See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/275622498 Infestation of the False King Crab Paralomis granulosa (Decapoda: Lithodidae) by Pseudione tuberculata (Isopoda... Article in Journal of Crustacean Biology · November 1999 DOI: 10.2307/1549296 CITATIONS READS 27 25 2 authors: Daniel C. Roccatagliata Gustavo A Lovrich 41 PUBLICATIONS 165 CITATIONS 130 PUBLICATIONS 1,647 CITATIONS National Scientific and Technical Research C… SEE PROFILE National Scientific and Technical Research C… SEE PROFILE All content following this page was uploaded by Gustavo A Lovrich on 28 May 2015. The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the original document and are linked to publications on ResearchGate, letting you access and read them immediately. JOURNAL OF CRUSTACEAN BIOLOGY, 19(4): 720-729, 1999 INFESTATION OF THE FALSE KING CRAB PARALOMIS GRANULOSA (DECAPODA: LITHODIDAE) BY PSEUDIONE TUBERCULATA (ISOPODA: BOPYRIDAE) IN THE BEAGLE CHANNEL, ARGENTINA Daniel Roccatagliata and Gustavo A. Lovrich ABSTRACT A total of 16,692 specimens of Paralomis granulosa was collected in the Beagle Channel, Tierra del Fuego, Argentina. between July 1996 and July 1997. This lithodid was parasitized by a bopyrid isopod identified as Pseudione tuberculata. Infested crabs exhibited a conspicuous bulge on their carapaces, which accommodated the parasite housed in the branchial chamber. The prevalence of infestation by P. tuberculata decreased with crab size, from 45.6% at 1O-19.9-mm to 0% at 90-99.9mm carapace length. Bopyrids were found on 251 occasions in the left branchial chamber and only once in the right branchial chamber. Except for two immature female parasites found in the branchial chamber of a small crab, all parasites were mature females, each usually carrying a dwarf male attached to its abdomen. The length of the female isopodsand that of their hosts were positively correlated. These two observations suggest that the parasites infest P. granulosa early in the life of the host, and remain on, and grow up with the host throughout its life. The finding of crabs without bopyrids, but with distended branchial chambers, shows that some crabs survive the infestation. While breeding is inhibited in parasitized hosts, the prevalence of the parasite is already low (about 1.2%) at the size of host maturity. Therefore, we suggest that the reproductive potential of the crab population is not seriously affected by the sterilizing effect of the parasite. Finally, the cooccurrence of this bopyrid and a second parasite, the rhizocephalan Briarosaccus callosus, was recorded. but the prevalence of double infestations was low. In the Beagle Channel, southern South America, two sympatric lithodid species occur in coastal waters: the southern king crab Lithodes santolla (Molina, 1782) and the false southern king crab Paralomis granulosa (Jacquinot, 1847) (see Lovrich and Vinuesa, 1996). Although these two species have sustained a modest commercial fishery since the 1960s, little is known about their parasites. These two lithodids are infested by two other crustaceans: the rhizocephalan barnacle Briarosaccus callosus (Boschma, 1930) and an epicaridean isopod, herein identified as Pseudione tuberculata Richardson, 1904. Briarosaccus callosus has been found on many lithodid species. Boschma (1962) recorded this parasite in P. granulosa and L. santolla from South Georgia Island, Falkland (Malvinas) Islands and the Magellan Strait. This parasite was also reported from the Magellan area by Stuardo and Solis (1963), Campodonico et al. (1983), and Vinuesa (1989). More recently, it was extensively studied by Hoggarth (1990) on the basis of material from the Falkland (Malvinas) Islands. Our knowledge on the bopyrid isopod is more fragmentary. Vinuesa (1989) reported an unidentified bopyrid isopod infesting P. granulosa and L. santolla from the Beagle Channel. Lovrich (1991) examined additional specimens of P. granulosa bearing bopyrids in the same area. The parasite of P. granulosa was herein identified as Pseudione tuberculata, a species described by Richardson (1904) on the basis of 13 specimens parasitic on Lithodes diomedae collected off Port Ortway, Chile, at a depth of 1,050 fathoms (1,920 m). As far as we know, this is the first time this species has been recorded after its original description. Of the approximately 50 species of Pseudione described, five occur in southern South American waters. Three are known only from Chile: P. brattstroemi Stuardo et aI., 1986, P. chiloensis Roman-Contreras and Wehrtmann, 1997, and P. humboldtensis Pardo et aI., 1998. Pseudione galacanthae Hansen, 1897, originally recorded from the west coast of North America, was found off Chilean and Argentinian Patagonia and off the Falkland (Malvinas) Islands. The fifth species, P. tuberculata Richardson, 1904, known from Chile, is herein recorded from southern Argentina (see Richardson, 1904; Rayner, 1935; Stuardo et aI., 1986; Roman-Contreras and Wehrtmann, 1997; Pardo et al., 1998). 