Male Reproductive Biology of Mud Crab Scylla olivacea in a Tropical Mangrove Swamps
Mud crabs of the genus Scylla are commercially important and conspicuous crustaceans provide basic source of income for coastal fishing communities throughout the Indo-Pacific region. The reproductive traits and size at sexual maturity of the male mud crab Scylla olivacea were investigated in Pak Phanang mangrove swamps, Thailand. Samples were taken seven times from the local middlemen mud crab traders during June 2006 to January 2008. Gonad development was determined based on histological appearance that was classified into three stages: (1) Immature (Spermatogonia) (2) Maturing (Spermatocytes) and (3) Mature (Spermatids and Spermatozoa). Among the sample population, the highest 56% was under gonad development stage I, whereas mature stage III was only 18%. The size at first maturity was estimated by the external allometric growth and histological observation of gonad. The size at which 50% of individuals attain sexual maturity was estimated by the two mathematical models such as probit analysis and logistic curve. The mean size at first sexual maturity and 50% maturation of male S. olivacea were 87 and 103 mm Internal Carapace Width (ICW) which revealed that 80% of individuals were immature. The present result suggested that the minimum legal size of male mud crab capture should be >100 mm ICW.
Received: October 09, 2011;
Accepted: November 19, 2011;
Published: January 09, 2012
The reproductive information on a commercially exploited species is crucial
for understanding its population dynamics which is fundamental for developing
an effective management models. The minimum legal size for catch is one of the
popular management regimes in mud crab fisheries with the purpose of protecting
the reproductive potential of resource stock (Goshima et
al., 2000; Conan et al., 2001). The restriction
of the harvest to males has been considered to have relatively little impact
on the reproductive output of the stock. However, concern for the effects of
reduction of males has prompted recently which triggered out the importance
of research on male maturity (Van Engel, 1990; Knuckey,
1996; Castilho et al., 2008).
In male crustaceans, there are three common methods to determine maturity.
First is the morphometric method; using change of allometric relationship between
sizes of body parts (e.g., Somerton, 1980; Somerton
and Macintosh, 1983; Haefner, 1990; Knuckey,
1996; Viau et al., 2006). Second is the histological
(gonad) method; histological examination of the gonad to see if spermatozoa
are present in the testes and/orvas deferentia (Hartnoll,
1969; Haefner, 1990; Robertson
and Kruger, 1994; Leal et al., 2008). The
third is functional maturity; usually refereed as to ability of mate successfully
(Conan and Comeau, 1986). In fact, the main criteria
for determining functional maturity in crustaceans are the presence of scars
on the sternum or forward walking legs which are produced by abrasion with the
female during the precopulatory embrace (Prasad and Neelakantan,
1990; Robertson and Kruger, 1994; Knuckey,
1996). Another commonly considered criterion for the maturity estimation
is the presence of spermatozoids or spermatophores in the testes or vas deferentia
as well as copulation marks (Hartnoll, 1969; Krouse,
1973; Haefner, 1990; Viau et
However, the mating scar in male could not find less than 125 mm internal carapace
width (ICW) (Knuckey, 1996) and completely absence in
smaller individuals than 115 mm (Robertson and Kruger 1994).
In the present study, it is noticed that no sample crab exceeds the size of
130 mm ICW and very few were >115 mm ICW. On the other hand, no prominent
scars were found in the samples. Moreover, maturity in male crabs is not easily
determined from external characteristics (Robertson and
Kruger, 1994). Thus present study was concentrate on the histological observation
of vas deferens/testes to establish the maturity status of wild male mud crab
The male reproductive biology and maturity size of mud crab (Scylla sp.)
has been established in Australia (Knuckey, 1996) and
in South Africa (Hill, 1975; Robertson
and Kruger 1994). There were very few study have been taken in Asian countries
like, Ong (1966) from Malaysia and Lavina
(1980) from Philippines. However, there was no subsequent study. Moreover,
all the previous studies focused on S. serrata and no study on other
Scylla species particularly on S. olivacea which is the most
commercial important species in Asian region. Thus paucity of information existed
on the male reproductive biology of S. olivacea in Asian countries was
the trigger to conduct the present study to provide detailed reproductive information
of male mud crab.
