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Local distribution and temperature preferences of predatory whelks (Thais spp.) in Taiwan: implications for oyster culture.

ABSTRACT Among the Thais species, the broad consensus has long been that Thais clavigera (Kuster) is the most noxious predator of cultured oysters in Taiwan. Recently, two new Thais species (i.e., T. rufotincta Tan & Sigurdsson 1996 and T. keluo Tan & Liu 2001) have been identified and named in Taiwanese waters yet their impact on oyster culture is unknown. In this study, the overall impact of the three species on the oyster industry was estimated on the basis of their distribution in the field, their feeding rate and their temperature preference based on laboratory tests. The proportion of T. clavigera varied monthly from 24% to 100%, whereas the percentage of T. keluo was negatively correlated with low tide levels (P < 0.01). Thais clavigera occurred widely in the intertidal zone and T. keluo and T. rufotincta near the subtidal, this distribution pattern was consistent with their specific-preferred temperatures in the upper-limits. As shown in the laboratory, T. clavigera, T. rufotincta and T. keluo preferred 36[degrees]C, 32C[degrees]and 30[degrees]C water, respectively. In the field, the respective average feeding rate of T. clavigera, T. rufotincta and T. keluo was significantly different at 0.054, 0.010 and 0.038 oysters [snail.sup.-1] [day.sup.-1] (P < 0.05). Based on the abundance of the three Thais species at oyster cultural sites (Liu 2002) and their feeding rates, when oyster predation was made up of T. clavigera, T. rufotincta and T. keluo, predation was respectively 87%, 11% and 2%. The most destructive Thais species in the oyster industry remains T. clavigera, and it accounts for 87% to 100% of all intertidal losses in Taiwan. To the other one-third subtidal culture industry, owing to the use of off-bottom raft or longline method, the distribution of snails extended to subtidal may be limited and the reported major predator is the flatworm of Stylochus orientalis.

KEY WORDS: Thais clavigera, Thais rufotincta, Thais keluo, temperature preference, distribution, Taiwan

INTRODUCTION

Thais clavigera (Kuster) is a common predator in intertidal rocky shores of East Asia, feeding on barnacles, chitons, gastropods, bivalves and polychaetes (Taylor & Morton 1996). It is also a major predator to oyster culture, which is responsible for an annual reduction of up to 10% to 50% of the oyster industry in Taiwan (Lin & Hsu 1979). According to the records of the Taiwan Fisheries Bureau, oyster cultural areas covered 10,700 hectares, and total production was 10,400 metric tons in 2003 (Taiwan Fisheries Bureau 2004). Although oyster predators (i.e., snails of T. clavigera, Cymatium pileare [Linnaeus] and Siphonalia fusoides [Reeve], crabs of Scylla serrata [Forskal] and Matuta iunaris [Forskal], flatworm of Stylochus orientalis Bock and fish of Therapon jarbua [Forskal]) have been documented, the prominent two are T. clavigera and S. orientalis (Kuo 1964, Lin & Tang 1980). Between the two, S. orientalis is the major predator in subtidal culture, causing up to 50% of the economic loss (Lin & Tang 1980). On the contrary, T. clavigera is the predominant predator intertidally (Kuo et al. 1998).

In light of such predatory behavior, the great economic and ecological significance of the snail T. clavigera cannot be denied. However, the situation may have become more complicated because two new Thais species have recently been identified, (i.e., T. rufotincta [Tan & Sigurdsson 1996], and T. keluo [Tan & Liu 2001 ]), and these two newly named species reportedly occur in the same areas as T. clavigera. Not until the present study have we gained much insight into their effects on the oyster industry. In the present study, therefore, the potential impact of these two congeneric Thais predators on the oyster industry of Taiwan was evaluated from the perspective of their field distribution, feeding rate and their temperature preference.

MATERIALS AND METHODS

Populations of Thais species were collected on a monthly basis from September 2000 to January 2002 at oyster cultural sites (i.e., Chiku and Tungkang) and nonoyster cultural sites (i.e., Tamsui and Taichung) (Fig. 1). In a preliminary survey, it was determined that although these three snails inhabit the same areas, by and large, they typically occur in different zones (i.e., T. clavigera is common in the intertidal areas, whereas T. rufotincta and T. keluo are more prevalent in the lower zones). Thus, the decision was made to collect snails in the zones near the subtidal during the periods of low spring tide. Information concerning the tidal heights on the sampling days was obtained from the Central Weather Bureau, Taiwan (Central Weather Bureau 2000-2003). As for data analyses, the number of each Thais species (i.e., T. clavigera, T. rufotincta and T. keluo) was counted, and the percentage of each species from every collection was determined.