720 ROCCATAGLIATA AND LOVRICH: BOPYRID ISOPOD FROM PARALOMlS IN ARGENTINA This study provides information on the prevalence of P. tuberculata in relation to host size, the loss of the parasite from the host, the effects of parasitism on the reproduction of infested female crabs, the relationship between the sizes of the female bopyrid and the host crab, and the cooccurrence of this parasite with the rhizocephalan Briarosaccus callosus. MATERIALS AND METHODS A total of 16,692 specimens of Paralomis granulosa was collected in the Beagle Channel (-54 °54'S, 67°12'W), Tierra del Fuego, Argentina, between July 1996 and July 1997. Crabs >50 mm carapace length (CL) were captured with commercial conical traps between 10-50 m depth in July, September, October, and December 1996, and in January, March, May, and July 1997. During each survey, samples ranging from 924-3,067 crabs were inspected on board the ship for parasites. The sex of each crab and the presence of eggs attached to the pleopods of females were recorded. The carapace length of all crabs sampled was measured and those specimens with a distension of the branchial region were inspected for bopyrid parasites (Figs. I, 2). The examination procedure involved stretching the lateral swelling of the carapace from the body, in order to determine whether the parasite was present. Most of the infested crabs were taken alive to the laboratory where they were fixed in 5% sea-water Formalin and dissected for bopyrids. Furthermore, all crabs showing rhizocephalan externae or scars (indicative of lost externae) were also taken to the laboratory and fixed in 5% seawater Formalin. Most crabs between 30-50 mm CL were caught with tangle nets of 40-mm mesh at 10-16 m depth in December 1996. Only crabs exhibiting characteristic bulging carapaces were dissected. Since crabs between 30-45 mm CL were scarce in our samples, we took I additional crab of this size range in May and 5 more in December 1997 by tangle nets and SCUBA diving, respectively. These 6 specimens were only used in the calculations of the relationship between host and parasite sizes. Crabs <30 mm CL were collected by SCUBA diving at 8-10 m depth near the Bridges Islands (54°51.0'S, 68°14.5'W) in August 1996 and February 1997. They were found inside crevices and under rocks or hydrozoan colonies (see Lovrich and Vinuesa, 1995). All crabs collected were measured and dissected. To investigate whether crabs >50-mm CL could harbor bopyrid parasites without developing a lateral swelling, 679 additional crabs (female and male), captured with commercial conical traps in June, August, and September 1996, were measured and dissected. The carapace length of each crab sampled was measured with a dial caliper to the nearest 0.1 mm according to Lovrich and Vinuesa (1993). Each crab was classified in one of the following infestation categories. (I) Infested by a bopyrid: crabs carrying I (rarely 2) adult female bopyrid (usually with a dwarf male clinging to her pleopods) in one of their branchial chambers; (2) Previously infested by a bopyrid: crabs with an empty but distended branchial chamber, indicative of a past bopyrid infestation; (3) Infested by a rhizocephalan: crabs with an externa under the abdomen; (4) Rhizocephalan-scarred: 721 crabs showing a dark rounded wound on the ventral abdominal surface, indicative of lost rhizocephalan externa; and (5) Healthy: uninfested crabs with neither parasites nor evidence of past infestations. The branchial chamber occupied by the bopyrid parasite was noted (i.e., right or left). All female bopyrids were removed from the host and measured under a dissecting microscope with an eyepiece micrometer to the nearest 0.01 mm. Total length (TL) was measured from the middle of the anterior margin of the cephalon to the anterior margin of the pleotelson. Female parasites were classified as either immature (with rudimentary oostegites, not meeting medially) or mature (with well-developed oostegites, slightly or completely overlapping each other). Since two linear functions may better explain the relationship between total parasite length and host size, we used the MATURE2 routine to find the intersection point of both lines (Somerton and MacIntosh, 1983). Other statistical analyses followed standard methods as described by Sokal and Rohlf (1995). Females of P. granulosa with eggs, or remains of hatched eggs, were considered reproductive. Females with eggs were present throughout the year and postovigerous females occurred from July-November (Lovrich and Vinuesa, 1993; Lovrich, personal observation). Therefore, the parasitic effect on host reproduction was analyzed on the basis of crabs collected throughout the year. RESULTS Distortion of the Carapace of the Host Crabs that were infested (or had lost their parasites recently) exhibited a gross bulge on the side that contained (or had contained) the parasite (Fig. 1). However, if a fraction of infested crabs did not show a noticeable bulge on .their carapaces, the prevalence of adult parasites might be underestimated. To test this hypothesis, 1,010 crabs. (331 crabs <30 mm CL + 679 crabs >50 mm CL) were dissected, and 138 mature female parasites were found, each usually carrying a dwarf male attached to its abdomen. The carapaces of all these infested crabs were clearly distorted on the side occupied by the parasite. Therefore, we are confident that we missed few, if any, par.asitized crabs when, on board the ship, we examined only those crabs which exhibited a bulge. Parasite Prevalence The prevalence of the parasite (number parasitized/total number of crabs) decreased with crab size in both sexes (Fig. 3, Table 1). Since we observed only three crabs <10 mm CL, this size class has been excluded from the analysis. The prevalence sharply declined from 45.6% at 10-19.9 mm CL to 15% at 30-39.9 mm CL, and stabilized at 8.7% and 6.9% for size classes 40-49.9 and 50-59.9 722 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 19, NO. 4. 1999 Fig. I. Paralomis granulosa (45.2 mm CL) showing lateral swelling on the carapace (left side) caused by infestation by a mature female Pseudione' ,ubercula,a. Fig. 2. Internal view of the carapace of a Paralomis granulosa (67 .0 mm CL) showing a female Pseudione luberculala on the left side. 723 ROCCATAGLIATA AND LOVRICH: BOPYRID ISOPOD FROM PARALOMIS IN ARGENTINA 70 3 60 Cl) N • Formerly parasitized D Parasitized 149 "C 50 E In I! ca 40 Q. Cl) ...cｾ＠ 30 179 Cl) ...CJ Cl) a. 20 40 277 708 10 4468 0 0 ｾ＠ v 1526 118 0> 0> 0> 0> 0> 0> 0> cri 0> 0> cri cri C') cri cri cri cri cri cri co 0 r-. ｾ＠ 0 ｾ＠ C\I Lt) J; 0C') 0Lt) "" ;g co 0co r-. 0> 00> 0 0 ｾ＠ fI Host carapace length (mm) Fig. 3. Size-specific prevalence (%) of Pseudione tuberculata on Paralomis granulosa collected from July 1996 to July 1997 in the Beagle Channel. Numbers at the top of the bars indicate the number of crabs examined for each size class. Table 1. Frequency of Paralomis granulosa infested and previously infested by the bopyrid Pseudione tuberculata, healthy crabs, and total number of crabs examined, sorted out by size class and sex of the host. For each size class, the probability (P) of the hypothesis of independence of infestation from sex was tested (parasitized crabs were contrasted with healthy crabs). Size class <10 mm CL 10-19.9 mm CL 20-29.9 mm CL 30-39.9 mm CL 40-49.9 mm CL 50-59.9 mm CL 60-69.9 mm CL 70-79.9 mm CL 80-89.9 mm CL 90-99.9 mm CL >100 mm CL Males Females Males Females Males Females Males Females Males Females Males Females Males Females Males Females Males Females Males Females Males Females Parasitized Previously parasitized Healthy Total number of crabs examined 1 I 36 32 24 22 3 3 13 II 19 30 24 14 18 0 I 0 0 0 0 0 0 0 5 2 0 3 0 0 7 5 16 25 34 60 99 22 47 I 6 0 0 0 0 I 41 33 60 59 13 18 115 109 195 404 913 2,083 4,128 1,784 4,181 234 1,508 12 118 0 1 2 82 67 90 89 16 24 144 133 232 476 984 2,169 4,252 1,813 4,230 238 1,514 12 118 0 Fisher's exact test P 0.1282 0.1350 0.3204 0.1643 0.0825 <0.001 0.0358 724 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 19, NO. 4. 