MATERIALS AND METHODS
Study site: The Pak Phanang estuary is located in Nakhon Si Thamarat
province, on the east coast of southern Thailand (8°9'-11
N and 100°9-18' E). The eastern half of the estuary is
fringed by a wide mangrove forest (approximately 9,000 hectares) which is associated
with an extensive mud flat (1-3 km wide) that emerges at low tide (Fig.
1). There are three distinct seasons: Hot-dry season (February-May), rainy
season (June-September) and the highest rainfall period of monsoon season (October-January)
with water temperature ranging 25-36°C (Thampanya et
al., 2002). Average annual rainfall ranges about 2000-3000 mm and salinity
fluctuates between 1-25 ppt (Boromthanarath et al.,
1991). Crab fishing is conducted throughout the year within mangrove channels
as well as associated channels connected to the bay. In the present study, survey
was focused on the communities within the mangrove (Fig. 1).
Sampling: Male S. olivacea were collected during June 2006 to January 2008 from the local mud crab middle trades which were contributed 49% of the total sample population. In the laboratory, 84 male crabs were examined which did not include any morphological anomalies. The following measurements of body size were taken with a digital caliper to the nearest 0.1 mm: Internal Crapace Wdth (ICW), Lower Paddle Width (LPW), Propodus Length (PL) and Chela Height (CH) of left cheliped.
Histological study: Tissue from the middle vas deferens/testes from
each male was dissected and preserved in Davidsons fixation for further
||Study area, Pak Phanang mangrove ecosystem and the sampling
place (scattered communities) inside of the mangrove
The tissues were dehydrated in ascending ethanol concentrations from 70 to
100%, transferred to Lemosol (Wako Pure Chemical Industries, Osaka, Japan) and
embedded in paraffin. The tissues were sectioned to 5 μm and stained with
Mayers Hematoxylin-Eosin (HE). The histological stage of development was
determined by making reference to those of other crustaceans (Comeau
and Conan, 1992; De Lestang et al., 2003;
Mura et al., 2005; Viau et
al., 2006). The development stages of the gonad were determined by the
macroscopic appearance based on the formation of spermatocytes and presence
Estimation of size at maturity: The middle vas deferentia were used for the histological study and maturity estimation. Sexual maturity was classified with the visibility of vas deferentia and the presence of spermatophores within their lumina. The relative frequencies of each stage of sexual maturity in the samples were analyzed to describe the reproductive cycle of males.
The size at first maturity was estimated by using three methods that are described following:
||Allometric increments proportional to ICW; the allometric
growth increments of CH, PL and LPW were plotted against the increments
of ICW and existence of the flexion point was investigated and treated at
the size of first maturation in male crab
||The minimum size at maturity recorded through histological studies of
the male mud crabs (>70 mm ICW)
||Chela Height (CH)/internal carapace width (ICW) index is another method
which calculated as the divides of CH by ICW. The samples were categorized
to two groups by the critical point of CH/ICW and the histological developments
of the gonad were compared between two groups. Regression analysis was performed
to determine the relation of Chela Height (CH) with internal carapace width
(ICW). A significant level of p>0.05 was considered
Two mathematical models (1 and 2) were used to estimate the size at which 50% of the individuals had reached sexual maturity that are described below.
||Model 1: Probit analysis (Robertson
and Kruger 1994) was performed using abdomen-width data using probit
analysis to determine the size at which 50% of females reach sexual maturity
(ICW50). The data from sample crabs were allocated to 10-mm ICW
size classes. The proportion (p) of mature male in each size class was calculated
according to Mikhaylyuk (1985) that was converted
to logit (logit (p) = ln (p/1-p)). The logistic data were then converted
to probit (P) = p + 5. Finally, the probit data were plotted against ICW
and a regression line was fitted to the data points. The ICW value equivalent
to probit 5 was extrapolated as the median size at sexual maturity
||Model 2: Ratio of matured individuals determined by the histological
observation in each size class was fitted to the sigmoid curve (see the
Where, pICW is the proportion of mature to immature crabs in each
ICW class (10 mm interval) and M1 and M2 are the equation
coefficients. The best fit curve was estimated by the using of Kaleida graph
software (Kaleida graph, version 3.6) (KoolKalya et al.,
Allometric growth: The male Chela Height (CH), Propodus Length (PL)
and Lower Paddle Width (LPW) were scattered plotted against the Internal Carapace
Width (ICW) and found that the relative growth of these secondary sexual allometric
parts were increased sharply at the size of 87 mm ICW (Fig. 2).
