongicolidae, it represents a paraphyletic clade. the abdomen or the inside of the posterior carapace region. A polytomy at clade D consisting of Paraspongicola, Spongicola The sponges have passive defence systems armed with and the ancestor of the remaining taxa is poorly de¢ned, poisons, and immune systems to protect themselves against and not supported by any synapomorphies. A monophyly fusion, overgrowth, and predation. The body wall of hex- at clade E is supported by only one synapomorphy of multi- actinellid sponges makes a perfect mesh resembling a state, a rudimentary exopod on the maxilliped 3 [25(1)]. ¢ltering system, which will strain out a variety of micro- The polytomy at clade F is supported by three synapo- bial and macroscopic fouling organisms from the seawater. morphies, one of which is unique and the others multi- Under those circumstances, the internal water of the state: no spines on the ischium of the maxilliped 3 [26(2)], gastral cavity of sponges is more clearly comparable to a rudimentary or no M3^P brush (28) and no P1^CP brush the outer water in physical or biological respects. In such

Journal of the Marine Biological Association of the United Kingdom (2003) 130 T. Saito and M. Takeda Phylogeny of spongicolid shrimp environments, applying to the frequency of exploitation on the Hexactinellida is to avoid genetic homogenization, sponges, all the characters about grooming behaviour are and the second is the competition among sedimentary not necessary for sponge associates and have degenerated organisms for substrata. One can not give a de¢nite because of disuse. Thus, the authors of this study believe answer, but a catastrophic faunal change at the Palaeo- that variation of the grooming characters within a family zoic^Mesozoic boundary was observed in the Hexactinel- will contribute to an understanding of Spongicolidae phylo- lida (Finks, 1960), a group with preference for deep-water geny. regions with a low density of planktonic and macrobenthic Gill formulae are generally considered to be charac- organisms. The ancestral spongicolids emerged during the teristic of major subgroups among decapods (Burkenroad, late to the late . At that time some 1981) and are believed to be constant in the families (Hong, members might be associated with hexactinellid sponges, 1988). Some semi-terrestrial crabs such as ocypodids which also £ourished in shallow-water during this period. (Takeda et al., 1996) and the Pinnotheridae (Pohle & Until the late Jurassic era, spongicolid habitats had shifted Marques, 1998) are known for having fewer gills. Gill from all vertical distribution to deep water accompanied reduction is also observed in the Spongicolidae, where gill by the transition in the host sponge habitat for some reason. formulae are more diverse than in the Stenopodidae. A comparison of gill formulae (Table 5) with a proposed phylogenetic relationship shows the distribution of char- We are grateful to Dr K. Konishi of the National Research Institute of Aquaculture for his encouragement and valuable acters and indicates how the reduction of gills evolved. A advice. Thanks are due to Mr K. Ikeue for collecting the ¢eld reduction in the number of gills in the Spongicolidae might materials, Mr Y. Ise, Dr Y. Kano, Ms M. Mitsuhashi and Dr have resulted from the adaptation to sponge-associated M. Osawa (NSMT) for their help throughout this study.We also habitats like the adaptation in pinnotherids with bivalves. acknowledge the following colleagues for the loan of specimens: The reduced gills are adequate to meet the respiratory T. Komai (CBM), R. Cleva and A. Anker (MNHN), R. Webber requirements of an inactive sponge-associated shrimp, (NMNZ), G. Dally (NTM), C. Fransen (RMNH), S. Kubota where space is at a premium. It is suggested that the (SMBL), S. Watanabe (TUFIL), R. Ueshima (UMUTZ), J.C. Walker (USNM), R. Ko«nig (ZMK), and J. Olesen (ZMUC). We reduction of gills was achieved during the evolution of also wish to express our gratitude to the director, Dr I. Uchida spongicolid shrimps. and the sta¡ of the PNPA for supporting our study. Reduction of gills in the Spongicolidae is related to the presence or absence of host sponges. The Microprosthema without symbiotic associations may have the same number REFERENCES of gills, while in genera with host sponges gill numbers Alcock, A., 1901. A descriptive catalogue of the Indian deep-sea vary. Generally, the selected characters were based upon Crustacea and Anomala in the Indian Museum: being a the spiniform and gills in shrimps. These characters are revised account of the deep-sea species collected by the Royal Indian considered to be variable due to their adaptation and reli- marine survey ship Investigator. Calcutta: Indian Museum. ance on the host sponge habitat. Thus, the reduction and Baba, K., 1979. 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Journal of the Marine Biological Association of the United Kingdom (2003)