1999 30 _ 25 E E -£ C) 20 I: .S! <11 15 ::: U) ca "ca C. <11 +" 10 iii E <11 LL " Males 5 + Females 0 0 10 20 30 40 50 60 70 80 90 Host size (mm) Fig. 4. Relationship between the carapace length of Paralomis granulosa and the total length (TL) of the mature female of Pseudione tuberculata. Lines were fitted after the calculation of the intersection point (= 30.3 mm CL) by MATURE2 routine (Somerton and MacIntosh, 1983). For crabs <30.3 mm CL, the regression equation was TL = -0.55 + 0.47 CL; for crabs 230.3 mm CL the regression equations were TL = 1.15 + 0.37 CL for females and TL = 7.0 + 0.25 CL for males. Double bopyrid infestations and simultaneous bopyrid and rhizocephalan (with externae or scars) infestations were excluded. mm CL, respectively. For crabs >60 mm CL, the prevalence dropped gradually from 1.2%-0%. Female crabs attain smaller maximum sizes than male crabs and consequently may lose their parasites at smaller sizes than male crabs. The prevalence for the size classes <60 mm CL was independent of the sex of the host, whereas the prevalence for the size classes 60-69.9 mm CL and 70-79.9 mm CL was significantly higher in male crabs than in female crabs (Table O. For the size class 80-89.9 mm CL, inadequate sample size prevented a rejection of the null hypothesis (i.e., that parasitism is independent of the sex of the host). In summary, infestation occurred early in the life of the host (CL < 10 mm) (see below) and, until the crabs reached 60 mm CL, there was no difference in the prevalence between female and male crabs. However, at size classes 60-69.9 and 70-79.9 mm CL, the prevalence decreased more abruptly in female than in male crabs, with parasitized females absent from the larger size classes (the largest parasitized female crab recorded was 67.1 mm CL). In contrast, parasitized males were still present in size classes 70-79.9 mm CL and 80-89.9 mm CL (the largest parasitized male recorded was 82.0 mm CL). Previously infested crabs occurred in all size classes except in those with 40-49.9 mm CL (Fig. 4, Table 1). Although for small crabs the prevalence did not show a clear pattern, it steadily decreased with size, for both sexes, in crabs >50 mm CL. Variation of the Size of the Parasite with the Size of the Host The length of the mature female bopyrid increased with the length of the host (Fig. 4; r = 0.93, P < 0.01). However, at 30.3 mm CL of the host there is a significant change in the slope of the regressions (MATURE2; F = 25.7; P < 0.01). Furthermore, for crabs :2:30.3 mm CL, the slope of the regression line for females was significantly greater than that for males (ANOVA F SLOPES = 8.74, P = 0.004). These regression lines were: length of 725 ROCCATAGLIATA AND LOVRICH: BOPYRID ISOPOD FROM PARALOMIS IN ARGENTINA Table 2. Frequency of Paralomis granulosa infested by the bopyrid Pseudione tuberculata, in relation to its ovigerous status. Females were selected in size between the smallest ovigerous female, 53.0 mm CL, and the largest parasitized female, 67.1 mm CL. Females parasitized by rhizocephalans (with externae or scars) were excluded. Ovigerous Nonovigerous Parasitized Healthy 2 31 998 467 the bopyrid (TL) = 1.15 + 0.37 CL (N = 57, r = 0.669) and TL = 7.0 + 0.25 CL (N = 77, r = 0.627), for female and male crabs, respectively. In contrast, for crabs <30.3 mm CL, the regression lines for female and male crabs were not significantly different (ANOVA F SLOPES = 0.623, P = 0.43; ANCOVA F ORDINATES = 0.071, P = 0.79). Therefore, the size relationship between the parasite and its host may be described by the common regression line: TL = -0.55 + 0.47 CL (N = 111, r = 0.89). Preponderance of Sinistral Infestation Bopyrid infestation was recorded in 251 crabs in the left branchial chamber and only once in the right branchial chamber. Three of the 251 crabs (12.5, 14.8, and 25.1 mm CL) showed double sinistral infestation, i.e., two female parasites in their left chambers. In two of these crabs, both parasites were mature females, whereas in the other crab both parasites were immature females. No other immature female parasites were found. In addition, no cases of bilateral double infestation (one female parasite in each branchial chamber) were noted. Among previously parasitized crabs, 330 had the left and two the right branchial chamber distended. Effects on Reproduction of the Host To investigate the influence of the bopyrid parasite on host reproduction, we selected those female crabs between 53.0 mm CL (the smallest ovigerous female) and 67.1 mm CL (the largest parasitized female). The frequency observed of infested, ovigerous crabs was significantly lower than expected, i.e., bopyrids inhibited