[FIGURE 1 OMITTED]

Feeding experiments were conducted during the November 2000 to October 2001 period. Thirty to thirty-five snails of a single species with a shell length of 20-30 mm were put into an enclosed cage (30 x 30 x 25 cm; mesh size 1.5 cm), and this was replicated 2-4 times for each species. The cages were hung in the oyster cultural area at Chiku. Cultural oysters (about 70-80 individuals [cage.sup.-1]) with a shell length of 50-60 mm were provided for the snails to feed ad libitum, and fresh oysters were replaced monthly. Additionally, cages containing oysters without snails were also supplied as control groups. The number of eaten oysters per snail, the shell lengths and the total wet weights of the snails were calculated to determine the feeding and growth rates.

For the experiments on temperature preference, snails were collected in the zones near the subtidal on the days of low spring tides in July and August 2003 and were kept moist during transportation. For comparative purposes, the collection site Shunsun (Fig. 1), which had enough specimens of the three Thais species was sampled. Upon arrival at the laboratory, the snails were kept in their shipping containers until experimental use. The total shipping and handling time prior to the experimental analyses was, at most, 6 h.

A thermo-preferendum chamber was installed horizontally with a 7.14-m long transparent plastic pipe with an inner 11-cm diameter and a 0.5-cm thick wall (Chen & Chen 1991). The pipe was closed at both ends. Two stainless-steel tubes (an outer diameter of 2.1 cm and a wall thickness of 0.05 cm) were placed in the upper one-fifth of the plastic pipe, and these served as heat exchangers. Chilled water was passed through one of the tubes in one direction, whereas heated water was passed through the other in the reverse direction, thereby forming a recirculating countercurrent heat-exchange system. An aeration tube, fitted with a stainless-steel rod to prevent flotation, was installed along the bottom of the plastic pipe to increase dissolved oxygen, improve heat exchange and prevent vertical stratification. On the upper surface of the plastic pipe, seven holes had been drilled to allow us to measure the temperatures and to release test snails into the pipe. When the system was in operation, a continuous thermal gradient was formed inside the pipe, and it ranged from 16[degrees]C at one end to 36[degrees]C at the other.

Each experiment began with the release of snails into the test pipe in the regions of the low-, mid and high-temperature openings after the thermal gradient had stabilized. The number of each species used in every experiment was in the range of 51-311 individuals. No food was provided during the trials, and none of the snails that had been used were ever reused. The pipe system and heat-exchange tubes were cleaned prior to each experiment. Because the distribution of snails did not change after the first 24-h during the observation period, over 4 days in the preliminary experiments, the results for the first 24 h were recorded.

For statistical analyses, the simple linear regression was used to determine if species appearance was dependent on tidal level. Linear regressions together with an ANCOVA were applied for the analyses of snails' feeding and growth data. The [chi square]-test of independence was used to determine whether there were differences in the 24-h distributions of the thermal preferences of the three Thais species.

RESULTS

Although all the Thais species were found at each of the collection sites, one of the three species was relatively uncommon (<1% of the total samples; data not shown) at each site. These were T. rufotincta at Tamsui and Taichung, T. keluo at Chiku and T. clavigera at Tungkang. Because of the limited number of samples, a species that was uncommon at a particular site was excluded in the analysis for that site. In Tamsui, the compositions of T. clavigera and T. keluo varied monthly from 24% to 97% and 3% to 76% of the total (Table 1 & Fig. 2). A positive correlation between the percentage of T. clavigera of the total and low tide was found (i.e., y = 0.43 + 0.936x; P < 0.01), but the percentage of T. keluo of the total was negatively correlated with the low tide on the sampling days (y = 0.568 - 0.932x; P < 0.01). In simple terms, the higher the tide level, the less abundant were T. keluo. This pattern was similarly observed in the August to September, 2003 collections from Taichung. However, the correlation was not significant for T. rufotincta and T. clavigera from Chiku or for T. keluo and T. rufotincta from Tungkang (Fig. 2).

