ON TYPES OF SEXUAL MATURITY IN BRACHYURANS, WITH SPECIAL REFERENCE TO SIZE AT THE ONSET OF SEXUAL MATURITY.
With approximately more than 6,500 species spread across 98 families within this infraorder, brachyurans are the most numerous group of decapod crustaceans (Tsang et al. 2014). They can be found in almost all ecosystems--freshwater, marine, and terrestrial habitats (Ng et al. 2008). All brachyurans share similar morphological characteristics, including having a short "tail" that is eventually folded under the thorax and becomes the abdomen segment, a body protected by a thick calcium carbonate exoskeleton (Ng et al. 2008), and a pair of pincers that functions as both "ornaments and armaments" (Berglund et al. 1996).
Based on the position of gonopores, Brachyura Latreille, 1802 is further divided into five sections, i.e., Dromiacea De Haan, 1833; Raninoidea De Haan, 1839; Cyclodorippoidea Ortmann, 1892; Heterotremata Guinot, 1977; and Thoracotremata Guinot, 1977. The gonopores of crabs of section Dromiacea, Raninoidea, and Cyclodorippoidea are located at the third leg in females and fifth leg in males (Ahyong et al. 2007). The gonopores of heterotreme crabs are at different locations based on sex, i.e., on the sternum in females and legs in males (de Grave et al. 2009). For thoracotremes, the gonopores of both sexes are found on their sternum instead of legs (de Grave et al. 2009). Previously, Dromiacea, Raninoidea, and Cyclodorippoidea were collectively termed as Podotremata (Guinot 1977) until Ahyong et al. (2007) split them up based on phylogenetic analysis of their nuclear 18S gene sequences. These three sections exhibit various ancestral characteristics and are regarded as primitive whereas Heterotremata and Thoracotremata, being more derived and advanced, are considered as Eubrachyura (Tsang et al. 2014).
Growth is often expressed and measured by the increase in size, volume, or weight over time. In contrast to most organisms with endoskeleton and growth continuously, the growth in crustaceans including brachyurans is brief and discontinuous as growth only occurs during molting (shedding of old exoskeleton) due to the presence of rigid and inextensible exoskeleton (Hartnoll 1982).
Like other crustaceans, the reproductive process of a brachyuran is governed by a series of changes, morphologically and physiologically. This process will only be initiated once the crab reaches sexual maturity and is ready to reproduce. It starts with gametogenesis, i.e., the proliferation, differentiation, and maturation of primary germ cells into mature gametes, followed by exhibition of reproductive mating behavior, successful copulation, fertilization of eggs, release of eggs from the ovary (spawning), incubation of embryos, and the hatching of larvae from eggs (Sastry 1983, Castiglioni et al. 2007). Larvae of brachyurans (termed as zoeae) go through several metamorphoses in estuarine or coastal waters until attaining megalopa and crablet stages before returning to their respective natural habitats (Cuesta & Anger 2005). After that, they will molt and develop until they attain sexual maturity, reproduce, and the life cycle is repeated.
In general, sexual maturity in crabs and other crustaceans are based on three criteria: morphometric (based on the change in morphometric relationships of secondary sexual characters), physiological (based on gonadal maturation), and functional (based on the size at which they are able to mate) (Pollock 1995, Lopez Greco & Rodriguez 1999). However, because of various internal (e.g., genetic selection) (Campbell & Eagles 1983, Linnane et al. 2008, Zheng 2008) and external governing factors (e.g., food availability and variation in physical parameters including latitudinal difference and temperature) (Wenner et al. 1974, Lizarraga-Cubedo et al. 2003, Litulo 2005a, Zheng 2008), the relationship between the three maturation criteria is complex and do not always synchronize with one another.
Thus, this review explores the different types of sexual maturity found in brachyurans. In addition, data on size at the onset of sexual maturity (SOM) of brachyurans around the globe are compiled and highlighted as well. A thorough understanding of sexual maturation and how to estimate the size at which it occurs in brachyurans have important implications for the conservation and management of brachyuran populations in their natural habitats.
The attainment of sexual maturity represents the transformation of immature individuals into sexually mature adults, and it involves distinct changes in brachyurans' external morphology and internal physiology (Pinheiro & Fransozo 1998). These observable and quantifiable changes allow us to determine different types of maturity based on different maturation characteristics.
Morphometric maturity is often characterized by a change in relative growth of certain body dimensions in brachyurans during sexual maturity. Sexual dimorphism is exhibited by adult brachyuran crabs (Clayton 1990, McLay & Van Den Brink 2009). Some of these ontogenetic variations include the increase in chelae size (length, height, and width) in males and increase in abdomen width in females (Hartnoll 1974, Knuckey 1996, Waiho et al. 2016a, 2016b). These abrupt changes occur once crabs reach maturity and have obvious functional significance (e.g., the growth of large chelae in mature males is important for combat, display, and courtship purposes; the exponential increase in abdomen width of mature females enables it to store and protect its eggs after spawning) (Hartnoll 1974, Hall et al. 2006, Ribeiro et al. 2013, Waiho et al. 2016a). In addition to secondary sexual characters, researchers also found that different body parts of brachyurans (e.g.. locomotor appendages and pleopods) showed significant differences in allometric growth as well after attaining sexual maturity (Clayton 1990, Ribeiro et al. 2013, Waiho et al. 2017).
The estimation of size at morphometric maturity generally involves the use and analysis of relationships between secondary sexual characters and a reference somatic character [e.g., carapace width (CW)], provided that the secondary sexual characters grow at different rates during immature and mature stages (Lemc 2005). The growth pattern between selected body dimensions relative to body size can be either isometric, positively or negatively allometric. In addition, the allometric relationships between different morphological characters with a primary character are often used by researchers to analyze variation in growth and health between and within different populations (Ribeiro et al. 2013). However, it is important to note that the prediction of SOM based on allometric growth is not applicable in all situations but greatly depend on the species studied, characters or variables measured, and methodologies used to interpret and analyze the morphometric data (Hartnoll 1974, Clayton 1990, Knuckey 1996, Waiho et al. 2016b).
In contrast to morphometric maturity, physiological maturity relies on the characterization of gonad development, especially the enlargement of gonad reproductive system in males and the expansion of ovarian mass with apparent color changes in females after reaching maturity (Hartnoll 1969, Robertson & Kruger 1994, Knuckey 1996). Thus, physiological maturity is defined as the ability of an individual to produce gametes (Corgos & Freire 2006).
