Sexual Dimorphism, Allometry, and Size at First Maturity of the Caribbean King Crab, Mithrax spinosissimus, in the Florida

Keys
Author(s): J. Antonio Baeza , Joshua R. Anderson , Angelo J. Spadaro and Donald C. Behringer Source: Journal of Shellfish Research, 31(4):909-916. 2012. Published By: National Shellfisheries Association DOI: http://dx.doi.org/10.2983/035.031.0401 URL: http://www.bioone.org/doi/full/10.2983/035.031.0401

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Journal of Shellsh Research, Vol. 31, No. 4, 909916, 2012.

SEXUAL DIMORPHISM, ALLOMETRY, AND SIZE AT FIRST MATURITY OF THE CARIBBEAN KING CRAB, MITHRAX SPINOSISSIMUS, IN THE FLORIDA KEYS

J. ANTONIO BAEZA,1,2* JOSHUA R. ANDERSON,3,4 ANGELO J. SPADARO5 AND DONALD C. BEHRINGER3,4 1 Smithsonian Marine Station at Fort Pierce, 701 Seaway Drive, Fort Pierce, FL 34949; 2Departamento de Biologa Marina, Facultad de Ciencias del Mar, Universidad Catolica del Norte, Larrondo 1281, Coquimbo, Chile; 3School of Forest Resources and Conservation, Fisheries and Aquatic Sciences Program, University of Florida, Gainesville, FL 32653; 4Emerging Pathogens Institute, University of Florida, P.O. Box 100009, 2055 Mowry Road, Gainesville, FL 32610; 5Department of Biological Sciences, Old Dominion University, Norfolk, VA 23529
ABSTRACT The Caribbean King crab Mithrax spinosissimus is the largest brachyuran found in the western Atlantic and it supports subsistence and small commercial sheries throughout the Caribbean and Gulf of Mexico. Because of its short larval duration and rapid growth, M. spinosissimus is considered a good candidate for aquaculture. Our study documents for the rst time the size at sexual maturity, sexual dimorphism, and allometric growth relative to carapace width for certain secondary sexual characters in male and female M. spinosissimus from the Florida Keys, Florida. Using principal component analysis, K-means cluster analysis, and discriminant analysis, we identied 2 major growth phases in the postlarval benthic life of this species (juvenile or prepubertal and adult or pubertal). The typical growth pattern for majoid crabs includes a third, intermediate growth phase that appears absent in M. spinosissimus. The major cheliped of males was larger than that of females and exhibited positive allometric growth to maturity, after which the level of allometry decreased. In females, both chelipeds exhibited positive allometry throughout ontogeny. Abdominal width was negatively allometric throughout ontogeny in males, whereas in females the abdomen exhibited positive allometric growth until reproductive maturity, at which point it became isometric. Logistic regression indicated that the carapace width at rst maturity was 45.2 mm in males and 69.7 mm in females. This new information should be taken into account when assessing stocks and setting harvest regulations if this shery is to be managed sustainably. KEY WORDS: King crab, size at rst maturity, male morphotypes, sexual dimorphism, sex ratio, Mithrax spinosissimus

INTRODUCTION

Spider crabs that belong to the economically important superfamily Majoidea (sensu Ng et al. 2008) display considerable diversity in body size, coloration, morphology, and behavior (Rathbun 1925, Baeza et al. 2009). For instance, the petite but colorful Mithraculus sculptus and Mithraculus forceps from the Caribbean are heavily harvested for the marine ornamental industry (Penha-Lopes et al. 2005, Rhyne et al. 2005). Other spider crabs that attain large body sizes are the focus of lucrative seafood sheries in temperate regions (e.g., Maja squinado in the Mediterranean (Sampedro et al. 1999, Sampedro et al. 2003), Chionoecetes opilio in the Bering Sea (Allunno-Bruscia & Sainte-Marie 1998)). In turn, overshing and a high market value have led to an examination of the aquaculture potential for several species, including Mithrax forceps (Penha-Lopes et al. 2005, Rhyne et al. 2005), Mithraculus sculptus (Rhyne et al. 2005), and Mithrax spinosissimus (Brownell et al. 1977, Adey 1987, Tunberg & Creswell 1988, Wilber & Wilber 1991). Thus, studies on the life history of spider crabs are warranted to inform sheries management and aquaculture (including stock enhancement) protocols. Although, the biology and ecology of spider crabs are quite diverse, some life history traits appear conserved within this clade (Baeza et al. 2009). All species studied thus far feature 2 free-swimming zoea larval stages followed by a single postlarval megalopa stage (Hartnoll 1965, Brownell et al. 1977,
*Corresponding author. E-mail: BaezaA@si.edu DOI: 10.2983/035.031.0401

