First report of polychaetes from the genus Oriopsis (polychaeta: Sabellidae) associated with the Japanese abalone Haliotis discus hannai and other native molluscs in Chile.

ABSTRACT The external morphology of sabellids polychaetes gathered from green abalone (H. discus hannai) and 2 species of Chilean native gastropods (Fissurella sp. and Concholepas concholepas) was studied. According to the taxonomic keys of Fauchald (1977) and Rozbaczylo (1980), all of these polychaetes belong to the family Sabellidae; subfamily Fabriciinae, and genus Oriopsis (according to Day 1967 and Fitzhugh 1989). This work constitutes the first report of the presence of sabellids of the genus Oriopsis forming tubes in the shell of the green abalone Haliotis discus hannai. The worms analyzed correspond to small sized sabellids (1-2 mm long). The body is fusiform, not sacciform like T. heterouncinata. The gill crown is constituted of three pairs of radiolae, unlike T. heterouncinata counting with 2 pairs of radiolae. Another important difference with this sabellid previously reported habiting abalone shells is the shape of the abdominal uncini, in Oriopsis are rasp-shaped plates, without main fang, defining a clear difference with the abdominal uncini acicular with a single main tooth crowned with shorter series of teeth, characteristic of T. heterouncinata.

KEY WORDS: abalone, boring polychaetes, eplbionts, Oriopsis, Concholepas, sabellid, shell damage

INTRODUCTION

Boring polychaetes frequently infest the shells of aquacultured mollusc species. These polychaetes can cause severe damage to the mollusc shells, affecting the fitness of their hosts (Blake & Evans 1973, Handley & Berquist 1997, Caceres-Martinez et al. 1998, Martin & Britayev 1998, Read 2004, McDiarmid et al. 2004) and often causing financial loss to aquaculturists. At least three families of boring polychaetes have been reported in the literature: Spionidae, Sabellidae, and Cirratulidae. In particular, boring polychaetes of the spionid genera such as Boccardia, Dipolydora, Polydora, and the sabellid Terebrasabella heterouncinata Fitzhugh and Rouse cause serious economic problems for the aquaculture industry at a global level (see Evans 1969, Kuris & Culver 1999, Lleonart et al. 2003a, 2003b, Cardenas & Canete 2004, Read 2004, Radashevsky & Olivares 2005).

The infestation in abalone shells caused by the sabellid Terebrasabella heterouncinata Fitzhugh & Rouse 1999 is a common problem for the abalone farmers. Until now, this was the only sabellid species recognized as the causative of serious shell damage caused by burrow formation. Terebrasabella heterouncinata was endemic to South Africa, infesting several sub and intertidal gastropods and became a pest on cultured abalones in South Africa and California in the early 1990s (Culver et al. 1997, Fitzhugh & Rouse 1999).

Moreno et al. (2006) published a complete list of boring polychaete species present in Chile, with a review of the information regarding each species' status as a native or non-indigenous species (NIS). They recorded a total of nine boring polychaetes present along the Chilean coast including native and NIS. The only sabellid registered in abalone in Chile at that time was Terebrasabella heterouncinata.

There are Oriopsis species registered in Chile: O. alata, O. alatoides, O. ehlersi, O. limbata, O. magellanica, and O. taltalensis. Like most of the worms belonging to this family are indirect deposit feeders as sedentary worms living in the sea bottom, none of this species has been described forming tubes in gastropod shells.

MATERIAL AND METHODS

To determinate the presence of sabellid polychaetes in native gastropods, a sample of 142 native gastropods of the species Concholepas concholepas (n = 62) and Fissurella sp. (n = 80) were obtained from a sublittoral area in central Chile (33[degrees]29'S, 71[degrees]38'W). On the other hand, a single sample of 345 green abalone Haliotis discus hannai was collected from an abalone farm in Central Chile, all these individuals belong to a single batch and were not considered in the productive scheme of the farm, they were maintained in a single tank for research purposes. The aim of the study was to determine the presence of sabellid polychaetes in a abalone farm in central Chile and its potential presence in the surrounding sea environment.

The initial study included all the mollusc species detected in the area surrounding the farm, including bivalves and gastropods. The sample points were defined as a 36-point grid in the coast next to the farm. Of this, only 2 gastropod species show the presence of sabellids (unpublished data), so for this study it decided to focus in both species: C. concholepas and Fissurella sp.

All of the individual were measured (total length) and the shells were separated from soft tissues to examine the inner and outer face of the shells seeking for abnormalities associated to sabellids infestation. This observation was conducted using a Leica stereomicroscope model S6D. Once the shell examination was finished, all the sabellid positive shells were separated and decalcificated using an acid solution (5% HN[O.sub.3]) for 12 h, and 5% NaS[O.sub.4] (12h) for acid neutralization (Vargas et al. 2005.).

