Marine Record | Open | Published:
Biancolina japonica Ishimaru 1996: first record of this burrowing amphipod from Australia and a review of host use in the genus Biancolina (Amphipoda: Peracarida: Crustacea)
Marine Biodiversity Recordsvolume 9, Article number: 32 (2016)
Biancolina Della Valle (Monograpie 20:1893) are minute amphipods that bore tunnels into algal tissue. Their global distribution and diversity are poorly known due to their small size and concealed habit.
Biancolina japonica Ishimaru (J Crust Biol 16:395–405, 1996) is reported from Bare Island, Botany Bay, New South Wales, Australia and is only the second species of Biancolina recorded in Australian waters following B. australis Nicholls (Rec South Aust Mus 6:309–334, 1939). B. japonica is found exclusively on species of Sargassum where it burrows into algal tissues to feed.
We report Biancolina japonica Ishimaru (J Crust Biol 16:395–405, 1996), previously known only from Japan, for the first time in Australian waters. A review of the known algal hosts of all eight species of Biancolina indicates high levels of feeding specialisation on brown algae from the order Fucales.
Biancolina Della Valle, 1893 are minute amphipods, usually less than 2 mm as adults, that bore tunnels into algal tissue. Eight species of Biancolina have been recorded world-wide, from the Sea of Japan, Hawaii, Caribbean Sea, Mediterranean, Sargasso Sea and southern Australia. Diversity in the genus Biancolina is most likely under-represented owing to their small size and concealed habit. Here, we report Biancolina japonica Ishimaru, 1996, previously known only from Japan, for the first time in Australian waters.
Biancolina japonica was found exclusively on two species of Sargassum, S. linearifolium (Turner) C. Agardh 1820 and S. vestitum (Turner) C. Agardh 1820 as part of a wider survey of algal associated amphipods (Poore et al., 2000). While feeding on algal material is common across many amphipod taxa, few are known to burrow into algal tissues and feed internally (Mejaes et al. 2015). Apart from Biancolina, these include members of the Eophliantidae (Lorz et al. 2009), Najna Derzhavin, 1937 and Carinonajna Bousfield & Marcoux, 2004 from the Najnidae (Bousfield and Marcoux 2004) and Amphitholina cuniculus (Stebbing, 1874), Peramphithoe stypotrupetes Conlan & Chess, 1992 and P. lessionophila Conlan & Bousfield, 1982 from the Ampithoidae (Conlan and Chess 1992; Gestoso et al. 2014). These burrowing amphipods have convergent morphologies, sharing a subglobular head, small and compact bodies and stout pereopods (Mejaes et al. 2015).
Until this study, B. australis Nicholls, 1939 was the only known species for the genus in Australian waters, described from south Western Australia. Biancolina australis has uropods 1 and 2 rami subequal in length which readily distinguishes it from other Biancolina species. Ishimaru (1996) indicated this species should warrant its own genus, yet refrained from making a formal change in status, as type material of this species is lost. Recent museum collections from Western Australia have not turned up specimens of Biancolina (LEH pers. Obs; Peart 2004), yet this is to be expected for such small cryptic fauna. This paper is the first step to encouraging more work on small burrowing amphipods, reporting B. japonica from Botany Bay, New South Wales Australia and reviewing known algal hosts for all species in the genus.
Material is lodged in the Australian Museum, Sydney (AM). Specimens were dissected in 80 % ethanol. Illustrated were made from a temporary slide mount, except for mouthparts, where permanent slides were made using Aquatex™ mounting agent. Specimens were prepared for electron microscopy as follows: specimens were sonicated in a 10 % solution of the surfactant TWEEN 80 to remove detritus before being transferred back to 80 % ethanol; preserving solution was sequentially advanced in 5 % increments from 80 % to 100 % ethanol; critical point dried; mounted individually on pins and gold sputter coated. Images were captured using on a Zeiss EVO LS15 Scanning Electron Microscope with Robinson Backscatter Detector (SEM). Diagnoses are provided in bold text within the descriptions. Standard abbreviation on the plates are: A, antenna; C, coxa; Ep, epimeron; G, gnathopod; Md, mandible; Mx, maxilla; Mxp maxilliped; P, pereopod; T, telson; U, uropod; Ur, urosome; L, left and R, right.