Goy et al. 1981, Tunberg & Creswell 1988, Tunberg & Creswell 1991, Rhyne et al. 2006). Likewise, a very brief prezoeal stage has also been described in some species (e.g., Mithrax pleuracanthus (Goy et al. 1981), Mithrax spinosissimus (Provenzano & Brownell 1977, Tunberg & Creswell 1988)). However, its occurrence has been suggested as resulting from stress of either the gravid female or the developing embryos (Tunberg & Creswell 1988). Most majoid species studied also have 3 postlarval ontogenetic phases of development (Hartnoll 1965, Sampedro et al. 1999, Carmona-Suarez 2003). The rst immature or juvenile phase and the second prepubertal phase are separated by a prepubertal critical molt, after which the level of allometry of the chelipeds and gonopods (modied pleopods) in males and the abdomen in females increase substantially (Hartnoll 1965, Hartnoll 1974, Hartnoll 1978, Allunno-Bruscia & Sainte-Marie 1998). The third adult phase begins after the pubertal and possibly terminal molt, which commonly entails considerable changes in the size, overall shape, and dentition of the chelipeds in males and of the abdomen in females (Sampedro et al. 1999, Sampedro et al. 2003). After the pubertal molt, growth ceases and individuals become sexually active; females mate any time after this nal molt and produce successive broods with sperm stored in their spermatheca (Hartnoll 1965, Hartnoll 1974, Sampedro et al. 1999). More important, males from various species have been shown to produce sperm (e.g., Mithraculus ndez-Reyes et al. 2001), Maja squinado (Sampedro forceps (Herna et al. 1999)) and inseminate females prior to the terminal molt (e.g., Maja crispata (Carmona-Suarez 2003)). A few species deviate from this basic life history pattern. For instance, males of Maja squinado (Sampedro et al. 1999,

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Goshen College Marine Laboratory, Long Key, FL, where all measurements were taken.
Measurement of Specimens of Mithrax spinosissimus

Sampedro et al. 2003) and Maja crispata (Carmona-Suarez 2003) exhibit 3 ontogenetic phases, but females exhibit only 2 phases: a prepubertal and an adult stage separated by the pubertal molt (Sampedro et al. 1999, Carmona-Suarez 2003, Sampedro et al. 2003). In other species (e.g., Leurocyclus tuberculosus, Mithrax tortugae), males and females exhibit only 2 distinct postlarval ontogenetic phases distinguished by the level of allometry and relative size of the abdomen and chelipeds n et al. 2009, Cobo & in females and males, respectively (Baro Alves 2009). Clearly, more studies are necessary to fully understand life history strategies in spider crabs. The Caribbean King crab, Mithrax spinosissimus, is the largest native crab in the tropical and subtropical western Atlantic, attaining a carapace length up to 180 mm and weighting more than 3 kg (Rathbun 1925, Tunberg & Creswell 1988, Winfree & Weinstein 1990, Tunberg & Creswell 1991, Wilber & Wilber 1991). This species exhibits a Caribbeanwide distribution, ranging from North Carolina to the northeastern coast of Venezuela (Rathbun 1925, Winfree & Weinstein 1990, Tunberg & Creswell 1991). The Caribbean King crab, M. spinosissimus, inhabits structures and ledges in the shallow subtidal to depths approaching 200 m. Crabs remain cryptic during daylight hours and emerge from shelter shortly after sunset to forage on algal turfs and macroalgae through the night (Winfree & Weinstein 1990, Tunberg & Creswell 1991, Wilber & Wilber 1991). Little is known about the basic life history of M. spinosissimus, but as reported for other majid crabs, 2 zoea larval stages occur prior to the postlarval megalopa stage (Brownell et al. 1977, Tunberg & Creswell 1988). It remains to be addressed the number of postlarval ontogenetic phases in males and females of M. spinosissimus. The short larval period (;6 days from zoea I to Megalopa), rapid growth, and continuous reproduction make M. spinosissimus a candidate for aquaculture (Brownell et al. 1977, Winfree & Weinstein 1990, Tunberg & Creswell 1991, Wilber & Wilber 1991). Incidental subsistence and artisanal sheries for M. spinosissimus are prevalent in various parts of the Caribbean and Gulf of Mexico (J. A. B. and D. C. B., pers. obs.) and a signicant commercial shery developed in Panama years ago (Wilber & Wilber 1991, Guzman & Tewk 2004). In this study we report previously unknown life history information about Mithrax spinosissimus. We studied sexual dimorphism, relative growth of secondary sexual characteristics, and size at rst maturity in males and females from the Atlantic and Gulf of Mexico sides of the Florida Keys. Our goals were to determine the number of postlarval growth (morphological) phases in this crab and to report other life history information (sexual dimorphism, sex ratio, size at rst maturity) needed for improving sheries management and aquaculture protocols of this economically valuable crab.
MATERIAL AND METHODS Sampling of Mithrax spinosissimus

