Commensal Leucothoidae (Crustacea, Amphipoda) of the Ryukyu Archipelago, Japan. Part II: sponge-dwellers

Abstract Commensal leucothoid amphipods have been collected from the canals of their sponge hosts throughout the Ryukyu Archipelago, Japan. Eleven new species are described in the genus Leucothoe with valuable location data and host records. An identification key to sponge-dwelling Leucothoidae of the Ryukyu Archipelago is provided.


Introduction
The Leucothoidae are a marine family of gammaridean amphipods that can be found inhabiting sessile invertebrate hosts worldwide. The family currently contains 146 species in five genera and can be divided into two clades (White 2011, White andReimer 2012a). Leucothoids are typically found as endocommensal associates of spong-es, ascidians, and bivalve mollusks, where they utilize the feeding current produced by their hosts to feed (White 2011, White andReimer 2012a).
There are currently 14 Leucothoidae species reported from Japan, with only seven of these from the Ryukyu Archipelago (White and Reimer 2012a). A map of the study area is available in part 1 (White and Reimer 2012a).
Entire sponges were isolated in zip-lock plastic bags for subsequent dissection in the laboratory or amphipods were captured individually in situ using a modified squirt bottle (following Thomas andKlebba 2006, 2007). When possible, pieces of sponge were preserved in 99% EtOH. Sponges were tentatively identified by Nicole de Voogd (Naturalis, Leiden) via photos of sponges and sponge spicules and by referencing Allen and Steene (2002). Coral rubble samples were also taken, elutriated, and sieved on location using both saltwater and formalin washes. Samples were sorted immediately. Amphipods were preserved in 2% seawater buffered formalin for morphological analysis and 99% ethanol for molecular studies.
Specimens used for morphological analyses were transferred to glycerin, dissected, mounted on slides, and illustrated using a Nikon® Y-IDT drawing tube attached to a Nikon® Eclipse 50I compound microscope. Pencil drawings were scanned and digitally inked in Adobe® Illustrator using a Wacom® Tablet, following the methods of Coleman (2003).
Descriptions are of males unless noted with sexually dimorphic characters described in a separate section. Terminology used in descriptions follows White and Thomas (2009) with 'proximal margin' of the carpus and dactylus referring to the margins closing on the propodus. Setae nomenclature follows Oshel and Steele (1988) where possible without having SEM images for the specimens described here. All setae are simple, unless noted.
Type material and sponge pieces are deposited in the University of the Ryukyus Museum (Fujukan), with the prefix RUMF for museum numbers. Additional material has been deposited in the National Museum of Nature and Science in Tokyo, with the prefix NSMT for museum numbers.
Etymology. After the Japanese words 'aka', meaning 'red', and 'oni', meaning 'barbarian' and referring to the red color and large size (pronounced ah-ka-oh-nee).
Remarks. Leucothoe akaoni sp. n. is deep red in color, darkest on the head, fading to deep orange posteriorly ( Figure 23A). This species has been collected only on Yakushima Island, Kagoshima and from the northwestern coast of Okinawa-jima Island, Okinawa.
Etymology. After the Japanese place name, 'Bise', and referring to the type locality. (Pronounced bee-say.) Ecology. In canals of sponges, Tedania of Gray 1867 ( Figure 25E); and among coral rubble.
Remarks. Some sexually dimorphic characters may be due to the larger size of the female. Some specimens have larger serrations on the saw-like gnathopod 1 propodus palm, suggesting morphological variation in this character, perhaps depending on size. Leucothoe bise sp. n. is translucent orange in color ( Figure 24B). This species has been collected on Iriomote-jima and throughout the western coast of Okinawa-jima Island, Okinawa.
Etymology. Named for Dr. Daisuke Ueno, who collected the type specimens of this species. Dr. Ueno has shared valuable specimens and collection locations on Okinawa-jima Island.
Remarks. Leucothoe daisukei sp. n. is peach in color, darkest along pereonite edges ( Figure 23F). This species has been collected only on Ishigaki-jima Island and from 30 meters on the west coast of Okinawa-jima Island, Okinawa.
Etymology. Named for Sara E. LeCroy, in recognition of her contribution to amphipod taxonomy. Ms LeCroy has been a colleague and friend for the past 7 years and the first author is very grateful for all her support.
Remarks. Leucothoe lecroyae sp. n. is faint yellow in color ( Figure 23C). This species has been collected on Yakushima Island and Amami-oshima Island region (both Kagoshima) and from the northwestern and eastern coasts of Okinawa-jima Island, Okinawa, Japan.
Remarks. Leucothoe nagatekubi sp. n. is pinkish-orange in color ( Figure 24C). This species is endemic to the western coast of Okinawa-jima Island, Okinawa.
Remarks. Leucothoe nurunuru sp. n. is deep orange in color ( Figure 23D). This species is endemic to Iriomote-jima Island.