egg production (Table 2, Fisher's exact test, P « 0.001). To determine whether the inhibitory effect on reproduction is still present in crabs that had lost their parasites, we selected those pre- Table 3. Frequency of Paralomis granulosa previously infested by the bopyrid Pseudione tuberculata, in relation to its ovigerous status. Females ranged in size between the smallest ovigerous female, 53.0 mm CL, and the largest female bearing distended branchial chamber and without parasite, 84.0 mm CL. Females parasitized by rhizocephalans (with externae or scars) were excluded. Ovigerous Nonovigerous Deparasitized Healthy 47 48 3,400 690 viously parasitized crabs between 53 mm CL (the smallest ovigerous female) and 84 mm CL (the largest previously parasitized female). Among previously parasitized crabs the frequency of ovigerous females was also lower than expected, but it was much higher than in the case of parasitized crabs (49.5% versus 6.1 %) (Table 3, Fisher's exact test, P « 0.001). Simultaneous Bopyrid and Rhizocephan Infestation The frequency of P. granulosa simultaneously parasitized by the bopyrid Pseudione tuberculata and the rhizocephalan Briarosaccus callosus was highest (about 4.6%) in crabs 20-29.9 mm CL. For this size class of the host, the prevalence of the bopyrid was 25.7% and that of the rhizocephalan was 10.0%; thus, both parasites were fairly common. In addition, for this size class, the frequency of the double infestation was marginally significant (Fisher's exact test, P = 0.043). For all the remaining size classes, the number of crabs infested simultaneously by both parasites were those expected in a noncontagious distribution (Table 4). DISCUSSION The southern king crab Paralomis granulosa is parasitized by a bopyrid identified as Pseudione tuberculata. In this study, the prevalence of P. tuberculata gradually decreased from 45.6% in crabs 10-19.9 mm CL to 0% in crabs 90-99.9 mm CL. Based on a sample of P. granulosa from the commercial fishery (CL >50 mm), Vinuesa (1989) reported a very low prevalence of this parasite (0.5%). Although our results confirm this low prevalence for P. granulosa >50 mm CL (0.68% on average), smaller crabs showed significantly higher prevalences. 726 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 19, NO. 4, 1999 Table 4. Frequency of Paralomis granulosa parasitized by the bopyrid Pseudione tuberculata and/or the rhizocephalan Briarosaccus callosus in relation to size class of the host. Crabs with signs of previous bopyrid infestation or rhizocephalan scars were excluded. Size class <10 mm CL 10-19.9 mm CL 20-29.9 mm CL 30-39.9 mm CL 40-49.9 mm CL 50-59.9 mm CL 60-69.9 mm CL 70-79.9 mm CL 80-89.9 mm CL 90-99.9 mm CL >100 mm CL Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Rhizocephala Bopyrida Bopyrida (+) H (-) 0 2 2 66 8 38 (+) I (-) 5 0 24 0 49 0 38 0 18 0 (+) (-) (+) (-) (+) (+) (-) (+) (-) (+) (-) (+) (-) (+) (-) I (+) 0 0 0 0 (-) (+) (-) In P. granulosa, the maximum size of uninfested crabs was larger than the maximum size of parasitized crabs. Differences in maximum sizes were also reported for other bopyrid-host associations (see Pike, 1961; Bourdon, 1968; Truesdale and Mermilliod, 1977). Several factors could account for these differences in sizes, namely, parasite loss from large hosts, selective mortality of parasitized hosts, retardation of the growth of parasitized hosts, and behavioral factors leading to a decrease in the catchability of large infested hosts (O'Brien and Van Wyk, 1985). We suggest that P. granulosa may lose their infestations of P. tuberculata. Previously infested hosts showing distended carapaces have also been identified in other bopyridhost associations (see Pike, 1953; Bourdon, 1968; Van Wyk, 1982). Somers and Kirkwood (1991) conclusively showed that Penaeus semisulcatus de Haan infested by Epipenaeon ingens Nobili, 1906, may lose their bopyrids; of 22 infested prawns that were released, six had lost their bopyrids upon recapture two weeks later. Cash and Bauer (1993) gave further direct evidence of parasite loss in Palaemonetes pugio Holthuis infested by Probopyrus pandalicola (Packard, 1879). They noted that the bopyrid was shed Fisher's exact test P 0 I 0 74 10 119 3 31 15 224 14 599 12 2,996 6 5,912 0.2275 0.0429 0.3929 0.2283 0.3370 0.8599 0.9819 I 4,415 0 1,520 0 118 0.9998 with the shrimp exuviae in 3 ofthe 112 moltings examined. A strong selective mortality appears to occur among