The carapace width (CW) and carapace length (CL), the abdominal width (AW; measured at the junction between the fourth and fth abdominal segment), the length of the propodus of the major cheliped (ChL), the length of the second right pleopod (2PL), and the length of the merus of the second and third left pereopod (rst [1L] and second [2L] walking leg, respectively) of each crab were measured using an SPI 2000 series dial caliper (precision, 0.1 mm). Crabs were classied as male or female depending on the shape of the rst pleopods (i.e., rigid and modied as gonopods in males but exible, long, and setose in females) and the width of the abdomen (considerably wider in females than in males) (Rathbun 1925). The presence or absence of embryos beneath the abdomen of females was recorded.
Allometric Growth in Mithrax spinosissimus

Individuals of Mithrax spinosissimus were collected from August 2010 to January 2011 from the subtidal (110 m depth) hard-bottom communities and coral reefs near Long Key (2449#26$ N, 8048#48$ W) and Cudjoe Key (2439.6# N, 8129.5#W), Florida Keys (Fig. 1A). At each locality, crabs (Fig. 1BD) were captured by hand while free diving or scuba diving and were transported alive to the wet laboratory at the

In brachyuran crabs, including spider crabs from the MithraxMithraculus species complex, the rst pair of pereopods bear large chelipeds that serve as weapons during interand intrasexual interactions (Hartnoll 1965). Likewise, to help protect the embryos carried beneath their abdomen (i.e., from physical abrasion) the abdominal segments are enlarged in ndez 2002). females compared with males (Baeza & Ferna We examined whether the chelipeds, abdomen, and pereopods increase linearly with body size (CW) in males and females. More specically, we compared the relationship between CW versus ChL, CW versus AW, CW versus 2PL, CW versus 1L, and CW versus 2L using the allometric model y axb (Hartnoll 1978, Hartnoll 1982). The slope b of the log-log leastsquare linear regression represents the rate of exponential increase (b > 1) or decrease (b < 1) of the measured body structures with a unit of increase in CW. To determine whether the relationship deviates from linearity, a t-test was used to test whether the estimated slope b deviated from the expected slope of unity. If the different body parts grow more or less relative to a unit increase in CW, then the slope should be greater or lesser than unity (Hartnoll 1978). To conrm the possible existence of 2 or more ontogenetic phases in Mithrax spinosissimus, a modied analysis similar to that described by Sampedro et al. (1999), Baeza and Asorey (2012) and Anderson et al. (2012) was performed using SAS/ STAT version 9.1 (SAS Institute, Cary, NC). First, a principal components analysis (PCA; using PROC PRINCOMP) between various pairs of variables (e.g., ChL vs. CW and PL vs. CW in males, and AW vs. CW in females) was conducted to determine the number of ontogenetic phases. Subsequently, a clustering analysis (K means; using PROC FASTCLUS) was used to assign growth phases to the different groups predetermined by the PCA. For this analysis, the maximum number of clusters was set at 2 based on the PCA results (Nclusters 2; see Results). Last, a bivariate linear discriminant analysis (using PROC DISCRIM) was used to cross-validate our results. This analysis permitted us to classify each crab into a discrete ontogenetic phase previously identied by the PCA and clustering analyses, with CW treated as the independent variable.

