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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 Records20169:32

DOI: 10.1186/s41200-016-0040-7

Received: 20 May 2016

Accepted: 3 June 2016

Published: 11 July 2016

Abstract

Background

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.

Results

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.

Conclusions

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.

Keywords

Biancolina japonica Amphipods Australia Burrowing

Background

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.

Methods

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.

Results

Systematics

Order AMPHIPODA Latreille, 1816

Family BIANCOLINIDAE J.L Barnard 1972

Genus Biancolina Della Valle, 1893

Biancolina japonica Ishimaru, 1996

(Figs. 1, 2, 3 and 4)
Fig. 1

Biancolina japonica Ishimaru, 1996, SEM image, upper specimen, male, 2.5 mm, AM P.98372, lower specimen, female, 2.2 mm, AM P.98370, Bare Island, Botany Bay, New South Wales, Australia. Scales 100 μm

Fig. 2

Biancolina japonica Ishimaru, 1996, SEM image, female, 2.2 mm, AM P.98370, male, 2.5 mm, AM P.98372, Bare Island, Botany Bay, New South Wales, Australia. Scales 20 μm

Fig. 3

Biancolina japonica Ishimaru, 1996, habitus, female, 3.1 mm, AM P.98555, Bare Island, Botany Bay, New South Wales, Australia. Scales A1, G1–2, P3–7, 0.05 mm, Ur1–3, T 0.1 mm

Fig. 4

Biancolina japonica Ishimaru, 1996, female, 3.1 mm, AM P.98555, Bare Island, Botany Bay, New South Wales, Australia. Scale 0.05 mm

Biancolina japonica Ishimaru, 1996: 398–403, Figs. 1, 2, 3 and 4.

Material examined

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).

Type locality

Sado Strait, Japan Sea (37°56'N 138°36'E).

Description

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).

Remarks

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.

Distribution

Japan (Ishimaru, 1996). Australia: Botany Bay and Tollgate Island, New South Wales (current study).

Discussion

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.
Table 1

Distribution and known host algae of all species of Biancolina. References are publications that include information on the macroalgal species inhabited by each species of Biancolina

Species

Type locality

Distribution

Host algae

References

B. algicola Della Valle 1893

Bay of Naples, Italy

Mediterranean Sea, Black Sea, Portugal

Cystoseira amantacea, C. barbata, C. foeniculacea, C. sauvageauana, C. spinosa, C. tamariscifolia, Phyllophora sp.

Ruffo & Wieser 1951; Krapp-Shickel 1993; Pereira et al. 2006; Tsytsugina 2011; Uzunova 2011

B. australis Nicholls 1939

Rottnest Island, Western Australia

Western Australia

  

B. brassicacephala Lowry 1974

Sargasso Sea

Gulf stream off south east USA, Sargasso Sea, Gulf of Mexico

Sargassum fluitans, S. natans

Fine 1970; Steele & Collard 1981; Stoner & Greening 1984; LeCroy 2002; Huffard et al. 2014

B. japonica Ishimaru 1996

Sado Strait, Japan Sea

Japan, Australia

Sargassum horneri, S. ilicifolium, S. linearifolium, S. vestitum.

Ishimaru 1996; Poore et al. 2000; Taylor & Steinberg 2005

B. lowryi Ortiz & Lalana 1996

Cayo Mendoza, Cuba

Cuba

Sargassum sp.

Ortiz & Lalana 1996

B. mauihina Barnard 1970

Kawela Bay, Hawaii

Hawaii, Fiji, Moluccas

Sargassum sp., Turbinaria sp., Ulva sp.

Barnard 1970; Ledoyer 1979; Myers 1985

B. obstusata Tzvetkova 1976

Possjet Bay

Sea of Japan

Cystoseira hakodatensis

Tzvetkova & Kudrjashov 1985

Not identified to species

 

North Carolina, USA

Sargassum filipendula

Duffy 1990

  

Japan

Sargassum confusum

Kito 1975

  

Florida, USA

Laurencia poiteaui

Lewis 1987

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).

Conclusions

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.

Declarations

Acknowledgements

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).

Authors’ contributions

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.

Authors’ information

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.

Competing interests

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Australian Museum Research Institute
(2)
Evolution & Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales

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Copyright

© Hughes and Poore 2016

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