Male Reproductive System and Gonadal Maturation
In general, the male reproductive system in brachyurans is bilateral and H-shaped. Paired testes are located anteriorly, followed by vas deferens (Krol et al. 1992, Waiho et al. 2017). The vas deferens of brachyurans can be further divided into three distinct regions: anterior vas deferens (AVD), median vas deferens (MVD), and posterior vas deferens (PVD) (Simeo et al. 2009). Spermatozoa are produced in testes and released into AVD, where spermatozoa are packed into packets of spermatophores. The produced spermatophores are then transferred and stored in MVD. Seminal fluids are also secreted in this region. The storage of seminal fluids and spermatophores in MVD gave rise to its prominent creamy white coloration. PVD in brachyuran crabs are often longer in length and bulkier in size compared with AVD and MVD and provides storage for spermatophores as well in some species (Zara et al. 2012, Waiho et al. 2017).
There are generally three male gonadal maturation stages applied in most brachyuran species, namely immature, maturing (intermediate), and mature (developed) (Shinozaki-Mendes et al. 2012, Soundarapandian et al. 2013). These three stages of gonadal maturation are characterized based on the physical morphology and/or internal histology of the male reproductive system (Table 1).
However, not all brachyuran crabs adhere to this three-stage gonadal maturation classification. For example, the male gonadal development of Uca burgersi (Holthuis, 1967) (Brachyura: Ocypodidae) (Benetti et al. 2007), Callinectes danae (Smith, 1869) (Brachyura: Portunidae) (Marochi et al. 2013), and Goniopsis cruentata (Latreille, 1803) (Brachyura: Grapsidae) (Cobo & Fransozo 2005) is classified into four main stages, namely immature (nondifferentiated gonads), rudimentary (filamentous deferent vessels and colorless), developing (visible gonad, vas deferens can be divided into two regions, deferent vessels start to reel and occupy body cavity, with either translucent or white coloration), and developed (enlarged and threaded gonads, occupying at least a quarter of the thoracic cavity, vas deferens clearly differentiated into three distinct regions and is milky-white in color). Both immature and rudimentary stages are considered as inactive in reproductive condition whereas crabs in the development and developed stages are considered as sexually active (Benetti et al. 2007). Apart from that, Pinheiro and Fransozo (1998) and Litulo (2005a) divided the male gonadal development of sesarmid crab Neosarmatium meinerti (de Man, 1887) (Brachyura: Grapsidae) and portunid crab Arenaeus cribrarius (Lamarck, 1818) (Brachyura: Portunidae) into five stages respectively, i.e., stage I--gonads not visible, stage II--vas deferens is thin, filamentous, and only visible under magnification, stage III--vas deferens is clearly visible and brown or transparent in color, stage IV--testes are partially convoluted and have white coloration, and stage V--testes are enlarged and gonad occupies all cephalothoracic cavity with white coloration. In addition, unlike previous classifications, the gonad maturation stages of Platyxanthus patagonicus (A. Milne-Edwards, 1879) (Brachyura: Platyxanthidae) are divided into five stages, with stage V being termed as "recovering" (white and swollen testes but vas deferens are lax and do not contain spermatophores), on top of the other four common stages (i.e., stage I--immature, stage II--maturing, stage III--mature, and stage IV--spent) (Leal et al. 2008).
In summary, the presence of spermatophores in vas deferens and/or the external morphology of gonad reproductive system (enlarged, milky white, and occupied most of the body cavity) are commonly used as a yardstick to determine physiological maturity in males (Table 1).
Female Reproductive System and Gonadal Maturation
The female reproductive system in brachyurans consists of two main components, i.e., spermathecae or seminal receptacles, and ovaries, with oviducts as the connector (Becker et al. 2011). Spermathecae or seminal receptacles act as a sperm storage organ in females and connects directly with the gonopores opening on the sixth thoracic sternum (Babu et al. 1989). The maturation of the female reproductive system and the production of mature gametes (oogenesis) are closely linked to vitellogenesis--a process of yolk deposition of the oocytes in the ovaries (Rani & Subramoniam 1997).
Based on the gross morphology of ovaries and histological appearance of ovarian cells, ovarian maturation of brachyurans can be divided into five main stages, namely immature (I), early maturing (II), late maturing (III), fully mature (IV), and spent (V) (Quinitio et al. 2007, Ravi et al. 2012). However, the staging descriptions and names differ between researchers as detailed out in Table 2.
It is important to note that the five stages of ovarian maturation are not definitive. The female terrestrial crab Sesarma rectum (Randall. 1840) (Brachyura: Sesarmidae) exhibits four ovarian maturation stages [i.e., stage I (immature): ovary not differentiated, stage II (rudimentary): narrow pale cream or yellow filamentous ovaries, stage III (in development): small, bright orange ovaries with visible oocytes, and stage IV (developed): ovaries in advanced stage of maturation and occupying more space in the cephalothorax] as described by Leme (2005). The ovarian maturation stages of portunid crabs Callinectes danae and Callinectes ornatus (Ordway, 1863) were divided into four stages as well but with stage I, II, III, and IV being classified as "immature," "developing," "ripe," and "spent," respectively (Keunecke et al. 2009). Pinheiro and Fransozo (1998) classified the ovarian maturation stages of Arenaeus cribrarius into three main stages (i.e., immature, developing, and developed), and each stage was subdivided into two substages, resulting in a total of six substages (females > substage III were considered as mature). The four-stage ovarian maturation of portunids Scylla olivacea (Herbst, 1796) (Ikhwanuddin et al. 2014) and Portunus pelagicus (Linnaeus, 1758) (Ikhwanuddin et al. 2012) was apparent with the transition of ovarian colors, i.e., stage I (immature): translucent and thread-like ovary, stage II (early maturing): ovary yellow in color and increase in size, stage III (late maturing): ovary yellowish to light orange, and stage IV (mature): ovary is dark orange or red, with visible individual eggs.
Functional maturity encompasses a broader spectrum than physiological maturity as functional maturity includes the ability to mate successfully, and to be able to do that, an organism must be mature physiologically and morphometrically (Conan & Comeau 1986). The onset of being able to mate and reproduce (functional maturity) is of prime importance to the monitoring of a population's reproductive capacity in their natural habitats (Knuckey 1996). However, functional maturity is difficult to quantify as most of the time, no physical evidence of mating can be observed after the copulation process. Various methods, including laboratory and aquarium observations (Viau et al. 2006), and in situ observation of the crab copulation processes have been used to determine functional maturity. However, these methods are costly and of limited applicability (Paul 1992).