small infested P. granulosa. The drop in prevalence from size classes 10-19.9 to 30-39.9 mm CL may be an indication of a high mortality induced by the parasite among small crabs. The percentage observed of previously parasitized crabs is insufficient to explain this decline in prevalence. In contrast, stable prevalences between size classes 40-49.9 and 50-59.9 mm CL suggest no selective mortality in these crabs. The gradual decline in prevalence of previously infested crabs >60 mm CL may be an indication of full recovery from the parasite. Early infestation and concurrent growth are suggested by the high positive correlation between the sizes of the bopyrid parasites and those of the crab hosts. Additional indirect evidence of early infestation is that all female parasites examined were mature, except two immature females found in an abnormal double infestation. Further studies should focus on crabs <10 mm CL, since infestations occur at an early stage in the life cycle of the crab. Although the sizes of mature female bopyrids and their hosts were positively correlated, a change was detected in the linearity at 30.3 ROCCATAGLIATA AND LOVRICH: BOPYRID ISOPOD FROM PARALOMIS IN ARGENTINA mm host CL (Fig. 4). The slope for small crabs was significantly higher than that for large crabs. We contend that this pattern may be due to the fact that once the crab reaches about 30 mm CL, the growth of the parasite begins to lag behind that of its host. In consequence, the slope of the regression line decreases. Furthermore, above approximately 30 mm CL, size relationships between the parasite and its host seem to vary with the sex of the host, so that the slope for females is higher than that for males. Female crabs reach a lower final size than male crabs, suggesting that they have a slower growth rate than males (Lovrich, 1991, 1997). Most probably this fact, rather than a faster growth rate of the bopyrids infesting female crabs, accounts for the higher slopes observed for the female regression line. Paralomis granulosa grows from 12-57 mm CL in about eight years (Lovrich and Vinuesa, 1995). Therefore, assuming that P. tuberculata infests the crab at CL <10 mm, and that subsequently host and parasite grow together, we can expect that, in infested crabs >57 mm CL, the parasite is somewhat more than eight years old. This is the maximum life-span of the parasite, since most of the parasites die before reaching this age. A longevity of about eight years is the longest reported for a bopyrid, a fact that may be connected with the low temperatures at which this parasite lives. Most branchial bopyrids occur nearly equally in the right and left gill chambers of their hosts. There are, however, species that occur predominantly or exclusively in only one chamber. All those known belong to the primitive subfamily Pseudioninae, and most are parasites of hermit crabs (Markham, 1986). Pseudione tuberculata overwhelmingly occupies left branchial chambers in 99.6% of the P. granulosa examined. The bopyrid larva arriving first at the definitive host develops into a female, while the second larva attaches to that female and becomes a male (Reinhard, 1949). Perhaps the strong preference of some bopyrids for the right or left branchial chamber evolved to increase the probability for the second parasite to find the female parasite and/or to avoid double infestations. The detrimental effects of bopyrid parasites on the reproductive capacities of their hosts are well known (Reinhard, 1956). While breeding is inhibited in parasitized P. granu- 727 losa, at the size female crabs attain their gonadal maturity (60.6 mm CL; see Lovrich and Vinuesa, 1993), the prevalence of the parasite is low (about 1.2%). We suggest that the sterilizing effect of the parasite does not seriously affect the reproductive potential of the popUlation of P. granulosa. Suppression of ovarian development by bopyrid castrators is not permanent. The effect of the parasite lasts only as long as the parasite is alive and, after the detachment of the latter, regeneration or maturation of the ovary occurs (Hiraiwa and Sato, 1939; Beck, 1980) and broods can subsequently be produced (Pike, 1960). The ovarian condition of P. granulosa was not examined. However, the fact that almost half of the previously infested females >53.0 mm CL were ovigerous suggests that they partially recover from the inhibitory effects on reproduction exerted by P. tuberculata. The