Figure 3 shows the relation between CH/ICW and ICW that represent
a clear allometrical growth of CH/ICW with the increments of boy size.
Gonad development: A total of 84 male crabs ≥70 mm ICW) were assessed
to observe the ovarian condition. The progress of ovarian maturation was classified
into three stages based on external appearance of ovary and the development
stage of the most advanced oocytes with the histological observation (Table
1, Fig. 4).
|| Scatter plotted of chela height (mm), propodus
length (PL) and lower paddle width (LPW) against internal carapace width
(mm) of male Scylla olivacea collected from Pak Phanang mangrove
swamps, Thailand. Vertical dash line represents the probable discontinuity
increments (growth at maturity) with observed body parts at the ICW of 87.34
||The relationship of CH/ICW values regarding body size of male
Scylla olivacea collected at Pak Phanang mangrove swamps during June
2006 to January 2008. The critical CH/ICW values estimated to be 0.31 at
the body size of 90 mm ICW
||Histological sections of Vas deference in Scylla olivacea.
(a): Immature (Spermatogonia), (b): Maturing (Spermatocytes) and (c): Mature
(Spermatids and Spermatozoa). Sg, spermatogonia; Psc, primary spermatocyte;
Ssc, secondary spermatocyte; Sz, spermatozoa; Std, spermatid; Lu, lumen
The histological examination showed that among the sample population, the highest
56% was under gonad development stage I whereas only 18% was belong to the mature
stage III (Table 1). The smallest mature male and largest
immature male were recorded 84 mm ICW and 102 mm ICW, respectively.
The immature stage (stage I) was represented by gonad with spermatogonia and primary spermatocytes (Fig. 4a). The maturing stage (stage II) was characterized with the containing of secondary spermatocytes as predominately, but with the presence of primary spermatocytes in few (Fig. 4b). The mature stage was defined as the dominancy of spermatozoa with the presence of spermatids (Fig. 4c).
The size distribution of stage I, II and III ranged from 60-97 mm, 80-101 mm
and 84-123 mm ICW, respectively. No spent males were registered during the study
period. In the present study, sexually mature male were defined with the gonad
stage of III as the presence of spermatozoa.
|| Stages of physiological sexual maturity
of male Scylla olivacea and their composition in respective stage
||Proportion of male chela height (CH) and internal carapace
width (ICW) of Scylla olivacea with reflecting the different stages
of gonadal development
||Percentage maturity, after histological observation, plotted
on a probit scale against internal carapace width to obtain the size at
M50 (the point at which 50% of the male crabs are mature) of
Scylla olivacea from Pak Phanang mangrove swamps, Thailand.
Relation between allometric growth and maturation: A significant relationship was observed between CH/ICW and carapace width (R2 = 0.618, p<0.05) (Fig. 3). Table 2 shows the assemblage of the CH/ICW index relating to stages of the gonad development. The CH/ICW values ranging from 0.21 to 0.30 were completely belongs to stage I-II, indicating the immature male. On the contrary, majority of the individuals were stage III in 0.31-0.40 class in and no individual was in stage I within mentioned ranged. Thus, the critical values of CH/ICW for maturation were estimated to be 0.31 in S. olivacea.
Estimation of size at 50% maturity: Probit analysis of the abdomen-width
data resulted in an M50 value of ICW 101 mm (Fig. 5).
This value represents the body size at which 50% of the males are assumed to
reach sexual maturity.
||Logistic fitted curve to the proportion of mature Scylla
olivacea males in Pak Phanang mangrove swamps at each internal carapace
width class (size class = 10 mm)
In another model, the logistic curve fitting with the equation of Koolkalya
et al. (2006) it is noticed that 50% of individuals attained sexual
maturity at the size of about 104 mm (Fig. 6). So, the mean
size of the above two mathematical analysis indicate that 50% individuals reached
sexual maturity in 103 mm ICW in the Pak Phanang mangrove swamps.