Order AMPHIPODA Latreille, 1816
Family BIANCOLINIDAE J.L Barnard 1972
Genus Biancolina Della Valle, 1893
Biancolina japonica Ishimaru, 1996
Female, 3.1 mm, dissected (urosome and carcass in microvial), 1 slide (mouthparts), AM P.98555; b female, 3.0 mm, dissected (carcass in microvial), 1 slide (head and mouthparts), AM P.98556; 1 male specimen, 2.5 mm, whole animal pin mount, AM P.98372; 1 ‘a’ female specimen, 2.2 mm, whole animal pin mount, AM P.98370; 1 ‘b’ female specimen, 2.4 mm, whole animal pin mount, AM P.98371; 25 specimens, AM P.42974, Bare Island, Botany Bay, New South Wales, Australia (34°00'S, 151°14'E), 2 m, brown alga Sargassum linearifolium (Turner) C. Agardh 1820, 4 May 1994, coll. A.G.B. Poore; 1 male, AM P.72591, west side of North Tollgate Island, New South Wales, Australia, (35°44'50"S, 150°15'28"E), 11 m, red calcareous Corallina berteri Montagne 1849, scattered low reefs, rocks and sand, 8 February 2003, coll. P.B. Berents, J. Eu, A.J. Millar and G.D.F. Wilson (Australian Museum, Marine Invertebrate station MI NSW 2019).
Sado Strait, Japan Sea (37°56'N 138°36'E).
Based on female specimen, 3.1 mm, AM P.98555.
Body cylindrical, head subglobular. Antennae 1peduncle article 1 length 1.1 x width; article 2 length 3 x width, 1.7 x article 1 length; article 3 length twice width, subequal to article 1 length; flagellum 8-articlulate (male AM P. 98372, 13–15 articulate). Antennae 2 less than half length of antennae 1, peduncule article 4 length 1.5 x width, slightly longer than article 5; flagellum 3-articlulate. Upper lip broader than long, ventral margin rounded. Mandible incisors with 6 teeth. Maxilla 1 inner plate reduced, apically rounded with 1 lateral slender seta; outer plate with 8 setal teeth, palp absent. Maxilla 2 inner plate slender with 2 lateral and 4 apical slender setae; outer plate broad, longer than inner plate, apically rounded with 10 apical slender setae. Maxilliped small; inner plate narrow, not reaching extent of outer plate, with 2 long apical setae; outer plate with slender apical setae; palp exceeding outer plate, article 2 with medial lobe, article 4 broad.
Coxae 1–4 similar in size. Gnathopod 1 parachelate, coxa 1 subquadrate, ventral margin straight; carpus subtriangular, length 1.2 x width; propodus length 2.6 x width, palm transverse, entire, straight; dactylus overreaching palm (twice length of palm), posterior margin with slender seta, unguis present. Gnathopod 2 similar to gnathopod 1, parachelate, coxa 2 subquadrate, basis stout, length twice width; ischium long, subequal to merus length; carpus subtriangular, length 1.2 x width; propodus length 2.6 x width, longer than gnathopod 1 propodus, palm transverse, distally convex, dactylus overreaching palm, unguis present. Pereopods 3–4 similar, coxa ventral margin convex; basis subovate, length 1.2 x width; ischium, merus, carpus and propodus subequal in length; merus anterior margin expanded with single long anterodistal seta. Pereopods 5–7 similar, coxa anterior lobe well-developed (decreasing in size from coxa 5 to 7); basis subovate length 1.1 x width; ischium, merus and carpus subequal in length; propodus weakly prehensile, distally expanded, length 4 x width, palm with 1 large robust setae; dactylus with unguis present. Epimera 1–3 shallow, posterior and ventral margins convex. Urosome dorsoventrally flatterned, urosomite 1 largest; urosomite 3 fused with telson. Uropod 1 peduncle length 1.5 x width, lateral margins lined with long plumose setae; outer ramus length 3 x width, half length of inner ramus with single apical slender seta; inner ramus length 3.5 x width, with 2 apical slender setae. Uropod 2 peduncle long, length 3.3 x width, lateral margin with setae; outer ramus length 2.5 x width, less than half length of inner ramus with single apical slender seta; inner ramus length 4.2 x width, with 1 distolateral and 2 apical slender setae. Uropod 3 peduncle broad, length 1.1 x width, lateral margin without setae, outer ramus length twice width, subequal to inner ramus, with 2 recurved robust setae; inner ramus with 1 recurved robust setae. Telson subovate, tissue fleshy, apically notched/incised (note: notch not observable in SEM images).
