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First studies on morphometric relationships and size at maturity of the red crab Platyxanthus patagonicus (Milne-Edwards) and variations caused by Rhizocephalan infestation, in the San Matias Gulf, Patagonia, Argentina.

ABSTRACT The size at onset sexual maturity in brachyurans can be evaluated considering different criteria, including growth allometry, gonad development stages, and presence of sperm in spermathecas or eggs in the abdomen. Morphometric aspects of males and the presence of eggs in females of P. patagonicus from the northern San Matias Gulf were respectively analyzed to determine its size at onset of the sexual maturity. Crab samples were obtained during a fishing experiment with traps (cubical, pyramidal, and conical, of similar internal volume), performed in the gulf during winter 2005. Also, the parasitism by a sacculinid rhizocephalan was analyzed to discuss possible effects on the reproductive success. All crabs caught were sorted by sex, carapace width (CW) and total weight (TW). Size frequency distributions were compared among sexes. Proportion of females bearing eggs were grouped into 16 size intervals of 5 mm to determine the size of first reproductive maturity based on a criterion of [L.sub.50%]. In males, the allometric change of chela length was analyzed for this purpose. Only individuals exceeding 50 mm were caught. Of 807 crabs caught, 36% (289) were males and 64% (518) were females. The size frequency distributions differed significantly between sexes with males larger than females (K-S test). Relationships of total weight (TW) to carapace width (CW) were calculated for all reproductive types and compared by ANCOVA with the following results: parasitized crabs < females < females with eggs = males. The mean size at first maturity of females was estimated to be 87.66 mm. Size at maturity for male crabs could not be determined from morphometric data because there was no significant difference in the relationship of chela length and CW for juvenile and adult males. All parasitized crabs (73) were females, whose mean width and mean weight were significantly lower than those from nonparasitized individuals. Prevalence was 9% and the mean intensity was one parasite per host. The parasitized crabs resembled juveniles. The size at first maturity and the reproductive capacity of P. patagonicus could be affected by presence of the parasite, even producing significant interference at the population level. Parasitism by sacculinid must be monitored after the starting of an emerging fishery to assess the actual contribution of the reproductive stock.

KEY WORDS: crabs, sexual maturity, Platyxanthus patagonicus, sacculinid infestation, San Matias Gulf

INTRODUCTION

Variability in market conditions for the main shellfish resources of the San Matias Gulf (mussels, scallops, and octopus), coupled with uncertainties in availability of any given species over time, led local businessmen and fisheries administrative officials to initiate the search for alternate, nontraditional fishery resources. Interest thus arose in the possibility of fishing for crab species from the San Matias Gulf, which until the present had not been exploited.

When species are of potential economic interest, knowledge on their reproduction is essential for developing management strategies. Although Platyxanthus patagonicus (Milne-Edwards) represents an economical potential resource in the San Matias Gulf, there is virtually no information about its reproductive biology. The reproductive capacity of a certain crustacean species can be assessed by the study of sexual maturity (Hines 1982). The size at onset sexual maturity in brachyurans can be evaluated considering different criteria, including growth allometry, gonad development stages, presence of spermatic bags or sperm in spermathecas, vestige eggs on the ovigerous areas or the presence of eggs in the abdomen as was analyzed by several authors (Brown & Powell 1972, Campbell & Eagles 1983, Lopez Greco et al. 1997, Lopez Greco & Rodriguez 1998, Pinheiro & Fransozo 1998, Muino et al. 1999, Castiglioni & Santos 2000, Flores et al. 2002).

Platyxanthus patagonicus is distributed in South America from Uruguay to Chubut (Argentina) between 20 and 45 m depth (Boschi et al. 1992). An experimental trap fishery plan was performed in July 2005 to provide information on efficiencies of different trap designs (cubical, pyramidal, and conical) and determine the relative spatial distribution and abundance of crabs in the northern area of the San Matias Gulf (Narvarte et al. in prep). Virtually no biological information is available for management of a potential fishery on P. patagonicus in the San Matias Gulf. Onset of maturity and the proportion mature over the size range can be used to develop fundamental management models such as commercial size.

A rhizocephalan (Sacculinidae) parasite was found on the crab abdomen during the fishing experiment. Several studies have shown that these parasites influence growth and reproduction in most crab species (Raibaut & Trilles 1993, Hoeg 1995, Takahashi & Lutzen 1998, Murphy & Goggin 2000).