Alternatively, functional maturity can be determined by the presence of scars on the sternum or forward walking legs in brachyurans (Robertson & Kruger 1994). These scars are formed during the precopulatory embrace when the male sternum and/or forward walking legs are constantly abrading with the female carapace (Robertson & Kruger 1994, Knuckey 1996, Ikhwanuddin et al. 2011). It is postulated by Knuckey (1996) that chitinoclastic bacteria are responsible for the formation of these abrasion scars once the exoskeletons are scraped off because of frequent abrading, exposing the inner layer of the shell, similar to the "burned spot" disease in other crustaceans (Sandifer & Eldridge 1974). The attack from chitinoclastic bacteria resulted in clear brown markings on the healed exoskeleton which only disappear after subsequent molting. Therefore, the presence of abrasion scars on males and depressions on females directly indicates that they are functionally matured and have mated. This serves as an important characteristic for researchers to determine functional maturity in males with ease and without the need for sophisticated instruments and methodologies (Knuckey 1996, Ikhwanuddin et al. 2011). It is also worthy to mention that the absence of mating scars on males or mating depressions on females does not necessarily indicate that they are not functionally mature. This is supported by Knuckey (1996) where he found that more than two-thirds of adult crabs do not have mating scars, postulating that either they lost the scars after molting or did not develop any at all. However, Waiho et al. (2016a) investigated the abdomen looseness of crabs [Scylla spp. (De Haan, 1833)] and found out that the abdomen of an immature male is tightly attached to the thoracic sternum whereas that of a mature male is loose and can be easily flipped open with the aid of a dissecting needle. This phenomenon was also reported in the blue crab Callinectes sapidus, in which the abdomen of an immature male is tightly sealed to the ventral surface of the abdomen whereas that of a mature male remains free and is held together by a press-button abdominal holding system (Van Engel 1958). The locking mechanism may be regarded as an indicator of sex, puberty molt, and age and may be found in almost all brachyuran species. It is worthy to note that the structure, however, differs between primitive and higher Brachyura, in that the former podotrematous brachyurans (Dromiidae and Homolidae) involve the coxae of thoracopods whereas the latter possess a press-button structure (a prominence on the fifth sternite and a socket on sternites 4-6 depending on families) (see review by Guinot & Bouchard 1998).
Identification of functional maturity in female brachyurans is more straightforward than that in their male counterparts. A female is functionally mature after the pubertal molt, which is often accompanied by an increase in width, change of shape (more globular), and darkened color of its abdomen (Hartnoll 1974, Ribeiro et al. 2013). After a successful copulation, females exhibit several characteristics that are easily observable, i.e., the release of eggs onto the abdomen (spawning) and the attachment of fertilized eggs to the abdomen's pleopods (ovigerous) (Waiho et al. 2015, Azra & Ikhwanuddin 2016). These features are frequently used by researchers to classify females as functionally mature (Viau et al. 2006, Grabowski et al. 2013). Other features that imply mating success are the presence of sperm plugs in the female's oviduct or spermatophores in its spermatheca/seminal receptacle (Ungfors 2007, Fazhan et al. 2017a). Both sperm plugs and the storage of spermatophores in spermathecae or seminal receptacles are mating strategies adopted by brachyurans to ensure paternity without the need of active mate guarding while waiting for the oocytes of females to fully mature (Dunham & Rudolf 2009).
SIZE AT THE SOM: DEFINITION, IMPLICATION, AND APPLICATION
Onset of sexual maturity is one of the most important biological characters in the life cycle of crustaceans, including brachyurans. It is considered as a crucial determining factor of brachyurans' reproductive output and the growth rate of a population (Hines 1989) as growth and SOM influence the reproductive dynamics of a population and subsequently affect the population recruitment process in a particular geographical region (Cobb & Phillips 1980). Throughout time, various methods have been used to estimate this important value. Attempted methodologies in the estimation of SOM generally revolve around two maturation-related processes, i.e., morphometric changes at the point of maturity (Corgos & Freire 2006) and biological changes (physiological and functional changes) (Litulo 2005b, Corgos & Freire 2006).
The SOM in brachyurans is coupled by a series of transformations which eventually transform immature individuals into mature adults that are capable of reproducing and propagating (Hartnoll 1969). In general, SOM is defined based on three main criteria: allometric variation (via morphometric analyses), gonadal maturation (via histological analyses), and sexual functionality after attaining sexual maturity (via the presence of mating scars in males and the presence of spermatophores/sperm plug in spermathecae/seminal receptacles of females) (Viau et al. 2006).
In the field of fisheries, an estimated CW value at which 50% of the sampled brachyuran population reached sexual maturity is termed as [CW.sub.50] [occasionally, the carapace length (CL) is used instead of CW] (Quiles et al. 2001) and is frequently used to define the reproductive state in crustaceans (Corgos & Freire 2006). Put differently, [CW.sub.50] is the CW at which a randomly selected sample has a 0.5 probability of being mature and is often being referred to as the estimated SOM (Somerton 1980). This value is often used to predict and monitor the health and population dynamics of selected populations through time as well as the detrimental effect of fishing pressure and ecological habitat destruction (Haig et al. 2015a). Overfishing is postulated to reduce SOM (Pollock 1995), as documented in several commercially exploited fish populations (Trippel 1995). In fact, concerns about how overfishing of some economically important brachyuran species (e.g., mud crab genus Scylla) might affect the sustainability of the local stock population have raised the need for probing into the sizes at which crabs attain sexual maturity (Ikhwanuddin et al. 2011, Waiho et al. 2016b).
In addition, [CW.sub.50] is also commonly used as the standard for legislation of minimum landing size (MLS) for various commercially important brachyurans around the world. For example, based on the [CW.sub.50], the MLS of edible crab Cancer pagurus (Linnaeus, 1758) (Brachyura: Cancridae) is recommended at 140 mm CW for both sexes along the strait of Skagerrak and Kattegat (Ungfors 2007) but 130 mm between the River Tyne and North East Lincolnshire in the United Kingdom (Inshore Fisheries and Conservation Authority 2015). minimum landing size for mud crabs Scylla spp. are presently being imposed in Australia with an MLS of 150 mm CW in Queensland (Le Vay 2001), 85 mm in New South Wales (State of New South Wales through Industry and Investment NSW 2010), and in South Africa with an MLS of 114-115 mm CW (Robertson & Kruger 1994). Similarly, the MLS enforced upon blue swimming crab Portunus pelagicus differs between countries, with an MLS in Indonesia being set at 100 mm CW (Zairion et al. 2015a) and in Australia at 127 mm CW (Potter et al. 1983). This is utterly important to avoid overfishing of brachyuran crabs in the wild and to ensure that crabs are able to at least mate and reproduce once before being captured (Ungfors 2007).