Biancolina japonica Ishimaru, 1996 may be separated from B. australis Nicholls, 1939, which also occurs in Australian waters, by the uropod 1 and 2 which have a shorter outer ramus, while the rami are subequal in B. australis. The coxae 1 to 2 ventral margin is reported as convex in the original description of B. japonica. SEM prepared specimens from Port Jackson include individuals with straight and convex coxal margins. As the genus is not heavily calcified and the tegument supple, this feature is now considered an artefact of tissue movement and not a species level character.
Japan (Ishimaru, 1996). Australia: Botany Bay and Tollgate Island, New South Wales (current study).
Specimens attributed to B. japonica are now reported from Japan and Australia. This small cryptic living species may represent a widely distributed taxon, a species complex or potentially an invasive species of unknown geographic origin. There is potential for widespread dispersal of these algal associated invertebrates on rafting material of their Sargassum hosts. Another species in the genus, B. brassicacephala, occurs largely on floating Sargassum in the Sargasso Sea and Gulf of Mexico (Table 1). Broader sampling and genetic study is required to investigate relationships among these morphologically similar populations.
Biancolina japonica is found within burrows that run lengthwise in the fronds of Sargassum. The burrows can extend for over 10 mm and have a diameter that is close to the thickness of the frond. Once complete, the sides of these burrows can become eroded leaving an empty slot that runs parallel to the main axis of the frond. Any individuals that have become disassociated from their algal host following collection have been observed to rapidly initiate a new burrow on contact with an algal frond. The burrowing starts in a central position on the frond and within minutes the individual amphipod has burrowed within the algal tissues.
In the shallow subtidal algal beds of the Sydney region, Biancolina japonica is found exclusively on two species of Sargassum (Poore et al. 2000). Such feeding specificity is rare among herbivorous amphipods (Poore et al. 2008). A review of host use of all known species of Biancolina, however, indicates that the genus as a whole displays a very restricted range of algal hosts (Table 1). Almost all records of Biancolina derive from collections of brown algae from just two genera, Sargassum and Cystoseira, both from the Sargassaceae in the order Fucales (Table 1). These hosts differ from those used by other burrowing amphipods, with Amphitholina cuniculus (Ampithoidae) recorded from Fucus and Bifurcaria (Fucales) (Gestoso et al. 2014), Peramphithoe stypotrupetes and P. lessionophila (Ampithoidae) from kelps (Laminariales) (Conlan and Chess 1992), Najna and Carinonajna (Najnidae) recorded from a wide variety of seagrasses and kelps (Bousfield and Marcoux 2004) and species from the Eophliantidae from kelps and Carpophyllum (Fucales) (Lorz et al., 2009).
Biancolina japonica, previously known only from Japan, is reported for the first time in Australian waters. Like other members of the genus, B. japonica burrows into the blades of brown algae and feeds from within those burrows. In contrast to most herbivorous amphipods, which are generalist consumers and found on many genera of host algae, this species is found almost exclusively on algae from one genus (Sargassum). A review of the known algal hosts of all eight species of Biancolina indicates high levels of host specialisation, with nearly all records derived from few genera of brown algae in the order Fucales.
Agardh, CA. Species algarum rite cognitae, cum synonymis, differentiis specificis et descriptionibus succinctis. Volumen primum. Pars prima. pp. [i-iv], -168. Lundae [Lund]: ex officina Berlingiana. 1820.
Barnard JL. Sublittoral Gammaridea (Amphipoda) of the Hawaiian Islands. Smithson Contr Zool. 1970;34:1–286.