The aim of this study was to describe morphometric aspects of males and the presence of eggs in females of P. patagonicus from the northern San Matias Gulf, which were respectively analyzed to determine its size at onset of sexual maturity. Also, the parasitism by a saceulinid rhizocephalan was analyzed to discuss its influence on the reproductive success of this species of potential fishery importance.

MATERIALS AND METHODS

Study Site and Sampling Design

All crabs were collected by commercial fishermen using a typical artisanal shellfish boat 9 m length, at 50 m depth. Crabs were captured in traps from the northern zone of San Matias Gulf (between 40[degrees]52'75"S 40[degrees]57'25"S and 64[degrees]25'00"W--64[degrees]37'00"W) (Fig. 1), when lowest temperatures (~8[degrees]C; Gonzalez, pers. comm.) occur in northern Patagonia. The sampling area was found to contain significant densities of crabs by the use of experimental trawling (Morsan, 2000). Three trap types were used (cubical, tubular-conical, and tubular-pyramidal) with 40 mm mesh aperture. Additionally, to avoid the escapement of small size individuals escape rings were not used. Nine traps, three of each type, were intercalated and separated at regular intervals of 20 m along a 10 mm diameter polyethylene main line. A total of 27 lines were set, each with 9 baited traps, in 10 fishing trips between 22 July and 5 August 2005. The lines were established perpendicular to the predominant currents in the area (Narvarte et al. in press.), and were collected 24 or 48 h after setting. The experiment was done in a short period to avoid find different biological processes during the execution.

A single "biological sample" was established by pooling all the crabs from the sampling period. All the individuals were sorted by sex, carapace width (CW; mm) and total wet weight (TW; g). To determine if both chelae were symmetric, length of the propodium was measured with a Venier caliper (precision: 0.01 mm) (LCh; mm) on a subsample of 35 individuals per sex. Crabs with missing or partially regenerated appendages were

not weighed. Externae of the parasite was removed and weighed.

Size frequency distributions were constructed based on the CW measurements and compared among sexes using a Kolmogorov-Smirnov test. The overall sex ratio of the crabs caught was calculated and bias from the 1:1 ratio was analyzed using Chi-square test.

[FIGURE 1 OMITTED]

The morphometric relationships between CW and TW were determined for each sex and condition (females, females bearing eggs, parasitized crabs) after log transformation of the data, and compared using linear regressions. The null hypothesis of no difference in TW between sexes and condition was analyzed with ANCOVA (Zar 1999) with CW as covariate.

For the study of the size at maturity in females we have considered the criteria corresponding to the functional maturity (i.e., the presence of eggs attached to the pleopods). Calculation was made of the percentage of females carrying egg masses, and proportion of females carrying eggs grouped into size intervals of 5 mm to determine the size at first maturity based on a criterion of 50% gravid females per size interval (Somerton 1981, Roa et al. 1999). Parasitized females were excluded. The following logistic formula was used:

Pi = 1 / ([1+e.sup.(a - bCw)])

where Pi is the proportion of sexually mature females to the size (CW), and a and b are constants. The fit of the function was carried out using the general method of least squares (Kimura 1980). The mean size at first sexual maturity was estimated from information obtained from our experimental catch of 444 females, distributed into 16 size classes.

Lengths of right and left chelae were compared for both sexes using a paired t-test. Morphometric maturity of males was based on the relative change in chela growth that represents the acquisition of secondary sexual characters (Hartnoll 1969). This method assumes that when chela and carapace measurements are plotted against each other on a double logarithmic scale, the points lie along two straight lines, one describing the relative growth for juveniles, the other describing the relative growth for adults (Somerton 1981). For this, judging the scatterplot of chela size versus carapace width, required values of juvenile and adult bound. A principal component analysis (PCA) was previously carried out with the above variables ([log.sub.10] ChL and [log.sub.10] CW) with the attempt to distinguish two groups of males, which would represent juveniles and adults. The allometry of the chelipeds was estimated by a simple linear regression using [log.sub.10]-transformed data, according to Sampedro et al. (2003):

ChL = [log.sub.10] a + [log.sub.10] CW

Host parasite relationships were analyzed to assess potential effects of sacculinid infection on reproduction of P. patagonicus. The terminology for prevalence and mean intensity of infection follows Bush et al. (1997).

RESULTS

All crabs collected were hard-shelled. Only individuals exceeding 50 mm in CW were caught. Of 807 crabs caught, 36% (289) were males and 64% (518) were females. The size frequency distributions differed significantly between sexes with males larger than females (Fig. 2; KS-statistic = 0.34; P = 0.002). There were significant differences in size between females, parasitized individuals and males (Tables 1, Table 2; ANOVA; P < 0.05). The males had the highest CW values (Tukey, P < 0.05) and the parasitized crabs had the lowest CW values.