frequency of P. granulosa simultaneously parasitized by the bopyrid P. tuberculata and the rhizocephalan B. callosus was slightly higher than expected for the size class 20-29.9 mm CL. We suspect that, after infestation by one of the parasites, these crabs may be somewhat more vulnerable than healthy crabs to infestation by the other parasite. However, no deviation from the expected frequencies was observed for the remaining size classes. Other studies have indicated combined bopyrid-rhizocephalan frequencies significantly higher than those attributed to chance alone (see Perez, 1934; Codreanu, 1941; Altes, 1962). To confirm whether in P. granulosa combined infestations are more frequent than expected at random, additional crabs should be examined, in particular those from size classes in which both parasites are well represented (20-29.9 and 30-39.9 mm CL). ACKNOWLEDGEMENTS We are grateful to the statl of Pesquera del Beagle S.A. for their invaluable support on board the ship and in the processing factory; to the Direcci6n General de Recursos Naturales of the Tierra del Fuego Province for the December 1996 samples; and to Dr. John Markham and Lic. Martin Torres Jorda for their valuable comments on the manuscript. This study was partially supported by the Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET, Argentina), the Universidad de Buenos Aires (Grant number EX-OSS), the Fundaci6n Antorchas, Argentina (Reentry Grant, and Grant for cooperation among Argentinean researchers), and the International Foundation for Science, Sweden (Grant number A2S071l). 728 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 19, NO. 4. 1999 LITERATURE CITED Altes, J. 1962. Sur quelques parasites et hyperparasites de Clibanarius erythropus (Latreille) en Corse.-Bulletin de la Societe Zoologique de France 87: 88-97. Beck, J. T. 1980. The effects of an isopod castrator, Probopyrus pandalicola, on the sex characters of one of its caridean shrimp hosts, Palaemonetes paludosus.-Biological Bulletin 158: 1-15. Boschma, H. 1962. Rhizocephala.-Discovery Reports 33: 55-92. Bourdon, R. 1968. Les Bopyridae des mers Europeennes.-Memoires du Museum National d'Histoire Naturelle A50: 77-424. Campodonico, I., M. B. Hernandez, and E. Riveros. 1983. Investigacion, manejo y control de las pesquerfas de centolla y centollon de la XII Region. Informe consolidado: recurso centollon.-Informe del Instituto de la Patagonia, Punta Arenas (Chile) 25: 1-97. Cash, C. E., and R. T. Bauer. 1993. Adaptations of the branchial ectoparasite Probopyrus pandalicola (lsopoda: Bopyridae) for survival and reproduction related to ecdysis of the host, Palaemonetes pugio (Caridea: Palaemonidae).-Journal of Crustacean Biology 13: 111-124. Codreanu, R. 1941. Sur les Pagures du littoral roumain de la Mer Noire et leurs Crustaces parasites.-Analele Academiei Romane-Memoriile Sectiunii Siintifice (3) 16:1095-1133. • •• Hiraiwa, Y. K., and M. Sato. 1939. On the effect of parasitic Isopoda on a prawn, Penaeopsis akayebi Rathbun, with a consideration of the effect of parasitization on the higher Crustacea in general.-Journal of Science of the Hiroshima University B(I) (Zoology) 7: 105-124. Hoggarth, D. D. 1990. The effects of parasitism by the rhizocephalan, Briarosaccus callosus Boschma on the lithodid crab, Paralomis granulosa (Jacquinot) in the Falkland Islands.-Crustaceana 59: 156-170. Lovrich, G. A. 1991. Reproduccion y crecimiento del centollon, Paralomis granulosa (Crustacea, Anomura, Lithodidae) en el Canal Beagle.-Ph.D. dissertation, Universidad de Buenos Aires, Buenos Aires, Argentina. pp. 1-160. - - - . 1997. La pesquerfa mixta de las centollas Lithodes santolla y Paralomis granulosa (Anomura: Lithodidae) en Tierra del Fuego, Argentina.-Investigaciones Marinas, Valparafso 25: 41-57. - - - , and J. H. Vinuesa. 1993. Reproductive biology of the false southern king crab (Paralomis granulosa, Lithodidae) in the Beagle Channel, Argentina.-Fishery Bulletin, United States 91: 664-675. - - - , and - - - . 1995. Growth of immature false southern king crab, Paralomis granulosa (Anomura, Lithodidae), in the Beagle Channel, Argentina.-Scientia Marina 59: 87-94. - - - , and - - - . 1996. Reproductive strategies of two lithodids in the Beagle Channel, Argentina: a complementary management tool in a changing fishery.In: B. Baxter, ed., High latitude crabs: biology, management, and economics. Alaska Sea Grant College Program No. 96-02. pp. 333-340. University of Alaska Fairbanks, Fairbanks, Alaska. Markham, J. C. 1986. Evolution and zoogeography of the Isopoda Bopyridae, parasites of Crustacea Decapoda.