The ecology of polychaetes that infest abalone shells in Victoria, Australia.

ABSTRACT Very little is understood regarding polychaete borers and the effect they have on their hosts. In Victoria and elsewhere in Australia many stunted populations of Haliotis rubra have extensively bored shells. This study investigated the infestation by polychaetes of abalone shells and their effect on the health and growth of abalone. Polychaete numbers were estimated by providing diatom food so that they emerged. Borers were most prevalent in the spire region and near closed respiratory pores. In larger H. rubra shells, the frequency of polychaete borers increased and borers were present in more parts of the shell. Experiments showed that uninfested H. rubra and H. laevigata shells from a hatchery could be colonized by Polydora woodwicki and Dipolydora armata from infested abalone over short periods in the laboratory. Live specimens of P. woodwicki were observed for the first time. Larger shells of H. rubra were found to be more susceptible to polydorid infestation than large H. laevigata or small H. rubra, apparently because they provide more suitable sites for settling larvae. Larvae from both species colonized specific places on abalone shells. X-ray photographs were used to determine burrow shapes of Boccardiella MoV 3840, Polydora woodwicki, and Dipolydora armata, which have not been previously described. Boccardiella MoV 3840 was found to cause the host abalone to form mud blisters. Rates of burrow growth could be determined using sequential x-rays. High levels of boring were correlated with shell thickness and had a detrimental effect on several condition indices of host abalone, showing that borers have marked detrimental effects on the health and growth of abalone. Thus borers may severely affect fishery yield and productivity.

KEY WORDS: parasite-host interaction, host susceptibility, shell parasites, polydoridae, burrow morphology, burrow growth, abalone productivity

INTRODUCTION

Blacklip abalone Haliotis rubra (Leach) are the most abundant abalone species in Victoria and are the basis for a lucrative fishing industry, worth over $58 million a year in Victoria in 1999 to 2000 (ABARE 2001). This species is also important to the rapidly developing Victorian abalone aquaculture industry. H. rubra are known to host a variety of organisms that bore through their shells (Shepherd & Breen 1992). Greenlip abalone (H. laevigata, Donovan), which support important commercial fisheries elsewhere in Australia, appear to be less often affected. The major species responsible for this boring belong to the family Spionidae (Annelida: Polychaeta) (Blake & Evans 1973). These polychaete borers, known as polydorids, may have important consequences for the biology of the hosts, and thus for the economics of the fishery and mariculture. At this stage however, there is little hard data to assess these claims.

Most research on shell borers is either taxonomically based or ecologically based. Taxonomic studies often concentrate on one species of boring organism and regularly do not record the host species or the effect on the host. Ecologic studies frequently seem to provide inaccurate descriptions and records of the species of boring organisms present (e.g., Smyth 1990). In either case, information is lost.

Polydorids produce eggs in capsules attached to the burrow, often in strings, and the larvae usually hatch at the 3 setiger stage and develop in the plankton before settlement, but some species are lecithotrophic (Blake & Woodwick 1975, Woodwick 1977, Day & Blake 1979, Sato-Okoshi et al. 1990). The settlement and burrowing behavior of polydorids is poorly understood considering their prevalence in easily studied tidal and subtidal environments and their significance to commercial fisheries (Blake 1996). Blake (p. 85) stated "we know little about how species initially become established in such a habitat (mollusc shells), the mechanism by which they expand their burrow, how they feed and how they interact with their hosts."

The impact of borers on commercially important bivalves depends on the site of colonization of the host shell (Blake & Kudenov 1978). Preferences for mollusc hosts and the effects of host size or encrusting algae on colonization by borers are also not currently understood. To understand the relationship between polydorids and abalone, one needs to determine how they become established in a shell, and the factors affecting establishment.

Burrowing by polydorids was initially believed to be carried out mechanically by the chaetae, in particular the modified chaetae of the filth chaetiger (Blake & Evans 1973). The most recent evidence however, suggests chemical breakdown of the shell instead of a mechanical process (Haigler 1969, Zottoli & Carriker 1974, Sato-Okoshi 1997). The burrows are not often seen to penetrate the inner surface of their host's shell and do not have any direct contact with the host animal, but this seems to be because the burrowing activity induces the host to secrete a protective layer of dark conchiolin, followed by a nacreous shell layer, on the inside of the shell (Haigler 1969, Kent 1979, Blake 1996, Marshall & Day 2001). High levels of burrowing cause some molluscs, including abalone, to significantly increase the shell thickness (Marshall & Day 2001). This repair response, of the mollusk, to holes penetrating the shell takes considerable time to complete (Thomas & Day 1995) and has been suggested to affect the health of the animal and even slow its growth (Kent 1979, Kojima & Imajima 1982, Handley & Berquist 1997, Handley 1998).