Possibility of external morphological observation for maturity: In the present
study there were no clear mating scars noticed and hence the estimate of functional
maturity is vague. Knuckey (1996) found less than a
third of all adult crabs are scarred and pointed out that there would be no
evidence that every mated crabs developed scars and mating scars lost during
molt. Thus the absence of scars does not necessarily mean that a crab has never
mated. In the present study, the size-distribution ranged 60-130 mm ICW and
98% of individuals were less than 110 mm ICW. Whereas, 125 mm ICW was the minimum
size recorded of scarred crabs in Australia (Knuckey, 1996).
Though Perrine (1978) noted that the majority of males
in Ponape only mate after they have attained a size of 138 mm ICW, smaller scarred
crabs noticed in Asia (Ong, 1966). Thus, it is questionable
to adopt the absence of the mating scars as the evidence of the virginity of
On the other hand, crabs can produce spermatozoa without mating (Conan
and Comeau, 1986; Robertson and Kruger, 1994). Several
authors have regarded the presence of spermatophores as indication of functional
maturity (Hartnoll, 1969; Paul,
1992), although this relationship is debated in other species where morphological
development seems to be an important determinant of functional maturity (Comeau
and Conan, 1992; Sainte-Marie et al., 1995;
Knuckey, 1996). Thus, in the present study, maturity
estimation of male mud crab was tried with the pattern of allometric relationship
as well as presence of spermatozoa.
Although all allometric variables showed discontinuity in relative growth associated
with sexual maturity, propodus length and chela height showed a clear sharply
increment in its relative growth. Although, the ratio of chela height to ICW
is commonly used to identify maturity stages in male brachyurans (Hartnoll,
1974; Somerton, 1980; Knuckey,
1996), other parameters like PL, CH can also be used to indicate the sexual
maturity of S. olivacea. This sexual character in present study also
showed different growth rates before and after sexual maturity, therefore indicating
the end of the immature phase and the beginning of the adult phase such as in
majo r crustaceans (Hartnoll, 1978).
Gonad development: Histological examination on male gonad development
is scare in case of crustacean and particularly on Scylla spp. Robertson
and Kruger (1994) described the presence of spermatophores in Anterior Vas
Deferens (AVD) in S. serrata but did not describe details on the development
stages. Sainte-Marie and Sainte-Marie (1999) describe
the formation and development of spermatophores in snow crab (Chionoecetes
oplilio). Spermatophore formation has also been studied for a number of
crustaceans using light microscopy, including the crab species; Scylla serrata
(Uma and Subramoniam, 1979), Callinectus sapidus
(Cronin, 1947; Johnson, 1980),
C. opilio (Beninger et al., 1988),
Portunus pelagicus (El-Sherief, 1991) and Lithodes
maja (Tudge et al., 1998).
In the present study, three gonad development stages observed by histological
microscopic observations and appear to be equivalent to those (De
Lestang et al., 2003) in portunid crab (Viau
et al., 2006) in anomuran crab and the first three of the five stages
defined by (Leal et al., 2008) in stone crab.
The stage I and II defined as the males with undifferentiated vas deferens and
males with differentiated vas deferens but no spermatophores. The final stage
characterized as males with prominent and convoluted vas deferens containing
spermatophores. There was no spent or postovulatory stage in both studied species.
Therefore it was not clear whether male crabs are multiple breeders or not which
found in other crustacean (Leal et al., 2008).
However, as female mud crab showed continuous multiple breeds and they stored
sperm at the first time of mating and used that for subsequent breeding (Robertson
and Kruger, 1994; Onyango, 2002; Moser
et al., 2005) male probably also have multiple breed patterns. In
the gonad development stages, the rarity of stage III could be due to a short
duration of existence and probably turned back to stage I.
Legal size for management: In fishery management, minimum legal size
limit is usually determined based on size at maturity, allowing individuals
to mate at least once after reaching maturity before they are large enough to
harvest in order to protect reproductive potential of the stocks (Donaldson
and Donaldson, 1992; Stevens et al., 1993).