The ratio of females to males collected was 1.8:1 and was significantly different from 1:1 ([chi square] = 72.5, P < 0.001). A total of 39% of females carried egg masses. All the parasitized crabs (n = 73) were females, as was confirmed by the presence of four pairs of pleopods on abdominal segments.

The total weight of individuals was related with carapace width and varied significantly with sex and condition (ANCOVA; P < 0.001; Table 3). Male red crabs above a size of 90 mm CW had a higher mean weight than the females at similar carapace widths. The nonparasitized females were heavier (37% more) at a highly significant level than the parasitized females (Tukey test; P < 0.05; Fig. 3). The mean weight of the externae of the parasite was 4.12 g (SD = 1.28).

The prevalence of this parasite in the catches was 9%, whereas the mean intensity was one parasite per host, with the exception of three crabs hosting two parasites. The parasitized crabs resembled juveniles and no parasitized females contained eggs within the abdominal cavity, which was completely invaded from the outside by the externae of the parasite (Fig. 4).

Size at First Maturity

The mean size at first maturity was estimated to be 87.66 mm for females of P. patagonicus (Fig. 5). The proportion of ovigerous females decreased beginning with those having CW greater than 100 mm.

[FIGURE 2 OMITTED]

In males, chela length did not differ significantly between the right (mean = 58.41 mm, SD = 11.24, n = 35) and the left (mean = 58.32, SD = 11.13, n = 35) (t = 0.03; P = 0.953). Also, in females, differences were not significant with a mean of 41.71 mm (SD = 7.58, n = 35) and 41.60 mm (SD = 7.24: n = 35) for right and left chelae, respectively. Damaged chelae were found in 3.8% of 430 females examined, and in 16% of 289 males examined. To estimate the size at first maturity in males we used only the right chela length. The morphometric relationship of ChL versus CW between males and females of P. patagonicus differed significantly, with males having a larger chela for a given carapace width (ANCOVA; P < 0.05). The PCA carried out with [log.sub.10] ChL and [log.sub.10] CW, did not allow differentiating two groups of males, juveniles and adults. Small males showed greater variations in length of the chelae with respect to carapace width. Slope and intercept of a Log-linear function adjusted for the overall ranges of size data of males were similar, not providing a good discrimination between juveniles and adults (Fig. 6). This method did not denote size at which allometry changed and then, it could not be used to estimate maturity for the red crabs caught during the experiment.

DISCUSSION

As most of the crabs studied in the rest of the world (Hartnoll 1969, Williams 1974, Winget et al. 1974, Boschi et al. 1984), males of P. patagonicus were larger than females, and had larger chelae. Most of the catches were made up of females and half of the females were carrying eggs. In other crab species like Cancer pagurus (Bennett & Brown 1983) and Uca spp. (Christy & Salmon 1984, Murai et al. 1987), females cease to feed, whereas spawning and incubating their eggs. P. patagonicus females seem to continue feeding when carrying eggs and then, they are very vulnerable to trap fishing. This finding must be considered in the design of management measures in a future fishery targeting this species. Catches of females are usually forbidden in crab fisheries around the world, as a mean to conserve the reproductive capacity of a stock (Caddy 1989).

As shown, the sex ratio of the trap catches was female dominated during the period and zone studied. This biased ratio would also reflect a great male mortality. Judging the 16% of the males found with their chelae damaged, a higher mortality rate is possible in this area during the breeding period.

The size-weight relationship of this species was similar, in value ranges, to that obtained for Cancer irroratus by Krouse (1972), although this author did not find differences between sexes as were found in the present study. Olmi and Bishop (1983) suggested that the morphometric relationships of Callinectes sapidus could vary among locations, between sexes, degree of sexual maturity, molt stage, and carapace form. Somerton (1981) found an important stratification of sizes with depth for three species of the genus Lithodes in Alaska. Because the mesh size of traps used in the San Matias Gulf was 40 mm and there were not used escape rings, the absence of individuals smaller than 60 mm CW suggest a spatial segregation by size in this area. Stehlik et al. (1991) found that the size frequency distributions of four crab species in the North Atlantic varied among zones and between sexes, indicating that the availability of food probably affected the distribution of the species studied. Krouse (1972) also noted differences among size frequencies between males and females of C. irroratus in the Gulf of Maine, which was attributed to the fact that in the areas studied there were no small-sized males.