The burrows end at two exterior apertures from which the worm feeds (Blake 1996). The boring activities of polydorids result in simple U-shaped burrows, Y-shaped burrows, pear-shaped, complex branching burrows, shallow depressions, or mud blisters (Blake & Evans 1973, Blake 1996). Burrow shape and size is also believed to be a factor in the effect of the borers on the host mollusc (Blake & Evans 1973, Zottoli & Carriker 1974). The rate of boring of different species may also determine the effect on the host mollusc (Zottoli & Carriker 1974).

There is little known about infestation of abalone (Haliotis spp.) by polydorids. A preliminary study (McDiarmid & Wilson, unpublished data) has identified several polydorid species in abalone that do not match any species known for Australia. This, and their presence only near major shipping ports, suggests some may be introduced as "exotic" species. Further taxonomic work is required to establish whether this is the case. The effect on the abalone is believed to increase with the degree of infestation (Blake & Evans 1973, Kojima & Imajima 1982). Abalone with shells weakened by many burrows would provide easier prey for large predators such as fish, stingrays, and octopus (Shepherd & Breen 1992).

This study examines the host-parasite relationship between boring polydorids and H. rubra and H. laevigata, in particular the effect of infestation on H. rubra. New methods are described that can be used to examine colonization behavior and the growth and morphology of the burrows formed and to measure the effect on the host.

MATERIALS AND METHODS

Extraction and Identification

Polychaetes were extracted from abalone shells by placing them in a 50% alcohol, 50% seawater mix. This method caused the worms to either escape their burrows completely and then die where they could be easily collected, or at least expose themselves out of their burrows where they could be extracted manually. An interactive key was constructed (Wilson & McDiarmid 2004), and used in conjunction with a review of the spionids present in southern Australia by Blake & Kudenov (1978) to identify the key features of these taxa.

Pattern of Infestation of Abalone Shells

Seventy abalone of varying sizes collected from Point Cook reef were used to determine whether the area of the shell and/or the level of encrusting algal cover were correlated with the number of polydorids present in the shell. The number of polydorids was determined by placing abalone shells in fresh seawater, to which dead diatoms were added to encourage the feeding behavior of the worms, and observing them under a stereo microscope. Polydorids are easily observed even to the naked eye when they are feeding, because their palps are distinctive (Fig. 1).

[FIGURE 1 OMITTED]

To determine the pattern of infestation over the shell, shells were divided into three sections: the spire, the area between the ostia and columella and the flat section of the body whorl between the spire and the growing margin (Fig. 2). Each section was observed for a period of 5 min. Counts on every fifth abalone were repeated and the standard deviation of counts was found to be very low (SD = 2.77). Algal cover was graded using a scale devised by Smyth (1989). Areas of shells and sections of shells were determined by wrapping the shells in graph paper and counting squares.

[FIGURE 2 OMITTED]

The polychaetes were extracted from 15 juvenile (30-60 mm) and 15 adult (>80 mm length) H. rubra and identified, to determine any host preferences of the polydorid species.

Colonization of Abalone Shells by Polydorids

Haliotis rubra infested with borers were collected from a depth of 3-4 m off the south eastern boundary of the Point Cook Marine Park in Port Phillip Bay, or at "Fred's Wall," 50 m offshore from the breakwater at Williamstown beach. Several shells from each sample of abalone were set aside and the worms were extracted for identification. One hundred and eighty juveniles of H. rubra and H. laevigata Donovan, free from borers, were purchased from an abalone mariculture facility for the colonization experiment. All abalone were wrapped in damp towels and placed in cool boxes during transport and left for 1 wk in the aquarium system to acclimatize before experiments. Injured or dying animals were eliminated.

To investigate the colonization behavior of borers and the susceptibility of abalone species to colonization by polydorid larvae, "recipient" hatchery abalone without borers were placed in contact with infested wild abalone from Point Cook reef ("source" abalone) carrying a known number of polychaetes. Recipient abalone were all checked to make sure no boring polydorids were present. They were then placed in either direct or indirect contact with infested abalone, using tanks either containing infested abalone or receiving water from a tank containing an infested source abalone. This experiment was conducted in tanks provided with flowing seawater from a large cooled recirculating seawater system, with temperature ranging from 11[degrees]C to 15[degrees]C.

Eighteen abalone with 30 to 40 polydorids present in the shell were used as source abalone in the "direct" colonization treatments. Three abalone that had ~180-220 polydorids were selected to be used as source abalone in the "indirect" colonization treatments. Several shells from the same sample were set aside and the polychaetes were extracted for identification.