Etymology. After the Japanese place name 'Oura', meaning 'large inlet' and referring to the type locality. Relationships. Leucothoe ouraensis sp. n. is similar to Leucothoe ctenochasma Moore, 1987 in having gnathopod 1 dactylus reaching less than 0.1 × propodus length and a bidentate apex on the telson. This species differs from L. ctenochasma in having a truncate anterior head margin, quadrate anterodistal head margin, 1-articulate maxilla 1 palp, setose posterior margin on gnathopod 1 basis, and pereopods 5-7 bases broadly expanded and posteriorly smooth.
Remarks. Leucothoe ouraensis sp. n. is yellow-orange in color ( Figure 23E). This species is endemic to the eastern coast of Okinawa-jima Island, Okinawa.
Etymology. After the Japanese word 'togatta', meaning 'sharp' and referring to the sharply pointed projection on the ventral cephalic keel. (Pronounced toe-ga-ta) Ecology. In canals of hard brown sponge, yellow inside with groups of small holes on top, ?Jaspis of Gray, 1867 ( Figure 25C); and among coral rubble.
Relationships. Leucothoe togatta sp. n. is similar to Leucothoe ashleyae Thomas & Klebba, 2006 and Leucothoe saron Thomas & Klebba, 2007 in having a rounded head margin, a 2-articulate maxilla 1 palp, high mediofacial setal row on gnathopod 2 propodus, wide pereopod 5-7 bases, and a tridentate telson. It also shares long curved setae on the distal margin of gnathopod 2 basis with L. saron. It differs from these species in having a ventral cephalic keel that is anteriorly excavate and anteroventrally quadrate with a projection. Leucothoe togatta sp. n. shares these keel characteristics with Leucothoe amamiensis White & Reimer, 2012a and Leucothoe hashi sp. n., but differs from L. amamiensis in the distally truncate gnathopod 2 carpus, from L. hashi in the robustness of gnathopod 1 propodus and length of gnathopod 1 dactylus, and from both species in the long curved setae on gnathopod 2 basis and robust row of submarginal setae on the gnathopod 2 propodus.
Remarks. Leucothoe togatta sp. n. is white in color ( Figure 23G). This species has been collected only on Yakushima Island and from both western and eastern coasts of Okinawa-jima Island, Okinawa.
Remarks. Leucothoe toribe sp. n. is faint pink in color, darkest along pereonite edges ( Figure 23H). This species has been collected only on Yakushima Island, Kagoshima and from both western and eastern coasts of Okinawa-jima Island, Okinawa.
Etymology. After the Japanese place name 'Zanpa', meaning 'wave slicing' and referring to the type locality.
Remarks. Leucothoe zanpa sp. n. is white in color with faint purple stripes along pereonite edges ( Figure 23B). This species is endemic to Zanpa Cape on the western coast of Okinawa-jima Island, Okinawa.
Distribution. East China Sea: Okinawa-jima Island, Okinawa, Japan.     Antenna 1 accessory flagellum 1-articulate; mandibular palp article 3 shorter than article 1 and with 1 distal seta; maxilla 1 palp 1-articulate; gnathopod 1 basis anterior margin bare, carpus slender; pereopods 5-6 coxae without facial setae, pereopods 5-7 bases narrowly expanded ........... Leucothoe hashi -Antenna 1 accessory flagellum absent; mandibular palp article 3 subequal in length with article 1 and with 2 distal setae; maxilla 1 palp 2-articulate; gnathopod 1 basis anterior margin setose, carpus robust; pereopods 5-6 coxae with facial setae, pereopods 5-7 bases broadly expanded . Ventral cephalic keel anteroventral margin with strong anterior projection; antenna 1 accessory flagellum 1-articulate; mandibular palp article 3 with 1 distal seta; gnathopod 2 propodus mediofacial setal row above midline; characters. Due to the difficulty in identifying sponges and lack of sponge specialists in the Ryukyu Archipelago, tentative identifications, photos, and descriptive data are provided here and pieces of host sponges have been deposited in the University of the Ryukyus Museum (Fujukan). Most of the species reported here were collected from 1-4 sponge host species and from coral rubble. Presumably, these amphipods are inhabiting sponges in the crevices of the coral rubble. Perhaps the ephemeral nature of the sponges is also forcing the amphipods to adapt to new and available hosts, which may explain the higher number of species found in the genus Leucothoe than found in the anamixid clade of the Leucothoidae. Leucothoe nagatekubi sp. n., Leucothoe nurunuru sp. n., and Leucothoe zanpa sp. n. show higher specialization or host preference. Each of these species were collected from only one host at one location. With the exception of the large white ball sponge, Tetillidae ( Figure 24I), individual sponges hosted only one leucothoid species at each location. Leucothoe akaoni sp. n., Leucothoe daisukei sp. n., Leucothoe hashi sp. n., and Leucothoe zanpa sp. n. were collected from the same white ball sponge at Zanpa Cape.
The very high diversity of new leucothoid species discovered in the Ryukyu Archipelago to date supports the theory of Roberts et al. (2002), stating that Indo-Pacific reefs are the most diverse areas in the world with high levels of endemicity.