[FIGURE 2 OMITTED]

Turning to the feeding experiments, oysters that remained alive during each experimental period were in the ranges of 11% to 90% in T. clavigera, 67% to 98% in T. rufotincta and 24% to 88% in T. keluo, respectively. No dead oysters were found in the control groups. The average feeding rate of T. clavigera, T. rufotincta and T. keluo was respectively 0.054, 0.010 and 0.038 oysters [snail.sup.-1] [day.sup.-1] (Fig. 3). The slowest feeder was T. rufotincta (P < 0.05), and monthly variations in the feeding rates of all three species were also apparent (P < 0.05) (Table 2). The overall growth of T. clavigera, T. rufotincta and T. keluo was found to have varied respectively from an average of 22.5, 25.2 and 25.3 mm to an average of 40.9, 26.6 and 37.0 mm in length (Fig. 4).

[FIGURE 3-4 OMITTED]

Positive correlations between shell length and cultural interval (month) in all Thais species were found (i.e., y = 1.78x + 24.52; P < 0.001) for T. clavigera; y = 0.13x + 24.75 (P < 0.001) for T. rufotincta; and y = 1.29x + 25.83 (P < 0.001) for T. keluo. The slopes significantly differed among species, with a descending order of T. clavigera>T, keluo>T, rufotincta (P < 0.05). Additionally, average monthly growth rate differed significantly among species, with values of 0.89, 0.07 and 0.64 mm [month.sup.-1] for T. clavigera, T. rufotincta and T. keluo, respectively (P < 0.01).

With respect to the temperature preference of the three Thais species, they were significantly different at all of the collection sites (P < 0.01, [chi square]-test) except at Chiku, the data for which are not shown because T. clavigera was the only available species, making comparisons with other species impossible (Fig. 5). Comparatively speaking, the Thais species in areas of low- (16[degrees]C to 20[degrees]C) to mid-temperatures (24[degrees]C to 28[degrees]C) were inactive during the 24-h experimental period, but what was particularly evident was the distinct tendency for T. keluo and T. rufotincta to escape areas with high temperatures. Just as in the collection from Shunsun, the snails in this experiment aggregated in different locations of the high-temperature area, with T. clavigera, T. rufotincta and T. keluo respectively showing a preference for 36[degrees], 32[degrees] and 30[degrees]C (Fig. 5C).

[FIGURE 5 OMITTED]

In summary, the average feeding rates of the snails ranged from 0.010-0.054 oysters [snail.sup.-1] [day.sup.-1], or in descending order, T. clavigera > T. keluo > T. rufotincta. Moreover, their respective preferred temperature differed significantly, with T. keluo and T. rufotincta exhibiting a clear preference for lower temperatures than T. clavigera. Such differences in relation to their distribution were, in essence, also indicative of the correlation between the low tide levels of their habitats and the percentage of species that appeared. However, this pattern was not always observed in samples from all the collection sites.

DISCUSSION

It has been documented that the distribution of intertidal gastropods reflects the thermal resistance and preferred temperatures of individual species (Newell 1979). Whenever a species had been investigated, the same spatial pattern with respect to other species is found (Underwood 1973). In this study, further evidence in support of spatial zonation was also observed in that T. clavigera widely occurred in the intertidal zone, whereas T. keluo and T. rufotincta appeared lower down. Such distribution pattern was consistent with their preferred temperatures in the upper-limits because T. keluo and T. rufotincta exhibited lower preferred temperatures than did T. clavigera (i.e., 30[degrees], 32[degrees] and 36[degrees]C), respectively. However, in our results, the correlation between tidal level and species appearance was only found for snails from Tamsui and Taichung but not for those from Chiku or Tungkang (Fig. 2). According to the Central Weather Bureau of Taiwan, the annual average tidal range at the sites of Tamsui, Taichung, Chiku and Tungkang was respectively 220, 390, 120 and 60 cm (Central Weather Bureau 2000-2003). On the level of thermal and desiccation stress, snails that normally inhabit a small tidal range may be less stressful because of their increased exposure to moisture from wave splash, which allows the lower-down species to distribute upwardly (Newell 1979). Possibly, the marked discrepancy of our results reflects the influence of tidal range on the spatial zonation of these snails.

Depending on the salinity and temperature of the water as well as the size of the oysters or snails, it has been reported earlier that the feeding rates of T. clavigera measured in the laboratories ranged from 0.018-0.103 oysters [snail.sup.-1] [day.sup.-1] (Lin & Hsu 1979). As for the southern oyster drill, Stramonita haemastoma (Linnaeus) (Kool 1987) fed on the American oyster Crassostrea virginica (Gmelin) ranges from 0.01-0.09 oysters [snail.sup.-1] [day.sup.-1] (Brown 1997). Our field feeding data were 0.010-0.054 oysters [snail.sup.-1] [day.sup.-1], in other words, falling well within the range reported in previous study. And, there was a 5-fold difference between the lowest and highest feeding rates of the three species, with T. clavigera having the highest followed by T. keluo (0.038 oysters [snail.sup.-1] [day.sup.-1]) and T. rufotincta (0.010 oysters [snail.sup.-1] [day.sup.-1]).