In each of the 9 direct colonization replicates for H. rubra and H. laevigata, two (30-35 mm) juvenile and one (60-65 mm) subadult abalone were used as recipients and were placed in 20-L polypropylene buckets along with an infested abalone (Fig. 3). In the indirect colonization experiment, water from a tank with the heavily infested abalone was led into 6 jars (6 L) containing 3 recipient abalone (one ~60 mm and two ~30 mm). Three jars contained H. rubra recipients, and three contained H. laevigata. There were three blocks of this arrangement (Fig. 4). Nine 20-L buckets containing H. rubra and nine containing H. laevigata were used as controls in a similar set up to the direct colonization treatment, without infested abalone. The replicates for each treatment and control were randomly placed, and assigned to alternating water supply outlets to reduce effects due to water flow rate.

[FIGURES 3-4 OMITTED]

The experiment was carried out in constant darkness, because this is believed to induce reproduction of the polychaetes (Evans 1969) and also seems to reduce stress on the abalone (previous observations). The tanks were cleaned every 4 days and fed artificial abalone food every 2 days. If an infested source abalone died it was replaced with another one carrying a similar number of polydorids. After 72 days shells from each of the treatments were closely examined under a dissecting microscope and the number of polydorids and the locations of their burrows were recorded. The polydorids were then removed for identification.

Burrow Morphology and Growth Rate

To determine the morphology and rate of expansion of the burrows, abalone shells with live polychaete borers from the wild and from the colonization experiment were x-rayed at the end of the colonization experiment and again 29 days later. Both adult and juvenile polychaete borers were investigated. X-rays were taken using a Hewlett Packard Faxitron x-ray system. An exposure of 30 Kv, 0.2 mA for 12 sec was used. After the last x-ray was taken the polychaetes were removed from the shell to relate the burrow morphology to the species producing it. Burrow areas were determined by tracing them onto graph paper, and the percentage increase between x-rays in the overall size of the burrow was calculated.

Effects on Host Abalone

To relate the condition of abalone to the abundance of borers in their shell, 65 H. rubra from Williamstown of a size range 95-110 mm were haphazardly selected. Each abalone's length and width was measured and the percentage of the shell bored was estimated using a grading system adapted from Handley (1997, 1998) (Table 1). Repetitive tests were carried out on 20 of the shells to determine the precision of this method. Eighty percent of these tests produced the same grade and the remaining ones were within one grade of the original.

The abalone body was removed from the shell and placed on absorbent paper to remove excess water, to determine the body wet weight. Wet muscle weight was recorded after the head and viscera were removed. Dry muscle weight was obtained by placing it in a drying oven at 60[degrees]C for 48 h or until a constant weight was achieved (Davenport & Chen 1987, Roper et al. 1991. Handley 1998).

The thickness of the shell was measured using modified vernier calipers at the top of the spire. Abalone are known to thicken the shell in response to borers (Marshall & Day 2001) and the extra shell deposition presumably diverts resources from other tissues (Blake & Evans 1973, Shepherd & Breen 1992). Because the abalone were collected just after the spawning season, the effect of boring on reproductive condition could not be determined.

Three indices were used to measure the condition of the abalone:

* Wet weight of muscle divided by the wet animal weight (C[I.sub.Wet]). Healthy animals would present a higher ratio because the muscle tissue is used to store glycogen as an energy reserve (Carefoot et al. 1993). Note that the gonads of all abalone were spent.

* Dry muscle weight divided by wet muscle weight (C[I.sub.Dry]). This index determines the amount of water in the muscle. Healthier muscles have a lower water content (Carefoot et al. 1993, Handley 1998).

* The width divided by the length of the shell (C[I.sub.WL]). Faster growing abalone (and thus presumably healthier) are known to lengthen the shell more in comparison to the shell width (Oakes & Fields 1996, Worthington et al. 1995).

RESULTS

Pattern of Infestation of Abalone Shells

There was a significant correlation between the shell area and the number of polychaete borers in the shell (r = 0.698, P < 0.001), but a linear regression explained only about half of the variation in the data ([R.sup.2] = 0.478) (Fig. 5). The deviations of the data from the line suggest that shells below about 1800 [mm.sup.2] (22 mm length) are seldom infested, and that the number of borers may increase more rapidly with size in larger shells. When the residuals for the number of borers versus shell area were plotted against the grades of encrusting algal cover, there was no obvious relationship. This may be because encrusting algal cover was correlated with shell area (r = 0.746).

[FIGURE 5 OMITTED]

Table 2 shows the species of polychaete borers present on different sized abalone. Only 4 species were found in abalone <60 mm length, and Dodecaceria sp, which was present in 83% of large shells, was absent in these smaller shells. Only the spire area was infested (usually in the groove between the whorls) in smaller shells (30-50 mm), while in progressively larger abalone increasing proportions were infested around the closed ostia and the columella (Fig. 6). Only abalone >100 mm were commonly infested in the flat section of the body whorl. Many borers in the flat section were observed near spirorbid or other serpulid polychaete tubes attached to the shell surface.