Barnard JL. The marine fauna of New Zealand: algae-living littoral Gammaridea (Crustacea Amphipoda). NZ Oceanogr Inst Mem. 1972;62:1–216.
Bousfield EL, Marcoux P. The talitroidean amphipod family Najnidae in the North Pacific region: systematics and distributional ecology. Amphipacifica. 2004;3:3–44.
Conlan KE, Bousfield EL. The amphipod superfamily Corophioidea in the northeastern Pacific region, Family Ampithoidae: systematics and distributional ecology. National Museum of Natural Sciences (Ottawa). Publ Biol Oceanogr. 1982;10:41–75.
Conlan KE, Chess JR. Phylogeny and ecology of a kelp-boring amphipod, Peramphithoe stypotrupetes, new species (Corophioidea: Ampithoidae). J Crust Biol. 1992;12:410–22.
Della-Valle A. Gammarini del Golfo di Napoli. Fauna und Flora des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Monograpie 20. 1893;1–948.
Derzhavin AN. Talitridae of the Soviet coast of the Japan Sea. Akademiya Nauk SSSR, Issledovaniya Fauny Morei. 1937;23:87–99.
Duffy JE. Amphipods on seaweeds: partners or pests? Oecologia. 1990;83:267–76.
Fine ML. Faunal variation on pelagic Sargassum. Mar Biol. 1970;7:112–22.
Gestoso I, Olabarria C, Troncoso JS. Selection of habitat by a marine amphipod. Mar Ecol. 2014;35:103–10.
Huffard CL, von Thun S, Sherman AD, Sealey K, Smith Jr KL. Pelagic Sargassum community change over a 40-year period: temporal and spatial variability. Mar Biol. 2014;161:2735–51.
Ishimaru S. Taxonomic review of the family Biancolinidae (Amphipoda: Gammaridea), with description of a new species from Japan. J Crust Biol. 1996;16:395–405.
Kito K. Preliminary report on the phytal animals in the Sargassum confusum region in Oshoro Bay, Hokkaido. J Faculty Sci, Hokkaido University. 1975;20:141–58.
Krapp-Shickel G. Do algal-dwelling amphipods react to the ‘critical zones’ of a coastal slope? J Nat Hist. 1993;27:883–900.
Latreille PA. Crustacés, Arachnides et partie des Insectes. In: Cuvier G, Le Règne, editors. Animal, distribué d’après son organisation, pour servir de base a l’histoire naturelle des animaux et d’introduction à l’anatomie comparée. Nouvelle édition, revue et augmentée. Paris: Tome IV; 1816. p. 1–584.
LeCroy SE. An illustrated identification guide to the nearshore marine and estuarine gammaridean Amphipoda of Florida. Volume 2. Families Ampelisicidae, Amphilochidae, Ampithoidae, Aoridae, Argissidae and Haustoridae. State of Florida Department of Environmental Protection, Talahassee. 2002.
Ledoyer M. Expédition Rumphius II (1975) Crustacés parasites, commensaux, etc. (Th. Monod et R. Serène, éd.) VI. Crustacés Amphipodes Gammariens. Bulletin du Muséum National d’Histoire Naturelle, Paris, 4e série 1, 1979; section A 1:137–181.
Lewis III FG. Crustacean epifauna of seagrass and macroalgae in Apalachee Bay, Florida, USA. Mar Biol. 1987;94:219–29.
Lorz AN, Kilgallen NM, Thiel M. Algal-dwelling Eophliantidae (Amphipoda): description of a new species and key to the world species, with notes on their biogeography. J Mar Biol Assoc UK. 2009;90:1055–63.
Lowry JK. A new species of the amphipod Biancolina from the Sargasso Sea. Trans Am Microsc Soc. 1974;93:71–8.
Mejaes B, Poore AGB, Thiel M. Crustaceans inhabiting domiciles excavated from macrophytes and stone. In Thiel M, Watling L, editors. Life styles and feeding biology of the Crustacea. Volume II in the Natural History of the Crustacea. Oxford, United Kingdom: Oxford University Press. 2015; p. 118–139.
