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Parapenaeon consolidatum (isopoda: bopyridae) and the relative growth and reproduction of Metapenaeopsis dalei (decapoda: penaeidae) in South Korea.

ABSTRACT This study describes the prevalence of a parasitic bopyrid isopod, Parapenaeon consolidatum, on Metapenaeopsis dalei and its effect on host growth and reproduction. The prevalence of P. consolidatum increased with shrimp size, from 27.3% at 5 mm CL to 68.4% at 16 mm CL. Lengths of female bopyrids and that of their hosts were positively correlated. This indicated that the bopyrid stays continuously with its host and is not detached when the host molts. Morphometric analyses indicated that parasitized male and female shrimp have slightly lower body weight and length than nonparasitized shrimp of the same carapace length. The gonadosomatic index was higher for nonparasitized than for parasitized female shrimp. Growth of the petasma, the copulatory organ of male shrimp, was significantly affected by the parasite.

KEY WORDS: Metapenaeopsis dalei, Purapenaeon cosolidatum, growth, reproduction

INTRODUCTION

The kishi velvet shrimp, Metapenaeopsis dalei (Rathbun), is distributed throughout the coastal waters of Korea, Japan, and China in sandy muddy substrates at 30-130 m depth (Kim 1977, Hayashi 1992). With seasonal warming of the waters starting in April, the shrimp begin to migrate from deeper water to the coastal area. They are exploited commercially in Korea from April to October, using shrimp trawl and stow nets (Cha 1997). Metapenaeopsis dalei exhibit higher burrowing rates than other penaeid shrimp (Sakaji 1995). Owens (1987) reported that the bopyrid isopod Parapenaeon consolidatum Richardson is a parasite on M. dalei from Japanese waters. However, little is known about the effects of this parasite on growth and reproduction of its host.

Bopyrids live on shrimp, brachyurans, and anomurans and cause a conspicuous bulge of the branchiostegite (Dall et al. 1990). Owens and Glazebrook (1985) showed that bopyrids on penaeids grow with their hosts and have a similar longevity, although there is some loss of parasites as the prawns approach asymptotic length. Some studies hypothesized a relationship between a bopyrid and its host because of a highly positive correlation between the sizes of female bopyrids and their shrimp hosts (see Beck 1980: Schuldt & Rodrigues Capitulo 1985). Cash and Bauer (1993) reported that Probopyrus pandalicola (Packard) remain on and grow synchronously with Palaemonetes pugio Holthuis; video recording has shown that reproductive activities of the parasites are synchronized with host molting.

Both growth and reproduction of shrimps can be affected by bopyrids. Abu-Hakima (1984) showed that parasitized male Penaeus semisulcatus De Haan grew to the same size as nonparasitized females but that host reproduction was totally inhibited. She also showed that a petasma, the male copulatory organ, was not formed in parasitized male shrimp. Chu & Leong (1996) indicated that parasitized male and female shrimp have slightly lower average body weights than nonparasitized shrimps of the same carapace length. Dawson (1958) reported that in the Arabian Gulf, only P. semisulcatus larger than 100 mm TL (total length) were parasitized with bopyrids. Mathews et al. (1988) found low parasite prevalence among P. semisulcatus of 14-18 mm CL (carapace length) by Epipenaeon elegans Chopra; prevalence increased up to a prawn size of around 28 mm CL, after which the rate fell, apparently because of loss of the parasite. Some bopyrid parasites alter the appearance or behavior of the host whereas others are asymptomatic.

This study provides additional information on the prevalence of P. consolidatum in relation to host size, the effects of bopyrid parasitism on the growth and reproduction of parasitized shrimp, and the relationship between the host shrimp and bopyrid breeding rate.