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Figure 1. (A) Map of the study site in the Florida Keys, FL. The arrow points at Long Key. (B) Dorsal view of the Caribbean King Crab Mithrax spinosissimus (scale bar$ 5 cm) (C). In situ photograph of a female crab in Curley Key, Belize (D) In situ photograph of a male crab near Long Key, FL. Notice the exaggerated claws in males but not in females. Photo credits: J. A. Baeza. ChL, length of the propodus of the major chelipeds; CL, carapace length; CW, carapace width.

If these analyses indicated the existence of different growth phases in Mithrax spinosissimus, then different allometric equations were calculated for each of the growth phases. The body size (CW) that separated different ontogenetic stages, both in male and female M. spinosissimus, was determined using a logistic regression (Wilson & Hardy 2002).
Size at Maturity in Mithrax spinosissimus

RESULTS Sexual Dimorphism and Allometry in Mithrax spinosissimus

In females, size at rst maturity was estimated as the CW at which the probability of encountering embryos was 0.5 using a logistic regression (Wilson & Hardy 2002). We also estimated behavioral size at rst maturity in males and females using a logistic regression. Behavioral maturity was estimated as the size at which the probability of having a movable abdomen was 0.5. In brachyuran crabs, including representatives of the MithraxMithraculus species complex, the abdomen is xed (engaged to the sternum) in immature individuals and it usually clicks or breaks when attempting to separate it from the ventral sterna with a probe. In contrast, the abdomen is movable in mature males and females (see Sal Moyano et al. (2011) and Bolan os et al. (2012) and references therein).

The mean (SD) CW for male crabs was 65.4 25.6 mm with a range of 21.9144.6 mm (n 83); for female crabs it was 57.5 19.3 mm with a range of 18.9106.5 mm (n 87). A signicant difference in CW between the sexes was detected (t-test: t 2.31, P 0.0219), indicating sexual dimorphism with respect to body size in Mithrax spinosissimus (Fig. 2). A positive correlation between the CW and the length or width of the different body structures was detected for crabs of both sexes (P < 0.001 in all cases). Structures also differed in the status and degree of allometry depending on sex (Table 1). In both sexes, the slope of the relationship between CW versus CL was signicantly less than unity; in other words, CL experienced negative allometric growth relative to CW (Table 1, Fig. 3). The merus of the second walking legs also experienced negative allometry in both sexes (Table 1, Fig. 3). In contrast, the merus of the rst walking legs grew proportionally in males, but the same structure featured signicant negative allometry in females (Table 1, Fig. 3).

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disproportionally (with negative allometry) throughout ontogeny, and examination of the data did not indicate any visible shift in ontogenetic phase. Female cheliped size underwent positive allometry throughout ontogeny, and the data indicate the existence of a single growth phase. In males, however, principal components and clustering analyses detected 2 ontogenetic phases. Discriminant analysis assigned correctly 92.8% of the crabs (77 of 83) to 1 of the 2 previously recognized ontogenetic groups. Logistic regression indicated that the CW at which 50% of the males changed from the rst to the second ontogenetic phase (according to the status and degree of allometry of the cheliped) was 64.85 mm (condence limits 62.92 mm and 66.59 mm, respectively). In males, the major cheliped underwent a highly positive allometric growth during the rst ontogenetic phase, then the degree of positive allometry decreased during the second phase (Table 1, Fig. 4). Last, the female second pleopod length underwent positive allometry throughout ontogeny, and the data indicate the existence of a single growth phase. In males, however, principal components and clustering analyses detected 2 ontogenetic phases. Discriminant analysis assigned correctly 98.8% of the crabs to 1 of the 2 previously recognized ontogenetic groups. Logistic regression indicated that the CW at which 50% of the males changed from the rst to the second ontogenetic phase (according to the status and degree of allometry of the pleopod) was 60.1 mm (condence limit 53.9 mm and 67.25 mm, respectively). In males, the pleopod underwent positive allometric growth during the rst phase, then negative growth during the second phase (Table 1, Fig. 4).
Size at Maturity in Mithrax spinosissimus

Figure 2. Sizefrequency distribution of the spider crab Mithrax spinosissimus in the Florida Keys, FL. Black bars denote males and white bars denote females. Note how males (n$ 83) attain larger mean and nal body sizes compared with females (n $ 87; see Results for details).