The 50% maturity size is the common minimum legal size used in many open water
mud crab fisheries but exclusively for female crab (Brown,
1993; Machintosh et al., 1993; Robertson
and Kruger 1994; Overton and Macintosh, 2002). In
addition (Overton and Macintosh, 2002) emphasized on
the account of male in maturity estimation. In the present study, though maturity
started at the size of about 90 mm ICW, the two mathematical models showed 50%
maturity was 103 mm ICW. Although each method has its limitations and the small
sample size in the present study, their close agreements in both aspects of
maturity make the results credible. Thus, to conserve mature stock in Pak Phanang
mangrove swamps, an effective minimum legal size of capture for male S. olivacea
would be >100 mm ICW. The same size limit also proposed for the female
S. olivacea in the same area (Islam et al.,
2010) which indicates maturity size does not vary widely with the sexes
of S. olivacea. Although, maturity size did not show much difference
in sexes in S. olivacea, there could be in case of other species as the
paucity of information. Thus, It is necessary to investigate reproductive traits
and maturity size in both sexes of other Scylla species in the study
area, because Overton and Macintosh (2002) suggested
that the legal size of capture for mud crab should be species-specific due to
difference in their maturity size.
The present study described details about the gonad development stages of male
mud crab, Scylla olivacea. The study revealed that 80% of the captured
population was under immature stage which indicates the great threat to the
sustainability of the population. Thus, present result suggested that the minimum
legal size of male mud crab capture should be >100 mm ICW. For indication
of more specific legal size limitation, it is needed to further research on
the other co-existence Scylla species of the locality.
The authors thank to Dr. Toyoji Kaneko, Department of Aquatic Bioscience, The University of Tokyo, for his kind support and guideline for the histological study. The authors also wish to thank Mr. Oo, Mr. Chouvanan and particularly to Yasmin Mostari for assistance with crab sampling and measurement.
1: Beninger, P.G., R.W. Elner, T.P. Foyle and P.H. Odense, 1988. Functional anatomy of the male reproductive system and the female spermatheca in the snow crab Chionoecetes opilio (O. Fabricius) (Decapoda, Majidae) and a hypothesis of fertilization. J. Crustacean Biol., 8: 322-332.
Direct Link |
2: Boromthanarath, S., S. Cobb and V. Lee, 1991. Coastal management in Pak phanang: A historical perspective of the resources and Issues. Hat Yai, Thailand: Coastal Resources Institute, Prince of Songkla University, p: 16-21.
3: Brown, I.W., 1993. Mangrove Crabs. In: Nearshore Marine Resources of the South Pacific, Wright, A. and L. Hill (Eds.). International Centre for Ocean Development, Canada, pp: 609-642
4: Castilho, G.G., A. Ostrensky, M.R. Pie and W.A. Boeger, 2008. Morphology and histology of the male reproductive system of the mangrove land crab Ucides cordatus (L.) (Crustacea, Brachyura, Ocypodidae). Acta Zool., 161: 157-161.
CrossRef | Direct Link |
5: Comeau, M. and G.Y. Conan, 1992. Morphometry and gonad maturity of male snow crab Chionoecetes opilio. Can. J. Fish. Aquat. Sci., 49: 2460-2468.
6: Conan, G.Y. and M. Comeau, 1986. Functional maturity and terminal molt of male snow crab, Chionoecetes opilio. Can. J. Fish. Aquat. Sci., 43: 1710-1719.
7: Conan, G.Y., M. Comeau and M. Moriyasu, 2001. Are morphometrical approaches appropriate to establish size at maturity for male american lobster Homarus mericanus?. J. Crustacean Biol., 21: 937-947.
8: Cronin, L.E., 1947. Anatomy and histology of the male reproductive system of Callinectes sapidus (Rathbun). J. Morphol., 81: 209-239.
9: Donaldson, W.E. and W.K. Donaldson, 1992. A review of the history and justification for size limits in Alaskan king, tanner and snow crab fisheries. Alaska Department of Fish and Game, Division of Commercial Fisheries, Fisheries Research Bulletin No. 92-02, pp: 1-33
10: El-Sherief, S.S., 1991. Fine structure of the sper and spermatophores of Portunus pelagicus (L.) (Decapoda, Brachyura). Crustaceana, 61: 171-179.