SYNCHRONIZATION BETWEEN TYPES OF SEXUAL MATURITY
Not all forms of maturities (physiological, morphometrical, and functional maturity) synchronize perfectly and occur exactly at the same time. Some crab species, such as the snow crabs Chionoecetes opilio (O. Fabricius, 1788) (Brachyura: Oregoniidae) are known to mature faster physiologically rather than morphometrically (Filina 2011). The physiologically mature but still morphometrically immature crabs, however, are unlikely to be able to mate (Filina 2011). There are species, however, that showed more synchronized physiological and morphometrical maturity, but even so, it still varies between genders. The male cancrid crabs Cancer pagurus were found to exhibit rather synchronized maturity, with the [CW.sub.50] of physiological maturity based on sperm production (117 mm) which is almost similar to the [CW.sub.50] of morphometric maturity based on chelae size (122 mm); the female C. pagurus, however, showed a higher [CW.sub.50] of physiological maturity based on ovarian maturation (132 mm) compared with the [CW.sub.50] of functional maturity based on the presence of sperm (107 mm) or sperm plug (118 mm) and the [CW.sub.50] of morphometric maturity based on abdominal width allometry (104 mm) (Ungfors 2007). The ability to store sperms after copulation in brachyuran females implies that females do not have to be physiologically mature (in terms of ovarian maturation stages) to be able to copulate. In summary, the physiological capacity to produce viable sperms and oocytes (physiological maturity) alone is insufficient to define sexual maturity in both male and female brachyurans. They have to be functionally mature as well to allow the copulation process to occur.
Materials and Methods
The maturity data (n = 211) of 133 brachyuran stocks were collected around the globe from peer-reviewed published sources for the period 1971-2015 (Table 3). The data were categorized based on different types of maturity (morphometric, physiological, and functional maturities), and brachyurans were further classified into their respective families and species. Valid species names and authorities were according to the World Register of Marine Species (WoRMS Editorial Board 2017). This review lists all data if more than one type of maturity data was reported from the same crab stock. However, for the quantification of numbers of literature collected based on family in Figure 1 and the sampling methods used in the literature in Figure 2, only data of crab stock (n = 141) instead of all maturity data cases (n = 220) were used to prevent redundant quantification of data for crab obtained from the same study.
In the literature, several forms of measurements/definitions were used to represent sexual maturity, with the most common measurement of using the CW at which 50% of the population reaches maturity--[CW.sub.50]. Occasionally, as provided by the original source, instead of CW, CL was used ([CL.sub.50]). In addition, some researchers used a range of CW or CL of the smallest to the largest mature crab ([CW.sub.mature]) or just the maximum ([CW.sub.max]) or minimum ([CW.sub.min]) CW or CL of the recorded specimens. In all cases, [CW.sub.50], [CL.sub.50], [CW.sub.mature], [CW.sub.max], and [CW.sub.min] were recorded and, when necessary, converted to millimeters.
Different researchers used different methods to determine the [CW.sub.50], including using breakpoint analysis (Overton & Macintosh 2002), probit analysis (Overton & Macintosh 2002). probability plots (plotting proportion of mature specimens over width or length) (Hines 1989), linear regression (transition inflexion point marks the size at maturity) (Ribeiro et al. 2013), or fitting of logistic curves (de Lestang et al. 2003). In this review, maturity data were extracted as provided by the original source, regardless of the statistical estimation methods used.
Additional information such as sex, indicators used to determine sexual maturity, sampling methods, the number of individuals, and country and year of sampling were included, if available (Table 3). Turkey was categorized in Asia continent as classified by the United Nations Statistics Division (United Nations 2017).
For the estimation of the relationship between [CW.sub.50] and [CW.sub.max], data from all cases were logarithmically transformed and plotted, with [CW.sub.50] on the Y axis and [CW.sub.max] on the X axis. In addition, the relationship between [CW.sub.50] and [CW.sub.max] in males and females, and in specific families, was also explored. However, only Portunidae was subjected to this analysis because of the low number of maturity cases (n < 15) in other Brachyuran families. The regression lines of all relationships were tested with analysis of covariance.
Studies of brachyuran SOM were conducted the most in the South America continent (38%, n = 51 stocks). Number of studied brachyuran stocks was high in Europe (18%, n = 24 stocks), followed by Asia (17%, n = 23 stocks) and Australia (12%, n = 16 stocks). Africa and North America contributed maturity data of 11 (8%) and 10 (7%) stocks, respectively. Only one study was reported from the Pacific Ocean (Fig. 3).
When classified according to taxonomic status (family), portunid crabs accounted for the largest number of reported maturity data out of 23 families in all three types of maturity (Fig. 1). Most maturity studies focused on this family as all portunid crabs (n = 82 maturity data) listed in Table 3 are edible and economically important species. Studies about the maturity of crabs from the family Geryonidae Colosi, 1923; Cancridae Latreille, 1802; and Majidae Samouellc, 1819 accounted for 18, 17, and 15 cases, respectively (Fig. 1). Other brachyuran families accounted for reported cases of less than 10 individuals. The least studied family of brachyurans is Dorippidac MacLeay, 1838, with only one maturity data available--Medorippe lanata (Linnaeus, 1767).
Most of the maturity data obtained were estimated based on morphometric maturity (n = 107 cases) (Table 3). Estimates of SOM based on physiological maturity and functional maturity only accounted for approximately half of that of morphometric maturity (n = 55 cases and n = 58 cases, respectively).
Sampling methods were described in all studies except for 26 stocks (Table 3). A total of 24 professional and experimental sampling methods were used during the sampling of brachyurans for the estimation of SOM. Only 31 stocks used a combination of sampling methods in capturing crabs. The most frequently used sampling method was baited trap, followed by hand capture and otter trap (Fig. 2). Trawls and nets (i.e., beach seine, beam trawl, crab net, double-rig net, trawl net, fyke net, gill net, ring net, otter trawl, trammel net, and unspecified trawl) were used most often (41%) for sample collection (Fig. 2). Traps (i.e., baited trap, fence trap, glass box, Neilsen trap, rocklobster trap, and shrimp trap) accounted for 33% usage among researchers. Samples were collected using individual efforts (i.e., baited line, hand capture, hooked pole, scuba diving, and sieve) in 41 stocks and accounted for 25% of the total usage. There were two stocks that obtained brachyuran samples from the fish stomach and one stock that laboratory reared their brachyuran samples from larvae to adulthood.
Size at morphometric maturity
The number of cases that estimated the SOM based on morphometric data was higher in males (n = 65) than females (n = 42). The morphometric relationship of abdomen width with CW was the most used indicator (55%) out of the 14 indicators used in predicting female size at morphometric maturity (Fig. 4). Most of the estimation of size at morphometric maturity used CW (79%) as the primary character for comparison (n = 33 cases). The usage of CL as the primary character accounted for six cases (14%) whereas gonopod length, sixth abdominal segment width, and short carapace width were each used once as primary characters in estimating female brachyurans' size at morphometric maturity (Fig. 4).