[FIGURE 6 OMITTED]

Colonization of Abalone Shells by Polydorids

None of the abalone in controls and none of the smaller juveniles (30-35 mm) in other treatments became infested. The presence/absence of infesting polydorids in the subadult abalone (60-65 mm) was analyzed (Table 3). Note that the use of these data avoids the assumption that each polydorid larva colonized the abalone independently.

H. rubra was found to be significantly more susceptible to infestation by borers than H. laevigata ([chi square] = 4.96, df = 2, P < 0.05). The infested H. rubra were also each colonized by more polychaetes than infested H. laevigata, so that the total number of polychaetes present in all shells was greater in H. rubra (Fig. 7). The proportion of H. rubra and H. laevigata infested with polydorids was not significantly different in the "direct" and "indirect" treatments ([chi square] = 1.56, df = 1, P = 0.3, combined test for both hosts). This result should be regarded with caution because the numbers of shells infested are small in this experiment, but it is clear that polydorid larvae can be carried in the water to infest new hosts.

[FIGURE 7 OMITTED]

The number of borers in each section of the shell expected by chance, based on the relative area of each section, was calculated. For each abalone species the observed numbers differed significantly from those expected (H. rubra: [chi square] = 150.4, df = 3, P < 0.001, H. laevigata: [chi square] = 26.2, df = 3, P < 0.001). The pattern of infestation did not differ significantly between the two abalone species ([chi square] = 4.259, df = 4, P > 0.05) (Fig. 8). These results should be viewed with caution however, due to the low numbers for H. laevigata and the fact that this analysis assumes each spionid larva colonized independently. In summary H. rubra are more susceptible than H. laevigata and borers are more common than expected in the spire, closed ostia and below the small calcareous tubes of polychaetes attached on top of the abalone shells.

[FIGURE 8 OMITTED]

Two species of spionid polychaetes, Polydora woodwicki (Woodwick) and Dipolydora armata (Langerhans), infested the abalone in this experiment. Several larvae of polydorids were observed crawling over the surface of juvenile abalone shells until they found a suitable crevice. These larvae were then observed to begin burrowing at these sites, but subsequent observations after a short period of time often showed they were no longer present, leaving the burrow half started. Those that did stay and produce large burrows were found to be P. woodwicki. Dipolydora armata burrows were much smaller and larvae of this species were not observed.

Burrow Morphology and Growth Rate

During this experiment it was observed that the majority of polychaetes present in a shell survived the death of the abalone. Their survival depended on the shell staying upright and being placed in an area of water flow and available food. The ability of the polychaetes to survive in an empty shell for a period of time allowed X-rays to be taken. Further, they did not bore through the inner surface of the shell during the 46 days that the dead shells were held.

Because several of the worms died alter the first x-ray, presumably due to the stress of the transport involved, the expansion of only 3 burrows was observed over the 29 days between x-rays (Fig. 9). Two of the burrows were formed by Polydora woodwicki and increased their sizes by 18.9% and 27.6% respectively, the third burrow was formed by Dipolydora armata and increased its size by 15.9% over the 29 days.

[FIGURE 9 OMITTED]

The shape of the burrow can be seen clearly in several of the x-rays; and burrows from the two species were found to be very distinctive. Dipolydora armata exhibited extensive and intricate burrows, whereas P. woodwicki had a distinct U-shaped burrow. The U-shape of burrows for Boccardiella MoV 3840 (sp. nov.) are also clearly visible in Figure 10A, and over the entire abalone shell in Figure 10B. This species was found only in abalone from Mallacoota. Note that these burrows do not interconnect, and change direction just before crossing another burrow. They are distinctive and clearly different to burrows of P. woodwicki. A mud blister, in which the abalone has walled off a space inside the shell with a new shell layer, is also shown in Figure 10B, and in cross-section in Figure 11. All blisters were found to be full of sediment and Boccardiella MoV 3840. Thus, X-rays (Figs. 9, 10B) can be used to identify burrows made by P. woodwicki and Boccardiella MoV 3840 and the smaller intricate burrows formed by Dipolydora armata and also reveal mud blisters, as well as the extent to which borers have colonized a shell.

[FIGURES 10-11 OMITTED]

Effects on Host Abalone

Many heavily bored shells were brittle and were shattered during the process of removing the abalone soft tissues, so that shell parameters could not be recorded. A Pearson correlation matrix of all the indices measured showed they were not correlated with each other or the spire thickness, so that they represent independent measures of condition. Both wet muscle weight as a proportion of body wet weight and the ratio of dry to wet muscle weight decreased significantly as the extent of boring increased (F = 16.604; df = 1,58; P < 0.001 and F = 7.655; df = 1,58;P = 0.008 respectively). The width to length ratio increased significantly with increased boring (F = 4.638; df = 1,58; P = 0.035). We did not find good evidence that the thickness of the shell at the spire increased with more extensive boring (F = 1.402; df = 1, 31; P = 0.245), perhaps because spire thickness would relate specifically to boring beneath the spire. Boring changed shell shape in other ways (Fig. 12). The inner surface is greatly deformed, and the overall shape of the shell is also affected in heavily bored abalone: it is wider than the lightly bored shell and the columella shelf is enlarged.