Visual examination of the relationship between CW versus CL and between CW versus merus length of the 2 walking legs did not indicate the presence of different ontogenetic phases in either sex. In contrast, visual examination of the relationship between CW versus AW in females suggested the existence of 2 ontogenetic phases (Fig. 4). Principal components and clustering analyses conrmed the existence of these 2 ontogenetic phases, herein named prepubertal (immature) and pubertal (mature) phases. Discriminant analysis cross-validated our nding, with 90.8% of the females (79 of 87) being assigned correctly to 1 of the 2 ontogenetic groups recognized previously by principal components and clustering analyses. Logistic regression indicated that the CW at which 50% of the females change from the prepubertal to the pubertal phase was 58.77 mm (condence limits 57.38 mm and 59.71 mm, respectively). The abdomen of small, immature females exhibited positive allometric growth until maturity, at which point growth became isometric (Table 1, Fig. 4). In turn, the abdomen of males grew

Logistic regression indicated that the CW at which 50% of the females achieved maturity (measured as the probability of

TABLE 1.

Growth of selected structures relative to the carapace width (CW) in both sexes of the spider crab Mithrax spinosissimus.
y Males CL AW PLsmall PLlarge ChLsmall ChLlarge 1L 2L Females CL AWsmall AWlarge PL ChL 1L 2L x CW CW CW CW CW CW CW CW CW CW CW CW CW CW CW Regression y 0.9151 3 0.1284 y 0.9385 3 0.7105 y 1.1426 3 0.6866 y 0.8603 3 0.1863 y 1.1447 3 0.6297 y 1.1155 3 0.4840 y 0.9772 3 0.2112 y 0.9329 3 0.1597 y 0.9373 3 0.0938 y 1.4019 3 1.1177 y 0.9392 3 0.1079 y 1.7075 3 1.5206 y 1.0288 3 0.4700 y 0.8803 3 0.0719 y 0.9029 3 0.1293 SEs 0.0066 0.0170 0.0536 0.0468 0.0215 0.0442 0.0170 0.0179 0.0056 0.0289 0.0543 0.0387 0.0138 0.0169 0.0168 r2 0.9978 0.9734 0.9285 0.8869 0.9869 0.9565 0.9756 0.9712 0.9969 0.9914 0.8769 0.9595 0.9852 0.9704 0.9720 ts 10.81 3.62 7.75 9.82 6.72 2.61 1.34 2.06 11.16 13.92 1.12 44.09 2.09 7.09 4.43 P <0.001 <0.001 <0.001 0.0444 <0.001 0.0141 0.1843 0.0429 <0.001 <0.001 0.2690 <0.001 0.0394 <0.001 <0.001 Allometry + + + 0 + 0 + +

The regression equations, standard errors of the slopes (SEs), correlation coefcients (r2), t-test statistic (ts) and P values obtained when testing whether the different slopes differ from the unity. The allometric status of each studied variable are shown: carapace length (CL), length of the propodus of the major cheliped (ChL), width of the abdomen at the level of the junction between the fourth and fth somite (AW), length of the left pleopod (PL), length of the merus of the left rst walking leg (1L), and length of the merus of the left second walking leg (2L). Small crabs pertaining to the rst ontogenetic stage. Large crabs pertaining to the second ontogenetic stage.

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Figure 3. (AC) Allometric growth of different morphological traits featuring a single ontogenetic growth phase relative to the carapace width in both sexes of the spider crab Mithrax spinosissimus. The graphs show the logarithm of the carapace length (A), the length of the merus of the second pereopod (B), and the length of the merus of the third pereopod (C) as a function of the logarithm of the carapace width. The slopes (b) of the different relationships are also presented. Black circles denote males (n $ 83) and white circles denote females (n $ 87).

carrying embryos) was 71.2 mm (condence limit 67.077.6 mm). In turn, the CW at which 50% of the males and females achieved behavioral size at rst maturity was 45.2 mm (condence limit 39.948.9) and 69.7 mm (condence limit 66.5 73.5), respectively (Fig. 5).
DISCUSSION