A total of 14 indicators were used in the estimation of size at morphometric maturity in male brachyurans. More than half (71%) of the cases used CW as their primary character whereas the remaining cases based their allometric relationship on CL (16 cases), short carapace width (two cases), and one unspecified case (Fig. 4). Approximately 88% of cases (n = 57) used chela propodus dimensions (e.g., length, height, and width) and 15% of cases (n = 10) used gonopod length as their secondary sexual characters to estimate the size at morphometric maturity in male brachyurans.
Size at physiological maturity
A total of 55 cases (22 cases in females and 33 cases in males) estimated the SOM using physiological maturity data (Table 3). Based on the gonad physiological changes that are observable by the naked eye, 91% (n = 20) and 61% (n = 20) of cases in female and male brachyurans relied upon gonad maturation stages in the estimation of size at physiological maturity (Fig. 4).
Another alternative indicator of size at physiological maturity in males is based on the presence of gamete cells (e.g., spermatozoa, spermatids, or spermatophores) in the male reproductive system (i.e.. testes or vas deferens), which accounted for 30% of cases in the estimation of male size at physiological maturity (Fig. 4).
Size at functional maturity
The number of size at functional maturity estimated in males (n = 10) was approximately a fourth of that of females (n = 47) (Table 3). Female ovigerous state is the key indicator in the determination of female size at functional maturity as proven in the current dataset (n = 19 cases). Abdomen morphology was used to determine female size at functional maturity in 17% (n = 8) cases. Five cases of female functional maturity were determined based on the status of their pubertal molt (11%). Other indicators such as the presence of mating depressions, presence of sperm plug, cheliped morphology, and being physically engaged in mating were the least favored methods of functional maturity determination (each with a usage percentage of less than 10%) (Fig. 4). In males, mating scars were used to determine size at functional maturity in two species of portunid crabs [Scylla olivacea and Scylla tranquebarica (Fabricius, 1798) (Ikhwanuddin et al. 2011)] and one geryonid crab [Geryon maritae (Manning & Holthuis, 1981) (Melville-Smith 1987)] (Fig. 4). The usage of cheliped morphology and abdomen morphology to determine male size at functional maturity accounted for two cases each (Fig. 4). Two cases of males were found to be engaged in mating during sample collection whereas two cases of successful fertilization (as implied by egg extrusion in females) of males were also reported.
Figure 2. The usage percentage (%) of sampling methods. BL, baited line; BMT, beam trawl; BS, beach seine; BT, baited trap; CN, crab net; DRN, double-rig net; FN, fyke net; FS, fish stomach; FT, fence trap; GB, glass box; GN, gill net; HC, hand capture; HP, hooked pole; LR, laboratory reared; NLT. Neilsen trap; OT, otter trawl; RN, ring net; RLT, rock-lobster trap; S, sieve; SD, scuba diving; ST, shrimp trap: T, unspecified trawl; TMN, trammel net; and TN. trawl net. LR, FT, NLT, T, FN, RN 4% SD 5% BS 8% TN 8% OT 9% BMT, GN, CN 10% RLT, FS, S, GB, ST, BL, HP, DRN, TMN 11% HC 16% BT 28% Note: Table made from pie chart. Figure 3. Global distribution of the maturity data (%) of brachyurans based on continents. * South America 1 * North America 51 * Asia 13 * Africa 23 * Australia 11 * Europe 16 * Pacific Ocean 24 Note: Table made from pie chart.
Maximum Size and Size at the Onset of Sexual Maturity
Maximum size ([CW.sub.max]) was reported for 74 stocks of brachyurans (Table 3). The smallest brachyuran species reported was Trichodactylus borellianus (Nobili, 1896) from the family Trichodactylidae, with a [CW.sub.max] of 10.4 mm in males (n = 155) and 12.4 mm in females (n = 182). This species was collected monthly (August 2001 to October 2002) from three sites of the Parana alluvial valley, Brazil (i.e., Las Sandias Stream, Aliviador Stream, and Santa Fe River) (Williner et al. 2014). The largest male and female brachyuran species were both from the family Portunidae Rafinesque, 1815, with the male mud crab Scylla serrata (Forskal, 1775), caught at Iriomote Island, Japan, being the largest male ([CW.sub.max] = 193.5 mm) (Ogawa et al. 2011) and Portunus pelagicus from Indonesia being the largest female ([CW.sub.max] = 173.2 mm) reported.
The [CW.sub.50], [CL.sub.50], or observed mature size ([CW.sub.mature]) were reported for all 23 families and 55 species (Table 3). The [CW.sub.50] ranged from 3.6 mm [Hymenosomatidae. male Halicarcinus planatus (Fabricius, 1775)] to 150.7 mm (Portunidae, male Scylla serrata) (Table 3). The mean, median, and range of each brachyuran family are shown in Figure 5. Brachyuran family with the largest mean [CW.sub.50] [+ or -] SE (116.1 [+ or -] 4.6 mm) was Cancridae whereas family Epialtidac MacLeay, 1,838 exhibited the smallest mean [CW.sub.50] [+ or -] SE (9.8 [+ or -] 0.9 mm). Being the family with the most stocks reported (n = 38 stocks), family Portunidae had a CW range of 26.8 mm [female Carcinus aestuarii (Nardo, 1847)] to 150.7 mm (male S. serrata) and a mean [CW.sub.50] [+ or -] SE of 81.8 [+ or -] 12 mm.
A strong positive linear relationship was observed between [CW.sub.50] and [CW.sub.max] across all maturity cases. Similar empirical relationships were found for both sexes and Portunidae (Table 4). When analyzed separately, the slopes of the regression lines of both sexes did not differ significantly from each other (analysis of covariance: F = 2.46. P = 0.12). The two logarithmically transformed regression lines intercepted at a [CW.sub.max] of approximately 20.5 mm, after which the [CW.sub.50] of females was generally larger than that of males of the same [CW.sub.max] (Fig. 6).
The family Portunidae was the most studied family in brachyuran crabs because of their huge species diversity, with 58 recognized genera and subfamilies and 687 species. A large number of maturity studies focused on this family as most portunid crabs (n = 82 maturity data) listed in Table 3 are edible and economically important species, such as portunids from the genus Portunus (Weber, 1795) (Rasheed & Mustaquim 2010, Ikhwanuddin et al. 2012) and Scylla (Baylon 2010, Ikhwanuddin et al. 2011, Waiho et al. 2016a, 2016b, Fazhan et al. 2017b).