MATERIALS AND METHODS

Shrimps were collected monthly from September 1998 to June 2000 with a research shrimp beam trawl (mesh size: 9.3 x 9.3 mm) in waters around Yongchodo, South Korea (128[degrees]40'E, 34[degrees]30'N). The study area was sandy mud in the channel between Hansando and Yongchodo at 20-30 m depth. During this study, water temperature varied from 6.7 to 25.8[degrees]C (Fig. 1). Samples were fixed immediately in neutralized formaldehyde for 1-2 days and were then preserved in 70% alcohol.

[FIGURE 1 OMITTED]

Specimens were sorted and sexed. Parasitized shrimps were detected by an obvious deformation of their carapace. Bopyrids were removed, and the females were classified as ovigerous or nonovigerous. In the shrimp, carapace length (CL, from posterior orbital margin to the posterior edge of carapace in the mid-dorsal line) and body length (BL, from the tip of the rostrum to the end of the telson) of shrimp were measured with a caliper to the nearest 0.1 mm. Shrimp body weight (BW) was determined to the nearest 0.01 g after the shrimp was blotted dry. In males, the petasma length (PL, from the tip of the lobe to the end of the petasma) was measured to the nearest 0.01 mm under a dissection microscope. In parasites, body lengths (from the anterior margin of the head to the posterior margin of the pleotelson) of female (FPL) and male (MPL) bopyrids were measured under a dissection microscope to the nearest 0.01 mm.

The effects of the parasites on host log transformed BW, BL. and PL (reproduction) were determined statistically by analysis with CL as covariance (ANCOVA) using Minitab version 2.0 (Sokal & Rohlf 1995). Analyses were based on individuals with no visibly developed gonads (CL <12.09 ram: Choi 2001), as gonad development alters the length-weight relationship of both female and male shrimp (Chu & Leong 1996).

RESULTS

Prevalence

A total of 2550 specimens of M. dalei were caught (Fig. 1). Females were consistently more abundant in all size classes; the overall proportion of tamales was 53.1% but varied with shrimp size. The proportion of females sharply increased from 50-100% for size classes >16 mm CL (Fig. 2). Forty-eight percent of both the 1360 female shrimp and the 1190 male shrimp were parasitized by P. consolidatum. The smallest parasitized female and male shrimp were 4.21 mm and 4.72 mm CL, respectively. The largest parasitized female and male shrimps were 21.25 mm and 18.44 mm CL, respectively. Female prevalence increased from 28.6% at 5 mm CL to 62.3% at 10 mm CL, leveled off between 11 and 12 mm CL, and sharply increased from 37.5% at 12 mm CL to 90% at 16 mm CL. Male prevalence increased from 25% at 5 mm CL to 59.5% at 9 mm CL, decreased between 10 and 11 mm CL, and increased from 43.4% at 11 mm CL to 100% at 15 mm CL. Parasitism incidence for females and males >16 mm CL and >15 min CL, respectively, dropped sharply (Fig. 3). Overall, parasitism occurred early in the life of the host and until shrimp reached 11 mm CL, prevalence was the same in both sexes. However, between 12 mm and 15 mm CL, prevalence among males was higher than among females.

[FIGURES 2-3 OMITTED]

Host-parasite Relationship

Female P. consolidatum filled most of and were tightly lodged within the host's branchial chamber, producing a characteristic bulge in the host's branchiostegite. Male parasites oriented perpendicularly to the female's body axis on the ventral side of the female's abdomen. Regression analysis showed a significant relationship between FPL and CL (Fig. 4). The relationship was similar for female and male hosts (ANCOVA intercept: F = 3.08, df = 1,254, P = 0.081). The relationship between FPL and MPL was also significant (Fig. 5).

[FIGURES 4-5 OMITTED]

Host Growth Rate Effects

CL-BL regression slopes for parasitized and nonparasitized shrimp were significantly different for female shrimp (ANCOVA: male, F = 3.72, df = 1,39, P = 0.06; female, F = 11.31, df = 1,71, P < 0.05) (Fig. 6). Also, parasitized and nonparasitized shrimp had significantly different CL BW regression slopes (ANCOVA: male, F = 5.13, df = 1.114, P < 0.05; female, F = 10.24, df = 1,153, P < 0.05) (Fig. 7).