[FIGURE 12 OMITTED]

DISCUSSION

Pattern of Infestation of Abalone Shells

The positive relationship between the size of the shell and the number of borers found in this study has also been observed in the abalone Haliotis diversicolor Reeve (Kojima & Imajima 1982), and in other molluscs (Mohammad 1972). We also found that the diversity of borers increased with host size. Both relationships would follow from the longer exposure to borers of older shells, and the fact that a larger shell area would provide a larger target for planktonic larvae to encounter and allow more borers to burrow. Adult abalone do not hide in crevices as juvenile abalone do, and thus would experience more water flow. They may also encounter more settling borers. Shell structure may also influence the degree of boring, as adult abalone shells are eroded, particularly at the spire. It is possible that the outer layer of prismatic calcite is more resistant to borers (Thomas & Day 1995), so that boring increases once it has worn away on the older spire area. Note that the closed ostia are plugged with aragonite nacre, and this is another area where borers are common.

The larger number of species in larger shells may also be due to some being secondary borers. Dodecaceria sp., which was present only in large shells, requires previous boring to be present in the shell (Gibson 1978). Such secondary borers recolonize unused burrows and extend these burrows for their own use (Smyth 1990).

Species common on smaller shells are likely to be primary colonizers. Identifying the primary borers is important, because preventing boring by these species would prevent the establishment of other borers. The colonization experiment reported here definitively identifies Dipolydora armata and Polydora woodwicki as primary colonizers, and as having planktonic larvae. Both were common on small abalone. Several species found on juvenile shells were not much more common in adult shells. These species may be suppressed by other borers, or the epibiota on larger shells.

Colonization in the Laboratory

Polydora woodwicki and Dipolydora armata were found to easily reproduce in tanks, and thus may affect aquaculture farm productivity and economic performance. Their planktonic larvae appear to settle in short periods, and could spread easily in mariculture facilities.

The laboratory experiments were designed to examine colonization while eliminating confounding influences in field observations. Our observations of the larval behavior of P. woodwicki, and the fact that Haliotis rubra were more susceptible than H. laevigata to colonization, suggests that small crevices associated with shell sculpture facilitate colonization by this polydorid. Shells of H. rubra are more sculptured than those of H. laevigata, and the spire and ostia are much more pronounced. Further, few borers were found in the flat parts of the shell, and these were often beside the tubes of spirorbids on the shell. Nothing was known about the colonization behavior of P. woodwicki prior to this study, but Zottoli & Carriker (1974) found that Polydora websteri (Hartman) preferred shell crevices on the oyster Crassostrea virginica and the mussel Mytilus edulis Lamarck. Blake (1996) suggested crevices provided the juvenile with a place to form a simple tube, to anchor itself and then initiate a burrow.

The observations of P. woodwicki larvae colonizing are the first observations of this type for this species. Borers that left burrows unfinished may have either died or left the burrow deliberately. The larvae may begin to burrow at one site on the surface of the shell and then decide that the site is unsuitable after they begin burrowing. The fact that the majority of the full sized burrows formed in juvenile shells were in the thickest sections of a shell, and that burrows did not connect, suggests borers can detect the shell thickness. Note that over a period of two and half months the worms did not bore through the inner surface of empty shells. Previous authors have suggested that polydorids do not break the inner surface of the shell because the abalone constantly produces extra layers of shell (Marshall & Day 2001). Thicker shell would actually allow the borers to increase the size of the burrows.

Size has an effect on both the number of boring worms present in the field, and on colonization, as only abalone 60 mm in length or larger became infested during this experiment. This suggests that larvae find it difficult to settle and bore into smaller shells. Kojima & Imajima (1982) found that the smallest H. diversicolor infested was 29 mm in length, but the majority of the boring occurred in abalone larger than 45 mm. Size also has a significant effect on the number of borers present in other mollusc shells (Smyth 1990). Perhaps this is to do with the smoothness of juvenile shells and the lack of crevices. Smaller shells are also very thin, making it difficult for a borer to form a burrow.

As reported previously by Lleonart & Handlinger (1998), polydorids continue to live in the shell after the host has died, as long as the shell stays in a position that allows them to continue filter feeding. These worms will hasten the degradation of the shell, and thus play a role in the longevity of dead mollusc shells. This should also be considered by ecologists who measure mortality using empty shells, or study their use by hermit crabs (Smyth 1990).