Seasonal variations in the abundance of the three Thais species have previously been observed at some major cultural sites investigated: Shunsun, Taishi, Budai and Chiku (Fig. 1) (Liu 2002). Densities of T. clavigera, T. rufotincta and T. keluo were in the ranges of 0-272, 1-317 and 0-34 individuals [m.sup.-2], respectively. Among these sites, T. clavigera varied in the range of 96% to 100%, 62% to 99%, 64% to 89% and 61% to 99%, respectively. For T. rufotincta, it was 0% to 3%, 1% to 38%, 11% to 36% and 1% to 39%, respectively, and for T. keluo, it was 0% to 1%, 0%, 0% and 0% to 2%, respectively. Obviously, T. clavigera is the most important species simply on the grounds that they always made up more than 60% of the total.

Based on the percent appearance of the three Thais species at the intertidal cultural sites and their feeding rates, in the extreme cases of the percent appearance of 61% for T. clavigera, 37% for T. rufotincta and 2% for T. keluo, the impact of oyster predation by T. clavigera, T. rufotincta and T. keluo was 87%, 11% and 2%, respectively. Of course, when T. clavigera was the only species, it was responsible for all of the losses. Considering the feeding rate and abundance of the three species, there is no doubt that the most destructive species to the intertidal oyster industry remains T. clavigera. However, intertidal culture is only two-thirds of the whole industry in Taiwan (Kuo et al. 1998).

To the subtidal one-third, T. rufotincta and T. keluo are the two new potential predators. Formerly, all oysters were cultivated on sandy tidal flats in the western coast of Taiwan and rocks, bamboo or plastic sticks were used to attract oyster spats to settle. Later on, in 1960s, oysters are grown off-bottom by the rack, raft, or longline method and subtidal culture is getting popular (Kuo et al. 1998). Although data on predation by snails in subtidal culture is not available, oyster farmers usually mentioned that the flatworm S. orientalis is a serious problem, causing more than 50% of their economic loss (Lin & Tang 1980). Owing to the use of off-bottom raft or longline method, the distribution of snails extends to subtidal may be limited. Consequently, the impact of snail predation on subtidal oyster industry may reduce greatly. However, further field survey on the distribution of these snails in the subtidal is necessary to verify this hypothesis.

ACKNOWLEDGMENTS

The authors thank the reviewers for their highly constructive comments that have substantially improved the overall quality of this manuscript. This study was supported by the National Science Council, Republic of China (NSC 91-2313-B-110-005).

LITERATURE CITED

Brown, K. M. 1997. Size-specific aspects of the foraging ecology of the southern oyster drill Stramonita haemastoma (Kool 1987). J. Exp. Mar. Biol. Ecol. 214:249-262.

Chen, Y. L. L. & H. Y. Chen. 1991. Temperature selections of Anguilla japonica (L.) elvers, and their implications for migration. Aust. J. Freshw. Res. 42:743-750.

Kuo, H. 1964. Investigation on Taiwan edible shellfish. Special Report of Joint Commission on Rural Reconstruction 38:1-99. (JCRR)

Kuo, J. C., H. I. Chen & Y. D. Ho. 1998. The production economic analysis of oyster culture in Taiwan. J. Taiwan Fish. Res. 6:55-70. (in Chinese)

Lin, Y. S. & C. J. Hsu. 1979. Feeding, reproduction and distribution of oyster drill, Purpura clavigera (Kuster). Bull. Inst. Zool. Academia Sinica, Taiwan 18:21-27.

Lin, Y. S. & H. C. Tang. 1980. Biological studies on cultured oyster in Penghu. Bull. Inst. Zool., Academia Sinica. Taiwan 19:15-22.

Liu, Y. C. 2002. The study of population biology of Thais spp. Thesis of the Institute of Marine Biology, National Sun Yat-sen University, Kaohsiung, Taiwan. (in Chinese)

Newell, R. C. 1979. Biology of intertidal animals. Faversham, Kent, UK: Marine Ecological Surveys Ltd. 781 pp.