In Mithrax spinosissimus, males attained a larger average and nal body size than females. This pattern of sexual dimorphism in body size (males > females) agrees with previous observations of this species (Tunberg & Creswell 1988, Winfree & Weinstein 1990, Tunberg & Creswell 1991, Wilber & Wilber 1991, Guzman & Tewk 2004) and of several other spider crab species (e.g., Hartnoll 1965, Hartnoll 1974, Sampedro et al. n et al. 1999, Carmona-Suarez 2003, Sampedro et al. 2003, Baro 2009; but see Cobo and Alves (2009)). Thus, our results for Mithrax spinosissimus support the notion that classic sexual dimorphism (males > females) is the rule in the Majoidea. When male sexual competition for sexual partners is intense and monopolization of receptive females occurs via overt aggression, males are expected to attain larger body sizes than females (Shuster & Wade 2003, Baeza & Thiel 2007). In agreement with this notion, preliminary observations in the laboratory have shown that the largest crabs almost invariably win during agonistic interactions between pairs of male crabs and, while collecting, we observed a mating pair of Mithrax spinosissimus that involved a male that was the largest compared with the other males in the surroundings (J. A. B., pers. obs.). Unfortunately, no other details are known about the reproductive biology of this crab, including malemale agonistic competition and female mate choice. Experiments examining

the effect of male body size in determining the outcome of competitive interactions among males for receptive females might help to explain sexual dimorphism in M. spinosissimus. The Caribbean King crab Mithrax spinosissimus is sexually dimorphic with respect to body size but also with regard to allometric status, growth rate, and relative size of various body parts. For instance, the abdomen was wider in females than in males and exhibited positive allometric growth in females up to maturity, after which this structure became isometric. In males, the abdomen exhibited negative allometry throughout ontogeny. The major cheliped also exhibited positive allometry in both sexes, but during the second growth phase males attained larger claws than females. This overall pattern of sexual dimorphism in the major cheliped and abdomen agrees with that reported in the literature for other spider crabs (Hartnoll 1965, Hartnoll 1974, Sampedro et al. 1999, Carmona-Suarez 2003, n et al. 2009). In females, wide Sampedro et al. 2003, Baro abdomens may translate into larger clutch sizes (Crawford & De Smidt 1922). Similarly, in males, larger claws might increase the likelihood of winning during agonistic interactions for access to receptive females, considering that dominance in crabs is largely determined both by body size (described earlier) and relative cheliped size (Scho ne 1968, Warner 1970, Hartnoll 1974). The exaggeration of body parts relevant for reproduction, such as those listed here, before or at the onset of sexual maturity is considered an adaptation for increasing reproductive output (e.g., in females) or mating success (e.g., in males), allowing individuals to optimize tness over their lifetime (Anderson et al. 2012). Male cheliped length and pleopod length and female abdomen width experienced substantial shifts in growth rate during ontogeny. These shifts occurred over a narrow body size range, indicating the existence of 2 ontogenetic phases in Mithrax

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Figure 4. (AC) Allometric growth of 3 morphological structures relative to the carapace width in both sexes of the spider crab Mithrax spinosissimus. The graphs show the logarithm of the abdominal width measured at the second segment (A), the length of the propodus of the chelipeds (B), and the pleopod length (C) as a function of the logarithm of the carapace width. Detected ontogenetic phases along with their corresponding slopes (b) are shown in males (n $ 83) and/or females (n $ 87). AF, adult females; AM, adult males; F, females from the 2 ontogenetic stages; JF, juvenile females; JM, juvenile males; M, males from the 2 ontogenetic stages.

n spinosissimus, as reported before in other spider crabs (Baro et al. 2009, Cobo & Alves 2009). Nonetheless, spider crabs most commonly exhibit 3 ontogenetic phases (Hartnoll 1965, Hartnoll 1974, Hartnoll 1978, Allunno-Bruscia & Sainte-Marie 1998). In females, the body size at which this shift in abdominal allometry occurred (CW, 58.77 mm) was smaller than our estimates of size at rst maturity based on the adherence of the abdomen to the ventral sterna (CW, 69.7 mm) and on the presence of embryos beneath the abdomen (CW, 71.2 mm). The latter 2 estimates of size at rst maturity occurred at the same body size (taking into account the condence intervals for these estimates; see Results). This suggests that behavioral maturity (abdomen exibility) is not synchronized with morphological (allometric shifts) and functional maturity (brooding) in female M. spinosissimus. Instead, the development of the abdomen precedes egg production during ontogeny of the females. This succession of changes in abdominal exibility and proportion is possibly benecial to females given that an exaggerated abdomen is probably only essential after puberty, but to be advantageous at maturity their shape and size must change and increase prior to the onset of sexual maturity (see Anderson et al. 2012). In males, the body size at which the allometric shift in cheliped size (CW, 64.85 mm) and pleopod length (CW, 60.1 mm) were observed was much larger than our estimate of behavioral maturity based on adherence of the abdomen to the ventral sterna (CW, 45.2 mm). No intermediate (adolescent) phase was apparent in males, in disagreement with that reported for various other species of spider crabs (Hartnoll 1965, Hartnoll 1974, Sampedro et al. 1999, Carmona-Suarez 2003, Sampedro et al. 2003) but in agreement with that reported for Leurocyclus tuberculosus and Mithrax tortugae, 2 species that n et al. 2009, Cobo & exhibit only 2 ontogenetic phases (Baro