Borrow Morphology and Growth Rate

The U-shaped burrows of Boccardiella MoV 3840 have not previously been observed. This seems to be an undescribed species. The shape of the burrow for Dipolydora armata concurs with those observed in several other substrates (Blake & Kudenov 1978) but it has not previously been observed in abalone. The U-shaped burrow for Polvdora woodwicki has not previously been observed, and specimens of this species have been collected only once before.

We have shown that x-rays are useful to measure burrow expansion rates, although only a few borers could be kept alive for subsequent x-rays. Methods to improve survival during handling are needed, to facilitate further work to determine burrow expansion rates of other species.

The size and number of burrows formed in 72 days during the colonization experiment demonstrate how quickly polydorids can become established in, and damage shells. The X-rays show the extent of the damage well. This method will allow measurements of rates of infestation and will be an important tool to estimate burrow morphology and rate of expansion in different borer species and thus to determine which species cause greatest damage to the host. Extraction of borers from heavily infested shells does not pinpoint which species inflicted the damage.

Effects on Host Abalone

This study shows that boring affects the condition of abalone. Both condition indices, reflecting storage reserves in the muscle and the health of the muscle, declined significantly with increased boring damage. The increased relative width of shells with more boring, and the other shape changes, indicates that the way heavily bored abalone enlarge their shells is different to those abalone with little boring present. The change in shell shape is obvious when lightly and heavily infested shells are compared. This change may be due to the disturbance caused by the deposition of extra shell layers (Marshall & Day 2001). Heavy boring at specific locations in the shell, such as the growing edge, may also cause the abalone to change the way it grows. The marketability of abalone as a live product and their shells as ornaments and jewelry is severely reduced by high levels of boring.

The mud blisters observed in abalone from Mallacoota have been observed in other molluscs, particularly oysters (Blake & Evans 1973), and can greatly reduce the internal volume of the shell. Thus a larger shell would be required to house the same soft tissue volume of the abalone. The species that caused these blisters also forms large burrows over the entire shell. It does not match any current descriptions from Australia and further work is urgently needed to determine if this species is an introduced or exotic species.

If the correlations reflect causation, then declines in condition indices with increased boring mean that boring affects the health and growth of abalone, and thus the muscle weight recovered by the fishery will be reduced by borers. Similar correlations have been found for other abalone and molluscs in general. Haliotis diversicolor had a reduced flesh weight when 10 or more polychaetes were present boring in the shell (Kojima & Imajima 1982). Other work on mussels and oysters has shown that heavy infestations by borers were associated with lower condition indices or reduced nutrient reserves (Kent 1979, Wargo & Ford 1993). In contrast, Clavier (1989) found no correlation between level of boring in H. tuberculata Linnaeus and the health of the abalone, but his study did not include heavily bored abalone, where the effect on muscle weight was found to be strongest in this study. Caceres-Martinez et al. (1998) found no significant effect of boring on condition indices of the oyster Crassostrea gigas (Thunberg), but again, their study did not include heavily infested oysters. They noted this was essential in determining the relationship between host and borer.

One would expect deleterious effects of borers on host condition because the shell thickening response would shift resources away from other functions. Bored H. rubra were found to increase shell secretion rates 4-fold (Marshall & Day 2001). Wilbur & Saleuddin (1983) suggested that one quarter to one third of the total energy of growth is required for shell deposition in molluscs. Thus substantial energy would be required for the increased shell thickening, with a corresponding decrease in resources for somatic growth or fecundity.

The correlation of borer infestation with an increased shell width to length ratio suggests reduced growth. Slow growth in H. rubra is indicated by increased width and height relative to length (Worthington et al. 1995). Abalone divers classify stocks in some areas as "stunted," because few abalone grow past the size limit (Wells & Mulvay 1995, Troynikov et al. 1998). Stunted stocks have both high, domed shells, and high levels of boring. Slowly growing abalone may reach older ages because they are not harvested, and thus accumulate many borers. Thus slow growth may lead to heavy boring, or the deleterious effects of boring may cause the stunted growth. Perhaps both effects occur. Further investigation of juveniles in stunted areas is needed to understand the link between boring and stunted growth.

Abalone extensively infested with sabellid polychaetes were reported to be less able to right themselves when turned over (Oakes & Fields 1996), apparently due to the doming of the shell due to abnormal shell deposition at the growing edge but perhaps also because of the diversion of resources to extra shell deposition. The effects of polydorids on shell shape are less severe.