With only one available maturity data, the benthic hairy crab Medorippe lanata of the family Dorippidae was the least studied brachyuran family. They can be found at the sea bottom of the Mediterranean shelf and is often the bycatch of dremersal trawling (Rossetti et al. 2006). They are habitually thrown away by trawlers as they are not economically valuable. Coupled with the low number of species (total of nine species) found in this family (de Grave et al. 2009), the scarcity of maturity data available for this family is reasonable.
The preference of estimating the SOM using morphometric data (morphometric maturity) over gonadal development status (physiological maturity) or external maturity/mating indicator (functional maturity) is attributed to its simplicity during data collection and its accuracy in estimating the SOM. Morphometric data used in the estimation of SOM only involve measurements of body dimensions whereas to determine physiological maturity, specimens have to be killed and their internal gonad examined. This is laborious and requires a certain level of expertise in the determination of gonadal development stages in both sexes of brachyuran species studied. Functional maturity is based on the observation of size during mating or any external cues (e.g., mating scars) that might indicate mating occurred. This determination method is the least favorite among researchers because of the difficulty and ambiguity during data collection (Knuckey 1996). The data obtained in these studies could potentially serve as guidelines for the establishment or revision of MLS, and aid in wild stock assessment and monitoring the effect of the fishing pressure exerted on these portunid crabs (Robertson & Kruger 1994, Marochi et al. 2013).
When considering each sampling method individually, baited traps (27%) and hand capture (21%) were used the most (both were used in 10 brachyuran families) compared with other methods. These two methods are predominantly used by fishermen throughout the world to harvest brachyuran crabs and have been proven successful (Gray 1995). Unlike fishes that swim in schools and often occupy the pelagic zone of the ocean, brachyuran crabs prefer the demersal zone of the water column and seldom travel or forage in groups. Hand capturing brachyuran crabs is applicable in freshwater (e.g., streams and shallow rivers) and intertidal zones (e.g., mangrove forests, estuaries, and seashores) where the water level is shallow and accessible by foot (Liu & Li 2000, Flores et al. 2002, Rostant et al. 2008, Diez & Lovrich 2010). Baited traps are more versatile and universal-can be used in all habitats (i. e., terrestrial, freshwater, intertidal, and marine) (Leite et al. 2013, Biscoito et al. 2015, Waiho et al. 2016a, 2016b). For deep-sea harvesting, buoys are attached to baited traps for easy retrieval (Eno et al. 2001). Baited traps are generally deployed and retrieved after a period of time (from a few hours to a day), enabling foraging brachyuran crabs to venture into the deployed baited traps (Eno et al. 2001, Waiho et al. 2015, 2016b). Compared with traps and individual efforts, trawls and nets are seldom species specific and researchers using such methods to collect brachyuran samples were either collecting the bycatch (brachyuran crabs) from fishermen or were a part of a larger research expedition, with brachyuran crabs being one of the target species (Di Beneditto et al. 2010).
The usage of baited traps and the biasness in the estimated SOM of brachyurans were reported recently (Smith et al. 2004). It was found that baited traps were size selective compared with trawls and nets, resulting in the collection of lesser immature crabs (CW < 100 mm) in baited traps (3.3% of the total catch in baited traps, 57.6% of the total catch in seine netting and otter trawling) and subsequently overestimating the SOM (Smith et al. 2004). However, this biasness might be beneficial from the population's conservation perspective. The overestimated SOM, which in turn resulted in an overestimated MLS, and the harvesting of mostly mature brachyuran crabs using baited traps pose a lesser threat and stress to the local brachyuran populations compared with the underestimated SOM and the all-in harvest strategy of nets and trawls. For research purposes, baited traps with different mesh size can be custom made and used to ensure more uniform catches.
Size at morphometric maturity
The usage of abdomen width (secondary sexual character) as an indicator in the estimation of size at morphometric maturity in female brachyurans is well documented and widely accepted by the scientific community (Leme 2005, Viau et al. 2006, Freire et al. 2011). The abrupt increase in female abdomen's dimension after pubertal molt is common in most brachyuran families, including Portunidae (Rasheed & Mustaquim 2010. Ikhwanuddin et al. 2011. Waiho et al. 2015), Sesarmidae Dana. 1851 (Flores et al. 2002, Ribeiro et al. 2013), Ucididae Stevcic. 2005 (Dalabona et al. 2005), and Ocypodidae Rafinesque, 1815 (Negreiros-Fransozo et al. 2003). This increase in abdomen's dimension is necessary to allow sufficient space for the deposition and incubation of eggs (Simons 1981). Hartnoll (1965), however, documented that in some grapsid crabs, the allometry changes in the female's abdomen width were not obvious and tend to overlap between immature and mature specimens.
Chela propodus dimensions and gonopod length are the preferred secondary sexual characters as they often showed drastic changes in allometric growth after attaining sexual maturity in most brachyuran species (Ribeiro et al. 2013). In comparison with females, male chelae have important functional purposes, i.e., they serve as sexual display accessory as well as a defense weapon (Koga et al. 2014). The increase in gonopod length is a morphological and functional change after the attainment of sexual maturity in male brachyurans as gonopods are the main sexual organs that will ensure successful copulation and transfer of male gametes over to a female's gonopores (Waiho et al. 2015, 2016b).
Size in physiological maturity
The number of stages in the classification of gonad development and maturation varies between species and researchers (Cobo & Fransozo 2005). However, some general descriptions are applicable in most brachyurans (Tables 1 and 2). The gonad maturation in females involves the increase in the dimension of ovaries and apparent color changes (typically from orange to red) in most brachyuran species and hence are used as the indicator for the estimation of the size at physiological maturity (Rasheed & Mustaquim 2010, Vallina et al. 2014). Males are generally classified as mature based on the enlargement of vas deferens and its physical appearance (milky white coloration). It is worthy to note that this indicator of male maturation should be used with caution as some brachyuran species such as Cardisoma guanhumi (Latrcillc in Latreille, Le Peletier, Serville & Guerin, 1828) (Brachyura: Gecarcinidae) (Shinozaki-Mendes et al. 2012) and Callinectes ornatus (Nascimento & Zara 2013) exhibit continuous sperm production even in immature individuals.
The indicators of physiological maturity, although providing direct visual confirmation of the maturation status, are not always the best option as the dissection and examination of the specimens' gonads in some circumstances such as during fishery dependent surveys are not recommended (Tallack 2007). In addition, because of the cyclical ripening of the ovaries, misidentification of mature female might occur if it was examined at the wrong time of its cycle (Tallack 2007).