Alves 2009). More important, preliminary dissections have demonstrated the presence of spermatophores packed with mature spermatozoa in the middle and posterior vas deferens of large males that pertain to the rst ontogenetic phase (with no exaggeration of chelipeds; J. A. B. pers. obs.) as reported ndez-Reyes et al. 2001) and before in Mithraculus forceps (Herna Maja squinado (Sampedro et al. 1999). Whether these large prepubertal males bearing regular-size chelipeds are capable of inseminating females, as demonstrated in Maja crispata (Carmona-Suarez 2003), remains to be addressed in Mithrax spinosissimus. However, this result suggests that physiological and probably functional maturity in males of M. spinosissimus may be attained much earlier than at the timing of the pubertal molt, when allometric and size shifts in cheliped and pleopod growth take place. Altogether, the information presented here suggests that M. spinosissimus might feature 2 different sexually active male morphotypes, each with a different mating tactic (sneaking vs. dominant), as reported before in other majoid crabs (e.g., Chionoecetes opilio (Conan & Comeau 1986) Chionoecetes bairdi (Donaldson & Adams 1989) Libinia emarginata (Sagi et al. 1991)). Additional studies in the reproductive ability of males from different ontogenetic phases are needed to test for alternative mating strategies in M. spinosissimus. Overall, uncertainty in size at maturity might have important implications for sheries stock assessment because small males without developed chelipeds might be misclassied as immature individuals, and this misclassication might result in overestimating size at rst maturity in Mithrax spinosissimus. Age-structured models built to evaluate the effect of uncertainty in size at rst maturity on stocks of exploited crustaceans have shown that even with low exploitation rates, an overestimation of size at maturity can affect values of the spawning potential

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models to recognize stock overexploitation when, in reality, overexploitation is indeed taking place (Anderson et al. unpubl. data). Studies constructing age-structured models to evaluate the effect of uncertainty in size at maturity on population assessments in M. spinosissimus are underway. Here we have improved our knowledge of the largest crab in the greater Caribbean with considerable potential for aquaculture. In Mithrax spinosissimus, males attain a larger average and nal body size than females. Two ontogenetic phases are clearly distinguishable in the 2 sexes of this spider crab by evident morphological changes. In females, these 2 phases correspond to the immature and adult life stages. In males, however, the rst detected ontogenetic phase appears to contain a combination of small immature crabs and putatively mature crabs of moderate size that do not exhibit exaggerated chelipeds. All this information needs to be taken into account when assessing the stocks of this species, establishing a sustainable shery management plan, and developing technology for aquaculture production.

ACKNOWLEDGMENTS

Figure 5. Predicted size at rst maturity for both sexes of the spider crab Mithrax spinosissimus. (A) The predicted size at rst maturity for females (n$ 87) using presence of embryos beneath the abdomen (Abd.) as a proxy for maturity. (B, C) Predicted size at rst maturity for females (B) (n $ 87) and males (C) (n$ 83) using abdomen exibility as a proxy for maturity. In each graph, the upper and lower curves are 95% condence limits.

ratio, causing the model to indicate incorrectly a stock that is being overexploited (Anderson et al. unpubl. data). Alternately, an underestimation of size at maturity could cause the failure of

We thank numerous people who helped collect or provide animals, including Rebecca Squib (UF), Casey Boleman (ODU), and Tom Matthews of the Florida Fish and Wildlife Conservation Commission, Marathon, FL. We thank Mark Butler for logistic and material assistance that helped make this study possible. This study was funded in part by the Florida Fish and Wildlife Conservation Commission (contract 103232 to D. C. B. and J. A. B.). J. A. B. was supported by a postdoctoral fellowship from Old Dominion University during the current study. This is Smithsonian Marine Station at Fort Pierce contribution no. 897.

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