Montagne C. Sixième centurie des plantes cellulaires nouvelles tant indigènes qu’exotiques. Annales des Sciences Naturelles Vol. 12; No. Botanique Série 1849; 3:285–320.
Myers AA. Shallow-water, coral reef and mangrove Amphipoda (Gammaridea) of Fiji. Rec Aust Mus Suppl. 1985;5:1–143.
Nicholls GE. The Prophliantidae. A proposed new family of Amphipoda, with description of a new genus and four new species. Rec South Aust Mus. 1939;6:309–34.
Ortiz M, Lalana R. Los anfípodos de la primera expedición conjunta Cuba-USA, abordo del B/I” Ulises”, a las Aguas del Archipielago Sabana-Camagüey, Cuba en 1994. Anales del Instituto de Biología serie Zoología. 1996;67:89–101.
Peart RA. Amphipoda (Crustacea) collected from the Dampier Archipelago, Western Australia. Rec West Aust Mus Suppl. 2004;66:159–67.
Pereira SG, Lima FP, Queiroz NC, Ribeiro PA, Santos AM. Biogeographic patterns of intertidal macroinvertebrates and their association with macroalgae distribution along the Portuguese coast. Hydrobiologia. 2006;555:185–92.
Poore AGB, Watson MJ, de Nys R, Lowry JK, Steinberg PD. Patterns of host use in alga- and sponge-associated amphipods. Mar Ecol Prog Ser. 2000;208:183–96.
Poore AGB, Hill NA, Sotka EE. Phylogenetic and geographic variation in host breadth and composition by herbivorous amphipods in the family Ampithoidae. Evolution. 2008;62:21–38.
Ruffo S, Wieser W. Osservazioni sistematiche ed ecologiche su alcuni Anfipoi delle coste mediterranee italiane. Mem Mus Civ Stor Nat Verona. 1951;3:11–30.
Stebbing TRR. On some species of Amphithoe and Sunamphithoe. Annals and Magazine of Natural History Series 4. 1874;14:111–8.
Steele P, Collard S. First Gulf of Mexico record for Biancolina brassiacephala (Amphipoda Biancolinidae). Northeast Gulf Sci. 1981;4:115–8.
Stoner AW, Greening HS. Geographic variation in the macrofaunal associates of pelagic Sargassum and some biogeographic implications. Mar Ecol Prog Ser. 1984;20:185–92.
Taylor RB, Steinberg PD. Host use by Australasian seaweed mesograzers in relation to feeding preferences of larger grazers. Ecology. 2005;86:2955–67.
Tsytsugina VG. Principles of ecological risk assessment to epiphyton by cytogenetic criteria. Mar Ecol Journal. 2011;10:86–90.
Tzvetkova NL. New species of Dexaminidae, Phliantidae and Biancolinidae, warm-water elements of the Possjet Bay fauna (Sea of Japan)]. Zoologichesky Zhurnal. 1976;55:684–95.
Tzvetkova NL, Kudrjashov VA. On the fauna and ecology of gammarids (Amphipoda, Gammaridea) in the biocoenoses of the upper parts of the shelf of the South Sakhalin. Issledovanija Fauny Morei. 1985;30:292–345.
Uzunova S. Higher crustaceans in the upper sublittoral zone along the Bulgarian Black Sea coastal area, Proc. Of the Union of Scientists–Varna, Marine Sciences. 2011. p. 67–76.
We thank two anonymous reviewers whose comments improved this manuscript.
Availability of data and material
The specimens of B. japonica examined in this study are held in the Australian Museum (voucher numbers AM P.98556, AM P.98372, AM P.98370, AM P.98371, AM P.42974, and AM P.72591).
LEH and AGBP conceived of the study. LEH prepared the figures and species description. AGBP reviewed the ecological literature. LEH and AGB wrote the manuscript. Both authors read and approved the final manuscript.
LEH is a Research Fellow at the Australian Museum with research interests in crustacean systematics. AGBP is an Associate Professor at the University of New South Wales, Australia, with research interests in the ecology and evolution of marine invertebrates, seagrasses and macroalgae.
The authors declare that they have no competing interests.