Size at functional maturity
In females, their ovigerous state (the presence of egg brood under the abdomen) was the main indicator used to estimate the size at functional maturity. This indicator was preferred over the others because of its reliability as the external biological indicator of functional maturity (Wilhelm 1995). For some species, however, ovigerous females are rarely caught in traps or nets (Tallack 2007, Waiho et al. 2015) and thus, other indicators of functional maturity are used. Abdomen morphology is the second most favorable indicator of functional maturity in females. The female's abdomen experienced abrupt changes upon reaching sexual maturity, including a change in dimension and coloration to accommodate for the incubation of eggs (Hartnoll 1974, Ribeiro et al. 2013). The presence of sperm plugs was only used in two cases involving Cancer pagurus (Tallack 2007. Ungfors 2007). This is expected as Hankin et al. (1997) and Oh and Hankin (2004) demonstrated that the detection of sperm plugs was not definitive in all cancrid crabs-sperm plugs did not cause bulging of the vulva in some examined cancrid species [e.g., Metacarcinus edwardsii (Bell. 1835)].
The low number of cases in the estimation of male size at functional maturity is due to the difficulty in finding an accurate yet simple and straightforward indicator. Unlike females, male brachyurans do not exhibit any obvious cues indicating that they have matured or mated. Usage of mating scars is ambiguous (Knuckey 1996), the possibility of finding mating pairs in the wild is low in most brachyuran species, and mating experiments are laborious and time consuming. It is therefore recommended to use the abdominal locking mechanism as an indicator to determine male sexual maturity, in which the abdomen of an immature male is locked whereas that of a mature male is movable and can be fully opened when gentle pressure is applied (Van Engel 1958. Guinot & Bouchard 1998, Rodriguez-Felix et al. 2015, Waiho et al. 2016a). The application of this proposed method, however, needs to be validated in each species as the abdominal locking mechanism is absent in some species, e.g., Mictyridae and some Ocypodidae (Davie et al. 2015).
Maximum Size and Size at the Onset of Sexual Maturity
Infraorder Brachyura consists of crabs with diverse shapes and forms, each adapted to different habitats and lifestyles. Thus, the huge difference in maximum size and SOM between family and species was expected. For example, freshwater crabs such as Trichodactylus borellianus inhabit the littoral benthic zones of shallow lakes, streams, and rivers with complex temporal variability because of flood pulses and are constantly adjusting their distribution and abundance based on external factors such as water and food availability and predator pressure (Neiff 1990, Collins et al. 2006). Thus, with the available prey types (algae, diatoms, fungi, copepods, rotifers, cladocerans, etc.), surrounding habitat, and various abiotic and biotic factors, T. borellianus needs to be small and mobile (Williner & Collins 2013).
In addition, it is also important to highlight that latitudinal variations in the estimates of SOM was apparent between populations within the same species (Table 3). For example, the [CW.sub.50]s of Portunus pelagicus based on both morphometric and physiological data were significantly larger in Shark Bay, Australia (25[degrees] S), than those in four locations further south (30[degrees] S) (de Lestang et al. 2003). The growth trend of SOM based on latitudinal variation, however, is not consistent across species. The [CW.sub.50]s of Cancer pagurus based on functional data were lower ([CW.sub.50] = 107.0-118.0 mm) at a lower latitude (57[degrees] N-59[degrees] N) (Ungfors 2007) than those ([CW.sub.50] = 122.9-143.7 mm) found at a higher altitude (60[degrees] N) (Tallack 2007). The effect of latitudinal variation in SOM was observed in other crustacean species as well. Distinct increase in the SOM of male Norway lobsters Nephrops norvegicus (Linnaeus, 1758) from a south to north gradient (55[degrees] N-61[degrees] N) was reported by Queiros et al. (2013). Researchers had postulated that in general, decapods' [CW.sub.50]s are inversely related to water temperature (Campbell & Robinson 1983, Jones & Simons 1983, Dugan et al. 1991) and the variation in water temperature is latitude dependent [NASA Earth Observations (NEO) 2017]. Temperature plays an important role in determining the growth, maturation, reproductive behavior, and strategies of aquatic organisms (Castilho et al. 2008, van de Kerk et al. 2016). In addition to temperature, other factors such as precipitation and food availability also vary with latitudinal changes (Eliot & Goldman 1981). This resulted in the variation of reproductive and growth strategies adopted by a species that ranges in different climate zones along a latitudinal gradient to ensure survival (van de Kerk et al. 2016). Consequently, this gives rise to the difference in SOM of a species in different climatic (latitudinal) ranges. It is not uncommon, however, that occasionally some cases do not abide to this inverse relationship of water temperature and SOM because of the variation in other governing factors such as population density, resource availability, predation pressure, and habitat alteration and destruction (Hines 1989, Pollock 1995, McGarvey et al. 1999, Jordan et al. 2008). For example, the [CW.sub.50] of the warrior swimming crab Callinectes bellicosus along the gulf of California was directly related to temperature and inversely related to latitudinal gradient. It was postulated that as a summer spawner, the SOM of C. bellicosus depends on the longer months of higher temperature in the south than it is in the north (Rodriguez-Felix et al. 2015).
The decrease in [CW.sub.50] throughout time within the same species from the same sampling location was apparent (Table 3). For instance, using the same estimation method (SOM based on morphometric maturity), the [CW.sub.50] of female Scylla para-mamosain (Estampador, 1950) from Ban Don Bay, Thailand, decreased from 138.0 mm (Overton & Macintosh 2002) to 112.0 mm (Hamasaki et al. 2011). Another comprehensive study of the female blue crab Callinectes sapidus at Chesapeake Bay showed significant decrease in the annual [CW.sub.50] over a period of 13 y (1988-2000) (Lipcius & Stockhausen 2002). Temporal variation in SOM was reported for several aquatic organisms, including common whelk Buccinum undatum (Linnaeus, 1758) (Haig et al. 2015b), western rock lobster Panulirus cygnus (George, 1962) (Melville-Smith & de Lestang 2006), New Zealand abalone Haliotis iris (Gmelin, 1791) (McShane & Naylor 1995). Chinook salmon Oncorhynchus tshawytscha (Walbaum in Artedi, 1792) (Lewis et al. 2015), winter flounder Pseudopleuronectes americanus (Walbaum, 1792) (Winton et al. 2014), and southern rock lobster Jasus edwardsii (Hutton, 1875) (Gardner et al. 2006). One of the possible explanations could be that the decrease in SOM is the evolutionary response by local brachyuran populations to external factors that affected their population biology and ecology, e.g., overfishing and climate changes (Lipcius & Stockhausen 2002, Olsen et al. 2004). The intensity of fishing pressure and its negative effect on SOM was shown experimentally by Conover and Munch (2002) and reported by others in many aquatic species (Hard et al. 2008, Chuwen et al. 2011, Heinisch et al. 2014, Hunter et al. 2015. Lappalainen et al. 2016). It was also reported that when the overall population of C. sapidus was low in number, a higher percentage of smaller adult females (<140 mm CW) were found (Lipcius & Stockhausen 2002). The warmer temperature due to climate changes, together with intensive fishing pressure, was proposed to be the cause of earlier maturity in a commercially exploited marine fish as well (Neuheimer & Gronkjaer 2012). Other possible contributing factors such as ocean conditions or competitive interactions with other species may also cause these phenotypic shifts of earlier maturation and reductions in size (Lewis et al. 2015). Earlier maturation (younger age and smaller size) in crustaceans and other aquatic organisms is considered to be a coping mechanism, optimizing the opportunities to mate when larger potential mates were scarce (Jamieson et al. 1998). In addition, it could also be a strategy to maximize lifetime reproductive output due to the low competition from other adults (Lipcius 1985).