The obtained material was separated from shell particles and observed in a Leica stereomicroscope model S6D. Once observed some basic anatomical features like segmentation, body shape, and gill crown presence; the polychaetes were fixed in 5% glutaraldehyde for scanning electronic microscope (SEM), to identify external structures with taxonomic importance, like the neuropodial thoracic hooks, very difficult to illustrate using conventional light microscopy. The microscope used for SEM was a Zeiss 940 model.

The three mollusc species studied (Figs. 1, 2) were analyzed in the same way, in the case of the native gastropods, because of the lack of information regarding the effect produced in the shell, all the shells were exposed to acid decalcification.

The taxonomic determination was carried out according to the keys of Fauchald (1977), Rozbaczylo (1980), and Day (1967).

RESULTS

The average length of the gastropod shells analyzed was 6.03 ([+ or -] 0.94) for Fissurella sp.; 5.05 ([+ or -] 1.18) for Concholepas concholepas and 5.04 ([+ or -] 0.55) for Haliotis discus hannai.

In the inner face of the shell of the examined abalones it was possible to detect the small tubules characteristic of sabellid infestations (Fig. 1), very similar to those generated for T. heterouncinata. Shell deformities related to the severe sabellid infestation were not observed. Of the abalones analyzed, 241 showed the presence of sabellid tubules on the inner face of the shells (70% of total sample). The mean intensity of tubes detected in the abalone sample was 2.6 per infected shell. The tubes were about 250 [micro]m wide and 2 mm length, these were distributed in the shell margin and also in the pores and central area of the inner face of the shell.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

In the case of the native gastropod examined (Fig. 2), they do not show the presence of sabellids tubules or shell deformities, but the shell decalcification allowed to collect many sabellids worms, counting 161 individuals in the total sample (76 obtained from C. concholepas and 85 from Fissurella sp.), corresponding to 1.22 worms per shell analyzed in case of C. concholepas and 1.06 in Fisurella sp. Giving the collection technique used, it is not possible to determine what part of the shell was being occupied by the sabellids.

The worms analyzed correspond to small sized sabellids (1-2 mm long). The body is fusiform (Figs. 3, 4, 5A), the gill crown is constituted of three pairs of radiolae, and it has 8 thoracic segments and 7-9 abdominal setigers. The thoracic notosetae are present in the setigers 2 8 (Fig. 5B). All of the thoracic neurosetae are long arm hooks with a single long tooth under another shorter tooth, crowned by many denticles (Fig. 5D). The neuropodial setae are not accompanied with bristles. The notopodial bristles of the abdomen (Fig. 5C) are subquadrangular uncinus with a short base containing approximately 8 lines of teeth with approximately 8 teeth on each (See Table 1).

[FIGURE 3 OMITTED]

DISCUSSION AND CONCLUSION

According to the keys of Fauchald (1977) and Rozbaczylo (1980), the analyzed worms belong to the family Sabellidae. Based on Day 1967 and Fitzhugh 1989, the thoracic neurosetae forming a single row of long handled hooks indicate that they belong to the subfamily Fabriciinae.

According to Day (1967) and Fitzhugh (1989) all the analyzed sabellids gathered from the mollusc shells described belong to the genus Oriopsis.

We conclude that the sabellid specimens found in H. discus hannai, Fissurella sp. and Concholepas concholepas in central Chile correspond to a single species of the genus Oriopsis.

This work constitutes the first report of the presence of sabellids of the genus Oriopsis forming tubes in the shell of the green abalone Haliotis discus hannai and the first record of sabellids associated with shells of two commercially important native gastropods, C. concholepas and Fissurella sp.

[FIGURE 4 OMITTED]

[FIGURE 5 OMITTED]

Apparently, the species of Oriopsis detected in this study is native and has a low preference by substrates because they were detected living in abalone shells, exotic mollusc, cultivated in Chile for more than a decade. Probably the low maintenance condition in which the abalone sampled for this study were kept in the tanks helped to increase the transmission of the sabellids between the individuals.

We suggest controlled infestations laboratory tests to elucidate the susceptibility of the abalones to Oriopsis infestations and the potential effects on the abalone production systems.

LITERATURE CITED

Blake, J. A. & J. W. Evans. 1973. Polydora and related genera as borers in mollusk shells and other calcareous substrates. Veliger 15:235-249.

Day, J. 1967. A monograph on the Polychaeta of Southern Africa. British Museum Nat. Hist. Publ. 656:878 pp.

Caceres-Martinez, J., P. Macias-Montes de Oca & R. Vasquez-Yeomans. 1998. Polydora sp. infestation and health of the pacific oyster Crassostrea gigas in Baja California, NW Mexico. J. Shellfish Res. 17:259-264.

Cardenas, C. & Canete J. 2004. Poliquetos polidoridos perforadores y su impacto en el cultivo de moluscos marinos en Chile. Revista Austro Universitaria, No. 15, 2004.