Size at First Sexual Maturity

The estimate of the size at sexual maturity in crabs is related to (a) the reproductive capacity (Conan & Comeau 1986, Paul & Paul 1990, Paul 1992, Sainte-Marie et al. 1995) and (b) the morphometric changes (Somerton 1980, 1981, Conan & Comeau 1986, Paul & Paul 1990, Paul 1992, Sainte-Marie et al. 1995). As small males, although sexually mature, have little chance of mating with large females, it has been suggested as more reasonable to estimate sexual maturity on the basis of morphometric criteria, considering the allometric increase in the chelipeds, which is related to courting and mating behavior (Rodhouse 1984, Jivoff 1997). We have been unable to determine the size at first maturity in males based on the linear relationships between chela length and carapace width. Although in our study a good fit for the ChL and CW relationship was obtained, a good discrimination between juveniles and adults was not identified. This requires determining the size at which physiological maturity is attained, to provide data to complement those already available, to obtain information on the sizes at which the males attain maturity. In majid species, plots of logarithms of chela dimensions against the log of the body size of males demonstrated a distinct change in allometry (Hartnoll 1969). Nevertheless, for males of some nonmajid species (Goshima et al. 2000, Hall et al. 2006), these plots may not exhibit allometric changes with sufficient confidence.

[FIGURE 3 OMITTED]

[FIGURE 4 OMITTED]

The size of berried females has been proposed as a key indicator in P. patagonicus, which, however, requires some improvement and comparison with results obtained from traditional methods used for other crustaceans (Somerton 1980, Sanpedro et al. 2003). The proportion of ovigerous females decreased at large sizes (CW > 100 mm). In most of Cancer species, viable sperm may be retained for >2 y and used to fertilize successive broods without the occurrence of a moult (Gardner 1997). A pattern of declining fecundity for successive broods produced between moults, was observed in most Cancer species (Shields et al. 1991, Gardner 1997). There are not previous studies on P. patagonicus and we do not know if it has successive broods between moults. The insufficient remaining sperm reserve may constitute a factor limiting reproductive output in the older females. Biological causes of the lower fecundity may also include the damage to pleopods (Hankin et al. 1989), nondevelopment of the ovary and senescence of older females (Gardner 1997). Sasaki and Kawasaki (1980) also showed that frequency of Ovalipes punctatus ovigerous females is higher in the intermediate size group (70-80 mm CW) but they did not discuss the main possible reasons.

[FIGURE 5 OMITTED]

In addition, it is probable that the size of the males at first maturity may be greater than in females, as has been found in the majid crabs (Conan & Comeau 1986, Ennis et al. 1988, Paul 1992). Sanpedro et al. (2003) suggested that given the large variability in the size at first maturity within the same cohort, any minimum size used in regulation may result in prohibition of the extraction of a portion of adults, and in the long term the protection of small adults may produce selective pressure on size at first maturity of exploited populations. For this reason, and following a strategy of precautionary management, besides a minimum size rule, no-take or protected areas should be enforced.

Presence of Sacculinid Parasites

Rhizocephalan parasites of crustaceans are well known to cause various abnormalities in the host such as castration (Boschma & Haynes 1969), reduction in growth rate (Hawkes et al. 1987), cessation of molting, lethargy, precocious maturation, and feminization of parasitized males (Weng 1987, Sumpton et al. 1994, Mathieson et al. 1998). In the present study, P. patagonicus females were affected by sacculinids and no parasitized females were found bearing eggs. The juvenile aspect and the small sizes of the hosts suggested the occurrence of castration in these individuals. Rhizocephalan parasites decreased the sizes of infested C. maenas and suggested that interference with molting occurred in the emergent stage of the parasite in adults of this crab (Veillet 1945, in Guillory et al. 1998, Hines et al. 1997). Condition factors were significantly lower in male blue and golden king crabs parasitized by the rhizocephalan Brairosaccus callosus (Hawkes et al. 1987), suggesting, as may occur in P. patagonicus, that growth of the host crabs is decreased. Guillory et al. (1998) indicated that the size at first maturity in the blue crab C. sapidus could vary because of infestation by Sacculina sp. If we compare the size at first maturity (86 mm) and the mean size of infested female crabs (82 mm) we can suggest that the reproductive performance is being affected. Then, in the present study the size at first maturity and reproductive capacity of P. patagonicus could be affected by presence of the parasite, even producing significant interference at the population level.