[FIGURES 6-7 OMITTED]

Host Reproduction Effects

There were no changes in the structure of the thelycum in parasitized female shrimps. In nonparasitized males, the petasma consisted of the typical complex of membranous folds and ridges in the endopodites of the first pairs of pleopods. In parasitized males, endopodites were only partially fused or more frequently were separate structures. The PL-CL regressions for nonparasitized and parasitized male shrimp had similar slopes (ANCOVA: F = 2.56. df = 1.204, P > 0.05) but different intercepts (ANCOVA: F = 125.31, df = 1,205, P < 0.05) (Fig. 8). Thus, the PL of parasitized male shrimp was smaller than that of nonparasitized male shrimp.

[FIGURE 8 OMITTED]

To investigate the influence of the bopyrid parasite on gonad development, the gonadosomatic index (GSI) of female shrimp caught during the breeding season (July-August, Choi 2001) were compared with CL. GSI values of nonparasitized female shrimps were significantly larger than those of parasitized shrimps (Kruskal-Wallis Test: H = 8.10, P < 0.01) (Fig. 9).

[FIGURE 9 OMITTED]

Parasite Maturity

Size frequency distribution of female parasites is shown in Figure 10.

[FIGURE 10 OMITTED]

DISCUSSION

In this study, the 48% parasitism rate of M. dalei by the bopyrid P. consolidatum was much higher than the 0.24% reported for Penaeus longistylus Kubo parasitized by Parapenaeon japonicum (Thielemann) and Parapenaeon prox. expansus on Queensland's east coast (Courtney 1991). Prevalence fluctuated during the sampling year, as observed for other bopyrid-host pairs (Beck 1980, Somers & Kirkwood 1991). Seasonal fluctuations have been ascribed to differential migration patterns among parasitized and nonparasitized shrimp or to seasonal variations in the reproduction and mortality rates of hosts and parasites (Mathews et al. 1988: Tones Jorda & Roccatagliata 2002).

Roccatagliata & Lovrich (1999) reported that the prevalence of the parasite Pseudione tuberculata Richardson decreased with Paralomis granulosa (Jacquinot) size and suggested a high mortality rate for small parasitized P. granulosa. In contrast, we observed increasing parasitism in proportion with size for the smaller host size classes (3-9 mm CL), suggesting that M. dalei did not cause increasing mortality in the small size classes. We suggest the decrease in prevalence between size classes 9 mm and 12 mm CL was due to a relatively higher host growth rate of these individuals during the study period. Choi (2001) reported that at these size classes, shrimp frequently molted during the summer. Somers & Kirkwood (1991) showed that P. semisulcatus parasitized by Epipenaeon ingens Nobili may lose their bopyrids: of 22 parasitized prawns that were released, six had lost their bopyrids upon recapture two weeks later. Cash & Bauer (1993) gave further direct evidence of parasite loss in P. pugio parasitized by P. pandalicola. They noted that bopyrids were shed with the shrimp exuviae in three of the 112 moltings examined. Additional indirect evidence of parasite loss is from the size of maturity of female parasites, which begin spawning at 4-5 mm FPL (host size of ca. 9 mm CL). Cash & Bauer (1993) reported that P. pandalicola larvae escaped from the host, P. pugio, during the latter's molting period. They showed that epicaridium larvae were released from the host's branchial chamber several hours before the host molted. A decreasing parasitism with larger size classes of shrimp can also perhaps be explained by a shorter life span of parasitized shrimp versus that of nonparasitized shrimp.