Culver, C. S., A. M. Kuris & B. Beede. 1997 Identification and management of exotic sabellid pests in California abalone aquaculture. California Sea Grant College Program. Publication No. T-041.36 pp.

Evans, J. 1969. Borers in the shells of the sea scallop, Placopecten magellanicus. Am. Zool. 9:775-782.

Fauchald, K. 1977. The Polychaete worms. Definitions and keys to the Orders, Families and Genera. Natural History Museum of Los Angeles County. Science Series 28:1-190.

Fitzhugh, K. 1989. A systematic revision of the Sabellidae-Caobangiidae-Sabellogidae (Annelida: Polychaeta). Bull. Am. Mus. Nat. Hist. 192:1-104.

Fitzhugh, K. & G. Rouse. 1999. A remarkable new genus and species of fan worm (Polychaeta: Sabellidae: Sabellinae) associated with marine gastropods. Invertebrate Biology 118: 357-390.

Handley, S. J. & P. R. Berquist. 1997. Spionid polychaete infestations of intertidal pacific oysters Crassostrea gigas (Thunberg), Mahurangi Harbour, northern New Zealand. Aquaculture 153:191-205.

Kuris, A. M. & C. S. Culver. 1999. An introduced sabellid polychaete pest infesting cultured abalones and its potential spread to other California gastropods. Invertebr. Biol. 118:391-403.

Lleonart, M., J. Handlinger & M. Powell. 2003a. Treatment of spionid mud worm (Boccardia knoxi Rainer) infestation of cultured abalone. Aquaculture 217:1-10.

Lleonart, M., J. Handlinger & M. Powell. 2003b. Spionid mud worm infestations of farmed abalone (Haliotis spp.). Aquaculture 221:85-96.

Martin D. & T. A. Britayev (1998) Symbiotic polychaetes: review of known species. Oceanog. Mar. Biol.: Ann. Rev. 36:217-340.

McDiarmid, H., R. Day & R. Wilson. 2004. The ecology of polychaetes that infest abalone shells in Victoria, Australia. J. Shellfish Res. 23:1179-1188.

Moreno, R., P. Neill & N. Rozbaczylo. 2006. Native and non-indigenous boring polychaetes in Chile: a threat to native and commercial mollusc species. Rev. Chil. Hist. Nat. 79:263-278.

Radashevsky V. I. & Olivares C., 2005. Polydora uncinata (Polychaeta: Spionidae) in Chile: an accidental transportation across the Pacific. Biol. Invasions 7:489-496.

Read, G. 2004. Guide to New Zealand shell polychaetes. National Institute of Water and Atmospheric Research, New Zealand (NIWA). Web publication, http://biocollections.org/pub/worms/nz/ Polychaeta/ShellsPoly/NZShellsPolychaeta.htm.

Rozbaczylo, N. 1980. Clave para el reconocimiento de familias de Anelidos poliquetos del mar chileno. Stud. Neotrop. Fauna and Environm. 15:167-196.

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FABIAN AVILES, (1) * NICOLAS ROZBACZYLO, (2) MARCELO HERVE (1) AND MARCOS GODOY (1)

(1) Aquagestion, Panamericana Sur 581, Puerto Montt, Chile, (2) Departamento de Ecologia, Facultad de Ciencias Biologicas, Pontificia Universidad Catolica de Chile, Alameda 340, Santiago

* Corresponding author. E-mail: [e-mail]

TABLE 1.
The main morphological differences between Terebrasabella
heterouncinata and the Oriopsis species detected in the
present work.

Terebrasahella heterouncinata                 Oriopsis Sp.

Branchial crown with 2 pairs of     Branchial crown with three to
  radioles                            five pairs of radioles
The anterior half of the body is    The body is thicker in the
  thinner than the rest               middle.
The posterior half of the body is   The posterior half of the body is
  lightly expanded                    pointed
Sacciform                           Fusiform
With 8 thoracic segments            With 8 thoracic segments
With 3 abdominal segments           Abdomen with seven to nine
                                      setigers
Neuropodial uncini of setigers      Inferior thoracic notosetae are
  2-6 are acicular and have a         bayonet setae, situated as
  main tooth crowned by shorter       simple row roughly parallel
  teeth series                        and posterior to superior
Neuropodial uncini of setigers 7      notosetae. Thoracic uncini
  and 8 are avicular, without         acicular: teeth above main fang
  main tooth, all the teeth with      unequal in size: hood present
  a uniform size
Companion setae absent in the       With companion setae in the
  neuropods in the setigers 7         neuropods of the setigers 7
  and 8                               and 8
Abdominal notopodial uncini are     Abdominal uncini as rasp-shaped
  present in the setigers 9-11        plates, without main fang.
Abdominal notopodial uncini are     Abdominal neurosetae situated as
  acicular with a single main         simple row of modified,
  tooth crowned with shorter          elongate, narrowly hooded setae
  series of teeth