[FIGURE 6 OMITTED]

Based on the prevalence observed in this study, infestation by sacculinids may have an important impact on the reproductive capacity of the resource and its fishery potential. Then, the parasitism by sacculinid must be monitored after the starting of an emerging fishery to assess the actual contribution on the reproductive stock.

We do not know if there is a stock-recruitment relationship in this species, but at present, whereas the stock has remained unexploited, the balance between sexes appears to be sufficient to guarantee the reproductive success. If the exploitation of this species becomes relevant with the starting of a new fishery, then, the size at first maturity estimated in the present study may be used as an alternative measure in the context of a management strategy. In such case, a minimum legal width referenced to the first maturity size, may allow significant escapement of females from fishing pressure.

ACKNOWLEDGMENTS

The authors thank the staff of the Instituto de Biologia Marina y Pesquera A. Storni. This research was supported with funds by the ANPCyT (Agencia de Promocion Cientifica y Tecnologica) through the grant PID #371. Special thanks are indebted to Paul Osovnikar, "Kelo" Camarero and Luis Sarmicnto.

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Weng, H. T. 1987. The parasitic barnacle, Sacculina granifera Boschma, affecting the commercial sand crab, Portunus pelagicus (L.), in populations from two different environments in Queensland. J. Fish Dis. 10:221-227.

Williams, A. B. 1974. The swimming crabs of the genus Callineetes (Decapoda: Portunidae). Fish. Bull. (Wash. DC) 72:685-798. Winget, R. R., D. Maurer & H. Seymour. 1974. Occurrence size composition and sex ratio of the rock crab, Cancer irroratus Say and the spider crab, Libinia emarginata Leach in Delaware Bay. J. Nat. Hist. 8:199-205.

Zar, J. H. 1999. Biostatistical analysis, 4th ed. Englewood Cliffs, N J: Prentice Hall.

MAITE NARVARTE, (1) * RAUL GONZALEZ, (1) SILVIA GUAGLIARDO, (2) DANIEL TANZOLA (2) AND LORENA STORERO

(1) Instituto de Biologla Marina), Pesquera Almirante Storni. Guemes 1030. (8520) San Antonio Oeste-Rio Negro. Argentina; (2) Departamento de Biologia, Bioquimica y Farmacia. Universidad Nacional del Sur. San Juan 670 (8000) Bahia Blanca--Buenos Aires, Argentina

* Corresponding author. E-mail: maitenarvarte@canaldig.com.ar
TABLE 1.
Mean carapace width and total weight in females (without eggs),
ovigerous female, parasited female and male crabs
(only complete crabs were considered for TW).

 CW (SD) (mm) TW (SD) (mm) N

Females 94.24 [+ or -] 10.77 194.28 [+ or -] 56.77 244
Females with
 eggs 93.58 [+ or -] 7.97 215.38 [+ or -] 51.84 201
Parasitized 82.13 [+ or -] 6.06 122.84 [+ or -] 24.33 73
Males 98.63 [+ or -] 12.09 263.03 [+ or -] 70.03 289

TABLE 2.
Results of ANOVA carried out to compare mean sizes (CW)
among individuals of P. patagonicus in different condition,
including: females with eggs, females without eggs, individuals
parasitized by sacculinids, and males.

Source SS df MS F P Value

Condition 13532.12 3 4510.71 41.16 <0.0001
Error 85805.30 783 109.59
Total 99337.41 786

Tukey test: females with parasite (CW mean = 81.82 mm) < females with
eggs (CW mean = 93.58 mm) < females (CW mean = 94.24 mm) < males
(CW mean = 98.63 mm) (P < 0.05).

TABLE 3.
ANCOVA results obtained in morphometric comparisons
(Log CW-Log TW) between sexes for P. patagonicus.
CW = covariable. (Note: In cases with parasitism by the
sacculinid, the weight of the parasite is not included in
the total crab weight).

 Source SS df MS F P Value Coef

Model 17.91 4 4.48 1474.60 <0.0001
Condition 0.79 3 0.26 87.04 <0.0001
Log CW 13.34 1 13.34 4394.31 <0.0001 2.72
Error 2.31 762 0.00
Total 20.22 766

Tukey Test: parasitized individuals < females
< females with eggs = males (P < 0.05).
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Author:Narvarte, Maite; Gonzalez, Raul; Guagliardo, Silvia; Tanzola, Daniel; Storero, Lorena
Publication:Journal of Shellfish Research
Date:Aug 1, 2007
Words:5354
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