The positive correlation of FPL of P. consolidatum with the CL of M. dalei (Fig. 4) suggests that the parasite attaches to small hosts and grows along with them. This should negatively affect host growth (Chu & Leong 1996). However, we found that with <8 mm CL size classes of parasitized shrimp, BL and WT averaged relatively larger on nonparasitized shrimp of the same CL. However, by the time they reached 8 mm CL, the ratios of BL and WT to CL were relatively similar for both groups of shrimp. This finding may be explained by two hypotheses. First, parasitized shrimp may initially consume more than nonparasitized shrimp and hence grow faster; the parasite may thus be influencing the behavior of the shrimp. Anderson (1977) reported that P. pugio parasitized by P. pandalicola are more Artemia salina Linnaeus nauplii than nonparasitized shrimp. Second, P. consolidutum may preferentially select larger CL hosts at the time of infection, because a larger host might provide more space for bopyrid development and reproduction. The strategy of the parasite may thus be to select a host with the optimal growth and size. Either approach might be adaptive, because parasite size and fecundity are related to host size (see Baudoin 1975; Sheader 1977).

BL and WT of parasitized shrimp are smaller than with nonparasitized shrimps for >8 mm CL size classes. The increased breeding rate of female parasites on shrimp >8 mm CL may be indicative of a negative effect on shrimp by the parasite. Bopyrid isopods have evolved as branchial parasites on decapod crustacean hosts (cf., Markham 1975) and affect their host in a variety of ways through their high rate of ingestion of the host's hemolymph (Walker 1977). Nelson et al. (1986) showed that the energy expenditure of breeding bopyrid Argeia pauperata Stimpson females is more than that of its normal host, Crangon franciscorum Stimpson.

Parapenaeon consolidatum affects the genital growth of M. dalei; the length of a parasitized shrimp's petasma is less than that on a nonparasitized shrimp. The length of the petasma normally increases directly with increasing CL (Burkenroad 1934). Some studies suggested that the petasma assists in the transfer of spermatophores to the female (Hudinaga 1942; King 1948). We suggest that in parasitized males, a smaller petasma length negatively affects sperm transfer and hence copulation success. In addition, our observation indicated that a few parasitized larger males had unfused or only a partly joined petasma. Dall (1958) defined male maturity of Metapenaeus mastersii (Haswell) (= Metapenaeus bennettae Racek & Dall) by the presence of a fully developed petasma. Tuma (1967) reported that small Penaeus merguiensis De Man males had a longitudinally constricted petasma on their pleonic endopodites; when mature, the end of endopodites had joined to form the petasma. Thus, P. consolidatum affects the growth of the petasma in M. dalei, which likely negatively affects male shrimp reproductive ability.

CONCLUSION

Our main conclusions are that M. dalei has an exceptionally high rate of parasitism by P. consolidatum. Parasitism proportion increased with host shrimp size. Selection of a larger host may provide more branchial chamber space for the parasite, or M. dulei may grow faster because of parasite induced hunger, because other studies have shown that parasitized shrimp eat more food than do nonparasitized shrimp. Because the parasite negatively effects growth of the host's genital organ and development of gonads, it may be reducing population fecundity because a large portion of the male population consequently cannot effectively reproduce.

ACKNOWLEDGMENTS

The authors thank Dr. Martin Torres Jorda (Universidad de Buenos Aires, Argentina) and Dr. Daniel Roccatagliata (Universidad de Buenos Aires, Argentina) for critical reading and comments on the manuscript.

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JUNG HWA CHOI, (1) GLEN JAMIESON, (1) KYEONG HO HAN (2) AND SUNG YUN HUNG (3)

(1) Fisheries and Oceans Canada Pacific Biological Station, Nanaimo, BC V9T 6N7, Canada; (2) Department of Aquaculture Yosu National University, Yeosu-shi 550-749, Korea; and (3) Department of Marine Biology, Pukyong National University, Busan 608-737, Korea

* Correspondence present address and E-mail: Korea Inter-University Institute Ocean Sciences. Pukyong National University, Busan 608-737, Korea; shrimpchoi@hanmail.net
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Author:Hung, Sung Yun
Publication:Journal of Shellfish Research
Date:Apr 1, 2004
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