Decreased growth, decreased muscle weights, and deformation of the shell would all reduce the profit of the commercial abalone industry directly. Polydorid borers may cause such effects. Reduced growth reduces fecundity, and boring weakens the shell, which would increase mortality. This in turn would lower the levels of fishing populations can sustain. If, as we suggest, borers in abalone cause these effects, they deserve attention. Yet there has been so little research that even the risk of new introduced species affecting fishing areas cannot be assessed. This study provides methods for future work to study colonization, burrow morphology and expansion, and the effects on abalone hosts.

TABLE 1.

The definitions of the grades used to describe bored abalone shells.

Grade    Percentage of Shell Bored

  1              0% to 10%
  2             10% to 30%
  3             30% to 60%
  4             60% to 80%
  5             80% to 100%

TABLE 2.

Species of boring polychaetes present in the shells of juvenile and
adult abalone at Williamstown. Numbers are percentages of shells in
which each species was found. A blank indicates the species was not
found. Museum of Victoria numbers refer to their cataloguing
system. Descriptions of taxa are available from Robin Wilson at the
Museum of Victoria.

                             Juvenile Abalone        Adult Abalone
     Borer Species          (30-60 mm) (n = 15)    (>80 mm) (n = 15)

Boccardia chilensis                                       16.7
  (Blake and Woodwick)
B. MoV 3833                                               16.7
Dipolydora armata                  33.3                   58.3
D. MoV 3834                                                8.3
D. MoV 3835                                                8.3
D. MoV 3836                                                8.3
D. MoV 3838                         6.6                    8.3
Dodecacaria sp.                                           83.3
Polydora giardi (Mesnil)                                  16.7
P. MoV 3842                         6.6                   16.7
P. woodwicki                       33.3                   33.3
Pseudopolydora MoV                                        16.7
  3837
Total species present               4                     12

TABLE 3.

The number of shells in which borers were observed in each
treatment of each species of abalone (results from 60-65 mm
abalone only).

Treatment                  Direct     Indirect
Recipient Abalone          (n = 9)    (n = 9)

H. rubra (blacklip)           7          3
H. laevigata (greenlip)       2          3

ACKNOWLEDGMENTS

The authors thank the Museum of Victoria and the Zoology Department and Dentistry Hospital at the University of Melbourne for the facilities provided and Ocean Waves Seafoods Pty Ltd. for the abalone. The authors also thank Prof. J. Clement, Cameron Dixon, and John Ahern for assistance and discussions, and referees for the many important suggestions.

LITERATURE CITED

ABARE. 2001. Australian fisheries statistics, 2000. ABARE, Canberra.

Blake, J. A. 1996. Family spionodae Grube. In: J. A. Blake, B. Hilbig & P. H. Scott, editors. Taxonomic atlas of the benthic fauna of the Santa Maria Basin and the western Santa Barbara Channel, vol. 6. Santa Barbara: Santa Barbara Museum of Natural History, California. pp. 81-92.

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

Blake, J. A. & J. D. Kudenov. 1978. Spionidae (Polychaeta) from South Eastern Australia and adjacent areas with a revision of the genera. Mem. Nat. Mus. Vic. 39:171-280.

Blake, J. A. & K. H. Woodwick. 1975. Reproduction and larval development of Pseudopolydora paucibranchiata (Okuda) and Pseudopolydora kempi (Southern) (Polychaeta: Spionidae). Biol. Bull. 149:109-127.

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.

Carefoot, T. H., P. Qian, B. E. Taylor, T. West & J. Osborne. 1993. Effect of starvation on energy reserves and metabolism in the Northern abalone, Haliotis kamtschatkana. Aquaculture 118:313-325.

Clavier, J. 1989. Infestation of Haliotis tuberculata shells by Cliona celata and Polydora species. South Australian Department of Fisheries Research Papers. 24:16-20.

Davenport, J. & X. Chen. 1987. A comparison of the methods for the assessment of condition in the mussel (Mytilus edulis). J. Moll. Studies 53:293-297.

Day, R. L. & J. A. Blake. 1979. Reproduction and larval development of Polydora giardi Mesnil (Polychaeta: Spionidae). Biol. Bull. 156:20-30.

Evans, J. W. 1969. Borers in the shell of the sea scallop, Placopecten magellanicus. Amer. Zool. 9:775-782.

Gibson, P. H. 1978. Systematics of Dodecaceria (Annelida: Polychaeta) and its relations to the reproduction of its species. Zool. J. Linn Soc. 63:275-287.

Haigler, S. A. 1969. Boring mechanism of Polydora websteri inhabiting Crassostrea virginica. Amer. Zool. 9:821-828.

Handley, S. J. 1997. Optimising subtidal oyster production, Marlborough Sounds, New Zealand: Spionid Polychaete infestations, water depth and spat stunting. J. Shellfish Res. 16:143-150.

Handley, S. J. 1998. Power to the Oyster: Do Spionid-induced shell blisters affect condition in subtidal oysters? J. Shellfish Res 17:1093-1099.