Tan, K. S. & J. B. Sigurdsson. 1996. Two new species of Thais (Mollusca: Neogastropoda: Muricidae) from peninsular Malaysia and Singapore, with notes on T. tissoti (Petit, 1952) and T. blanfordi (Melvill, 1893) from Bombay, India. Raffles Bull. Zool. 44:77-107.

Tan, K. S. & L. L. Liu. 2001. Description of a new species of Thais (Mollusca: Neogastropoda: Muricidae) from Taiwan, based on morphological and allozyme analysis. Zool. Sci. 18:1275-1289.

Taylor, J. D. & B. Morton. 1996. The diets of predatory gastropods in the Cape d'Aguilar Marine Reserve, Hong Kong. Asian Mar. Biol. 13:141-166.

Underwood, A. J. 1973. Studies on zonation of intertidal prosobranch molluscs in the Plymouth region. J. Anim. Ecol. 42:353-372.

JING-YING WU, (1) YU-CHIH LIU, (1) PEI-JIE MENG, (2) YUH-WEN CHIU (3) AND LI-LIAN LIU (1)*

* Corresponding author. E-mail: lilian@mail.nsysu.edu.tw

(1) Institute of Marine Biology, National Sun Yat-sen University, Kaohsiung 804, Taiwan; (2) National Museum of Marine Biology and Aquarium, Biology Department, 2 Houwan Road, Checheng, Pentung, Pingtung 944, Taiwan; (3) Faculty of Biomedical Science and Environmental Biology, Kaohsiung Medical University, Kaohsiung 807, Taiwan
TABLE 1.
Thais species sampled at the four sites on the basis of monthly
intervals.

 Location

 Tamsui Taichung

Date/Species T. clavigera T. keluo T. clavigera T. keluo

Sept. 2000
Oct.
Nov.
Dec. 120 (55%) 99 (45)
Jan. 2001
Feb. 131 (95%) 7 (5%)
Mar. 134 (89%) 17 (11%)
Apr.
May 62 (50%) 62 (50%)
June 66 (24%) 211 (76%)
July
Aug. 182 (97%) 6 (3%)
Sept.
Oct. 95 (89%) 10 (11%)
Nov.
Dec.
Jan. 2002 76 (93%) 6 (7%)
Aug. 2003 (1) 300 (59%) 210 (41%)
Aug. (2) 1188 (100%) 0 (0%)
Sept. 2003 592 (57%) 450 (43%)

 Location

 Chiku Tungkang

Date/Species T. clavigera T. rufotincta T. rufotincta T. keluo

Sept. 2000 330 (85%) 60 (15%)
Oct. 176 (61%) 112 (39%) 355 (98%) 6 (2%)
Nov. 124 (75%) 41 (25%) 814 (100%) 0 (0%)
Dec. 490 (87%) 73 (13%) 402 (92%) 37 (8%)
Jan. 2001 74 (97%) 2 (3%) 417 (95%) 20 (5%)
Feb. 272 (89%) 35 (11%)
Mar. 79 (88%) 11 (12%) 232 (88%) 32 (12%)
Apr. 258 (91%) 26 (9%)
May 158 (91%) 15 (9%) 155 (93%) 11 (7%)
June 133 (62%) 81 (38%)
July 657 (89%) 84 (11%) 152 (65%) 83 (35%)
Aug. 383 (98%) 7 (2%)
Sept.
Oct. 231 (92%) 20 (8%) 305 (80%) 75 (20%)
Nov.
Dec. 478 (99%) 6 (1%)
Jan. 2002 226 (100%) 1 (0%)
Aug. 2003 (1)
Aug. (2)
Sept. 2003

TABLE 2.
Tests of the GLM and least square means of the feeding rates of the
Thais species. The species with different letters indicate significant
differences in the feeding rates (P < 0.05).

 Sum of Mean
Source DF Squares Square F Value Pr > F

Model 29 0.042 0.001 5.25 <0.001
Error 46 0.012 0.000
Corrected total 75 0.053

 Type Mean
Source DF 3 SS Square F Value Pr > F

Species 2 0.020 0.010 37.83 <0.001
Month 9 0.006 0.000 2.46 0.022
Species x month 18 0.007 0.000 1.39 0.183

Species T. clavigera T. keluo T. rufotincta

Feeding rate
 (oysters [snail.sup.-1] 0.054 A 0.038 B 0.010 C
 [day.sup.-1])
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Author:Liu, Li-Lian
Publication:Journal of Shellfish Research
Geographic Code:9TAIW
Date:Aug 1, 2006
Words:3661
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