Direct Link |
11: Goshima, S., M. Kanazawa, K. Yoshino and S. Wada, 2000. Maturity in male stone crab Hapalogaster dentate (Anomura, Lithodidae) and its application for fishery management. J. Crustacean Biol., 20: 641-646.
Direct Link |
12: Haefner, P.A., 1990. Morphometry and size at maturity of Callinectes ornatus (Brachyura, Portunidae) in Bermuda. Bull. Mar. Sci., 46: 272-286.
13: Hartnoll, R.G., 1969. Mating in the brachyura. Crustaceana, 16: 161-181.
Direct Link |
14: Hartnoll, R.G., 1974. Variation in growth pattern between some secondary characters in crabs (Decapoda Brachyura). Crustaceana, 27: 131-136.
Direct Link |
15: Hartnoll, R.G., 1978. The determination of relative growth in crustacea. Crustaceana, 34: 281-293.
Direct Link |
16: Hill, B.J., 1975. Abundance, breeding and growth of the crab Scylla serrata in two South African estuaries. Mar. Biol., 32: 119-126.
17: Islam, M.S., K. Kodama and H. Kurokura, 2010. Ovarian development and size at maturity of the mud crab Scylla olivacea in Pak Phanang mangrove swamps, Thailand, Mar. Biol. Res., 4: 503-510.
18: Johnson, P.T., 1980. Histology of the Blue Crab, Callinectes Sapidus. A Model for the Decapoda. Praeger Publishers, CBS Educational and Professional Publishing, New York, USA., Pages: 440
19: Koolkalya, S., T. Thapanand, S. Tunkijjanujij, V. Havanont and T. Jutagate, 2006. Aspects in spawning biology and migration of the mud crab Scylla olivacea in the Andaman Sea, Thailand. Fish. Manage. Ecol., 13: 391-397.
20: Knuckey, I.A., 1996. Maturity in male mud crabs, Scylla serrata and the use of mating scars as a functional indicator. J. Crustacean Biol., 16: 487-495.
Direct Link |
21: Krouse, J.S., 1973. Maturity, sex ratio and size composition of the natural population of American lobster, Homarus americanus, along the maine coast. Fish B-Natl. Oceanic Atmos. Administration, 71: 165-173.
22: Lavina, A.F., 1980. Notes on the Biology and Aquaculture of Scylla serrata (F.) de Haan. In: Aquabusiness Project Development and Management, Diliman, U.P. and T. Iloilo (Eds.). Vol. 2. Department of Aquaculture, South-East Asian Fisheries Development Center, Philippines, pp: 1-19
23: Leal, G.A., J.B. Dima, F.G. Dellatorre and P.J. Baron, 2008. Schedule of reproductive events and maturity at size of the patagonian stone crab, Platyxanthus patagonicus (Brachyura, Platyxanthidae). J. Crustacean Biol., 28: 262-269.
CrossRef | Direct Link |
24: De Lestang, S., N.G. Hall and I.C. Potter, 2003. Reproductive biology of the blue swimmer crab (Portunus pelagicus, Decapoda: Portunidae) in five bodies of water on the West coast of Australia. Fish. Bull., 101: 745-757.
Direct Link |
25: Machintosh, D.J., C. Thongkum, K. Swamy, C. Cheewasedtham and N. Paphavisit, 1993. Brood stock management and the potential to improve the exploitation of mangrove crabs, Scylla serrata (Forskal), through pond fattening in Ranong, Thailand. Aquacul. Res., 24: 261-269.
26: Mikhaylyuk, A.N., 1985. Use of probit analysis for studying the dependence of maturation on body length of fishes. J. Ichthyol., 25: 61-65.
27: Moser, S., D. Macintosh, S. Laoprasert and N. Tongdee, 2005. Population ecology of the mud crab Scylla olivacea: A study in the Ranong mangrove ecosystem, Thailand, with emphasis on juvenile recruitment and mortality. Fish. Res., 71: 27-41.