-In: R. H. Gore and K. L. Heck, eds., Crustacean biogeography. Crustacean Issues 4: 143-164. A. A. Balkema Publishers, Rotterdam, The Netherlands. O'Brien, J., and P. Van Wyk. 1985. Effects of crustacean parasitic castrators (epicaridean isopods and rhizocephalan barnacles) on growth of crustacean hosts.In: A. M. Wenner, ed., Factors in adult growth. Crustacean Issues 3: 191-218. A. A. Balkema Publishers, Rotterdam, The Netherlands. Pardo, L. M., C. Guisado, and E. Acuiia. 1998. Pseudione humboldtensis, a new species (Isopoda: Bopyridae) of parasite of Cervimunida johni and Pleuroncodes monodon (Anomura: Galatheidae) from the northern coast of Chile.-Proceedings of the Biological Society of Washington Ill: 272-277. Perez, c. 1934. Notes sur les Epicarides et les Rhizocephales des cotes de France. VII. Infection simultanee des Pagures par un Athelges et un Rhizocephale.-Archives de Zoologie Experimentale et Generale 75: 541-565. Pike, R. B. 1953. The bopyrid parasites of the Anomura from British and Irish waters.-Journal of the Linnaean Society of London (Zoology) 42: 219-237. - - - . 1960. The biology and post-larval development of the bopyrid parasites Pseudione affinis G. O. Sars and Hemiarthrus abdomina lis (Kroyer) [= Phryxus abdominalis KroyerJ.-Journal of the Linnaean Society of London (Zoology) 44: 239-251. - - - . 1961. Observations on Epicaridea obtained from hermit-crabs in British waters, with notes on the longevity of the host-species.-Annals and Magazine of Natural History 13: 225-240. Rayner, G. W. 1935. The Falkland species of the crustacean genus Munida.-Discovery Reports 10: 211-245. Reinhard, E. G. 1949. Experiments on the determination and differentiation of sex in the bopyrid Stegophryxus hyptius Thompson.-Biological Bulletin 96: 17-31. - - - . 1956. Parasitic castration of Crustacea.-Parasitology 5: 79-107. Richardson, H. 1904. Contributions to the natural history of the Isopoda.-Proceedings of the United States National Museum 27 (1350): 1-89. Roman-Contreras, R., and I. Wehrtmann. 1997. A new species of bopyrid isopod, Pseudione chiloensis, a parasite of Nauticaris magallanica (A. Milne-Edwards, 1891) (Crustacea: Decapoda: Hippolytidae).-Proceedings of the Biological Society of Washington 110: 242-248. Sokal, R. R., and F. J. Rohlf. 1995. Biometry. The principles and practice of statistics in biological research, third edition.-W.H. Freeman & Co., San Francisco, California. Pp. 1-887. Somers, I. F., and G. P. Kirkwood. 1991. Population ecology of the grooved tiger prawn, Penaeus semisulcatus, in the north-western Gulf of Carpentaria, Australia: growth, movement, age structure and infestation by the bopyrid parasite Epipenaeon ingens.-Australian Journal of Marine and Freshwater Research 42: 349-367. Somerton, D. A., and R. A. MacIntosh. 1983. The size at sexual maturity of blue king crab, Paralithodes platypus in Alaska.-Fishery Bulletin, United States 81: 621-628. Stuardo, J., and I. Solis. 1963. Biometrfa y observaciones generales sobre la biologfa de Lithodes antarcticus Jaquinot.-Gayana (Zoologfa) 11: 1-49. - - - , R. Vega, and I. Cespedes. 1986. New bopyrid isopod parasitic on Callianassa uncinata H. Milne Edwards: with functional and ecological remarks.Gayana (Zoologfa) 50: 3-15. Truesdale, F. M., and W. J. Mermilliod. 1977. Some observations on the host-parasite relationship of Macro- ROCCATAGLIATA AND LOVRICH: BOPYRID ISOPOD FROM PARALOM1S IN ARGENTINA brachium ohione (Smith) (Decapoda, Palaemonidae) and Probopyrus bithynis Richardson (lsopoda, Bopyridae).---Crustaceana 32: 216-220. Van Wyk, P. M. 1982. Inhibition of the growth and reproduction of the porcellanid crab Pachycheles rudis by the bopyrid isopod, Aporobopyrus muguensis.-Parasitology 85: 459-473. Vinuesa, J. H. 1989. Efectos e incidencia del parasitismo en la centolla (Lithodes santolla) y cento1l6n (Paralomis granulosa) del Canal Beagle.-Physis 47: 45-51. View publication stats 729 RECEIVED: 27 August 1998. ACCEPTED: 25 January 1999. Addresses: (DR) Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, (1428) Buenos Aires, Argentina. (e-mail: rocca@bg.fcen.uba.ar); (GAL) Centro Austral de Investigaciones Cientificas (CADIC-CONICET), CC92, (9410) Ushuaia, Tierra del Fuego, Argentina. (e-mail: centolla @tierradelfuego.org.ar)