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.

Kent, R. M. L. 1979. The influence of heavy infestations of Polydora ciliata on the flesh contents of Mytilus edulis. J. Mar. Biol. Assoc. UK 59:289-297.

Kojima, H. & M. Imajima. 1982. Burrowing polychaetes in the shells of abalone Haliotis diversicolor aquatilis chiefly on the species of Polydora. Bull. Japan. Soc. Sci. Fish. 48:31-35.

Lleonart, M. & J. Handlinger. 1998. Treatment of abalone "Mud Worms". Proceedings of the 5th Annual Abalone Aquaculture Workshop, Hobart, July 1998. Canberra Fisheries Research and development Corporation,

Marshall, D. & R. Day. 2001. Change in rate of shell deposition and shell microstructure in response to shell borers in the abalone Haliotis rubra. Mar. Freshw. Behav. Physiol. 34:189-195.

Mohammad, M-B. M. 1972. Infestation of the pearl oyster Pinctada margaritifera (Linne) by a new species of Polydora in Kuwait, Arabian Gulf. Hydrobiologia 39:463-477.

Oakes, F. R. & R. C. Fields. 1996. Infestation of Haliotis rufescens shells by sabellid polychaete. Aquaculture 140:139-143.

Roper, D. S., R. D. Pridmore, V. J. Cummings & J. E. Hewitt. 1991. Pollution related differences in the condition cycles of Pacific oysters Crassostrea gigas from Manukau Harbour, New Zealand. Mar. Env. Research. 31:197-214.

Sato-Okoshi, W. 1997. Microstructure of scallop and oyster shells infested with boring Polydora. Bull. Mar. Sci. 60:622.

Sato-Okoshi, W., Y. Sugawara & T. Nomura. 1990. Reproduction of the boring polychaete Polydora variegata inhabiting scallops in Abashiri Bay, North Japan. Mar. Biol. 104:61-66.

Shepherd, S. A. & P. A. Breen. 1992. Mortality in abalone: its estimation, variability and causes. In: S.A. Shepherd, M. J. Tegner & S. A. Guzman del Proo, editors. Abalone of the world: biology, fisheries and culture. Oxford: Fishing News Books.

Smyth, M. J. 1989. Bioerosion of gastropod shells: with emphasis on effects of coralline algal cover and shell microstructure. Coral Reefs 8:119-125.

Smyth, M. J. 1990. Incidence of boring organisms in Gastropod shells on reefs around Guam. Bull. Mar. Sci. 46:432-449.

Thomas, M. & R. W. Day. 1995. Site selection by a small drilling predator: why does the gastropod Haustrum baileyanum drill over muscle tissue of the abalone Haliotis rubra? Mar. Freshw. Res. 46:647-655.

Troynikov, V. S., R. W. Day & A. M. Leorke. 1998. Estimation of seasonal growth parameters using a stochastic gompertz model for tagging data. J. Shellfish Res. 17:833-838.

Wargo, R. N. & S. E. Ford. 1993. The effect of shell infestation by Polydora species and infection by Haplosporidium nelsoni (MSX) on the tissue condition of oysters, Crassostrea virginica. Estuaries 16:229-234.

Wells, F. E. & P. Mulvay. 1995. Good and bad fishing areas for Haliotis laevigata: a comparison of population parameters. Mar. Freshw. Res. 46:591-598.

Wilbur, K. & A. Saleuddin. 1983. Shell formation. In: K. Wilbur & A. Saleuddin, editors. The Mollusca. Pergamon Press. pp. 235-287.

Wilson, R. W. & H. D. McDiarmid. 2004. Australian spionidae (Polychaeta) Delta database. In: R. W. Wilson & P. A. Hutchings, editors. Southern Australian polychaetes: interactive identification and information retrieval. Melbourne: CSIRO.

Worthington. D. G., N. L. Andrew & G. Hamer. 1995. Covariation between growth and morphology suggests alternative size limits for the abalone, Haliotis rubra, in New South Wales, Australia. Fish. Bull. 93:551-561.

Woodwick, K.H. 1977. Lecithotrophic larval development in Boccardia proboscidea Hartman. In: D. J. Reisch & K. Fauchild, editors. Essays on polychaetous annelids in memory of Dr. Olga Hartman. Allan Hancock Foundation, University of Southern California. pp. 347-371.

Zottoli, R. & M. R. Carriker. 1974. Burrow morphology, tube formation and microarchitecture of shell dissolution by spionid polychaete Polydora websteri. Mar. Biol. 27:307-316.

H. MCDIARMID, (1) R. DAY, (1) ** AND R. WILSON (2)

(1) Zoology Department, University of Melbourne, Victoria, 3052, Australia; (2) Museum of Victoria, Carlton Gardens, Victoria, 3051, Australia

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