28: Mura, M., F. Orru and A. Cau, 2005. Size at sexual maturity of the spidder crab Anamathia rissoana (Decapoda: Majoidea) from the Sardinian Sea. J. Crustacean Biol., 25: 110-115.
Direct Link |
29: Ong, K.S., 1966. Observations on the post-larval life history of Scylla serrata Forskal, reared in the laboratory. Malays. Agri. J., 45: 429-443.
30: Onyango, S.D., 2002. The breeding cycle of Scylla serrata (Forskal, 1755) at Ramisi River estuary, Kenya. Wetl. Ecol. Manag., 109: 257-263.
Direct Link |
31: Overton, J.L. and D.J. Macintosh, 2002. Estimated size at sexual maturity for female mud crabs (genus Scylla) from two sympatric species within Ban Don Bay, Thailand. J. Crust. Biol., 22: 790-797.
Direct Link |
32: Paul, A.J., 1992. A review of size at maturity in male Tanner (Chionoecetes bairdi) and king (Paralithodes camtschaticus) crabs and the methods used to determine maturity. Am. Zool., 32: 534-540.
CrossRef | Direct Link |
33: Perrine, D., 1978. The mangrove crab (Scylla serrata) on Ponape. Marine Resources Division, Ponape, East Caroline Islands, Trust Territory of the Pacific Islands.
34: Prasad, P.N. and B. Neelakantan, 1990. Size at maturity in the male crab Scylla serrata as determined by chela allometry and gonad condition. Fish. Tech., 27: 25-29.
35: Robertson, W.D. and A. Kruger, 1994. Size at maturity, mating and spawning in the Portunid crab Scylla serrata (Forskal) in Natal, South Africa. Estuarine Coastal Shelf Sci., 39: 185-200.
CrossRef | Direct Link |
36: Sainte-Marie, B., S. Raymond and J.C. Brethes, 1995. Growth and maturation of the benthic stages of male snow crab, Chionoecetes opilio (Brachyura: Majidae). Can. J. Fish. Aquatic Sci., 52: 903-924.
37: Sainte-Marie, G. and B. Sainte-Marie, 1999. Reproductive products in the adult snow crab (Chionoecetes opilio). I. Observations ons spermatogenesis and spermathophore formation in the vas deferens. Can. J. Zool., 77: 440-450.
38: Somerton, D.A., 1980. A computer technique for estimating the size of sexual maturity in crabs. Can. J. Fish. Aquatic Sci., 37: 1488-1494.
CrossRef | Direct Link |
39: Somerton, D.A. and R.A. Macintosh, 1983. The size at sexual maturity of the blue king crab, Paralithodes platypus, in Alaska. Fish. Bull. (US), 81: 621-628.
40: Stevens, B.G., W.E. Donaldson, J.A. Haaga and J.E. Munk, 1993. Morphometry and maturity of paired Tannercrabs, Chionoecetes bairdi, from shallow- and deepwater environments. Can. J. Fish. Aquat. Sci., 50: 1504-1516.
Direct Link |
41: Thampanya, U., J.E. Vermaat and C.M. Duarte, 2002. Colonization success of common Thai mangrove species as a function of shelter from water movement. Mar. Ecol. Prog. Ser., 237: 111-120.
42: Tudge, C.C., B.G.M. Jamieson, L. Sandberg and C. Erseus, 1998. Ultrastructure of the mature spermatozoon of the king crab Lithodes maja (Lithodidae, Anomura, Decapoda): Further confirmation of a lithodid-pagurid relationship. Invertebrate Biol., 117: 57-66.
Direct Link |
43: Uma, K. and T. Subramoniam, 1979. Histochemical characteristics of spermatophore layers of Scylla serrata (Forskal) (Decapoda: Portunidae). Int. J. Inver. Rep. Dev., 1: 31-40.
44: Van Engel, W.A., 1990. Development of the reproductively functional form in the male blue crab, Callinectes Sapidus. Bull. Mar. Sci., 46: 13-22.
Direct Link |
45: Viau, V.E., L.S.L. Greco, G. Bond-Buckup and E.M. Rodriguez, 2006. Size at the onset of sexual maturity in the anomuran crab, Aegla uruguayana (Aeglidae). Acta Zool., 87: 253-264.