The results in this study (Table 3) showed clear sexual dimorphism in terms of the estimates of SOM between males and females. This is in agreement with the postulates of Hartnoll (1978). stating that brachyuran crabs, along with other crustacean species exhibit different relative growth between sexes. These differences in relative growth are apparent in the secondary sexual characters of crustaceans and enable the estimation of size at morphometric maturity (Hartnoll 1974). The trend, however, is not consistent even within the same species. For example, the [CW.sub.50]s at morphometric maturity of female Cancer pagurus was significantly larger than that of the male in the Shetland Islands. Scotland (Tallack 2007), but the opposite was reported in Skagerrak coast and Kattegat, Sweden (Ungfors 2007) (Table 3). As discussed, various factors could affect the SOM of a population, including climate changes (Olsen et al. 2004), food availability (Siddon & Bednarski 2010), and fishing pressure (Hard et al. 2008). Another possible postulation is that populations of lower densities may have higher growth rates and larger SOM because of the lower competition for food (Goni et al. 2003).
The study on the empirical relationship between SOM ([CW.sub.50]) and [CW.sub.max] is important because of the easier acquisition of body size measurements compared with other morphometric characters. Empirical equations of [CW.sub.50] with [CW.sub.max] may be useful in determining the [CW.sub.50] or [CW.sub.max] when only one variable is available (Tsikliras & Stergiou 2014). Such methods are frequently used in the assessment of other aquatic organisms such as fish (Binohlan & Froese 2009). The comparison of the two regression lines of both sexes revealed that the females of brachyuran species with [CW.sub.max] more than 20 mm may show delayed maturation compared with their male counterparts and females of smaller species. A possible explanation would be the positive exponential relationship between fecundity (number of oocytes) and body size. Thus, by delaying maturation, females are ensuring that they are of the optimum size and that oocyte generation can be at its maximum. This is especially important as some brachyuran species encounter terminal molt upon reaching sexual maturity (Diez & Lovrich 2012). This relationship, however, warrants further analysis, and the development of the empirical relationship of [CW.sub.50] with [CW.sub.max] of individual species with sufficient sample size is suggested for future monitoring of its populations.
CONCLUSIONS AND RECOMMENDATIONS
In brachyurans, sexual maturity is ultimately defined as the phase in which they are able to reproduce (i.e., achieving all morphometric, physiological, and functional maturities). The data collected in the present study reflect the scarcity and availability of maturation data of brachyurans on a global scale. In comparison with other aquatic species such as fishes (Tsikliras & Stergiou 2014), data such as number of specimens studied, the SOM, maximum size, and minimum size are inconsistent and often incomplete. This prevents in-depth comparison among brachyuran species and families. Thus, a standardized data reporting method is necessary. Data on SOM are important for the monitoring and management of a population and are useful as a predictor of the negative impact of overfishing, especially of commercially important crab species such as Scylla spp. and Portunus spp. It is recommended that the monitoring and estimation of SOM be conducted on a longer time frame (e.g., over few consecutive spawning seasons) to reveal the health and growth of a population and also the effect of fishing pressure and/or other anthropogenic factors such as habitat destruction, pollution, and climate changes. In addition, the enforcement of MLS in all landing sites, especially for commercially important brachyuran species such as crabs of the families Cancridae and Portunidae, is needed. Setting the MLS well above the SOM is also recommended. Size-limit fishing is able to reduce the impact of fishing on stocks' population health as brachyurans are able to grow into sexual maturity and have the chance to at least reproduce once before being captured. Last, the sustainability and survival of a population rely on the SOM data as their health benchmark, and the continuous availability of these data is urgently needed.
This work was partially funded by Malaysia's Ministry of Higher Education under Niche Research Grant Scheme (NRGS) (Vot. No. 53131); STU Scientific Research Foundation for Talents (No. NTF17006); the National Program for Support of Top-Notch Young Professionals; and the "Sail Plan" Program for the Introduction of Outstanding Talents of Guangdong Province, China (14600702). Our sincere gratitude to Mr. Basil C. Baylon for proofreading this manuscript.
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KHOR WAIHO, (1,2) HANAFIAH FAZHAN, (1,2*) JULIANA C. BAYLON, (3) HASHIM MADIHAH, (2) SHAIBANI NOORBAIDURI, (2) HONGYU MA (1*) AND MHD IKHWANUDDIN (2*)
(1) Guangdong Provincial Key Laboratory of Marine Biotechnology, Shantou University, Daxue Road, 515063, Shantou, Guangdong, China; (2) lnstitute of Tropical Aquaculture, Universiti Malaysia Terengganu, Mengabang Telipot, 21030, Kuala Terengganu, Terengganu, Malaysia; (3) Division of Biological Sciences, College of Arts and Sciences, University of the Philippines Visayas, 5023, Miagao, Iloilo, Philippines
(*) Corresponding authors. E-mails: firstname.lastname@example.org, email@example.com, and firstname.lastname@example.org
TABLE 1. Summary of the characteristics of the three gonadal maturation stages found in male brachyurans. Family Genus Immature Cancridae Cancer Small, transparent testes, or undetectable Gecarcinidae Cardisoma Testes similar size with other stages Smaller AVD, MVD, PVD No spermatophores in PVD Geryonidae Chaccon Colorless gonad Vas deferens not differentiated Majidae Anamathia Thin and translucent testes Portunidae Arenaeus Gonad only observable under magnification Colorless vas deferens Callinectes Small testes and vas deferens All germ cells present in the seminiferous lobules of testes Portunus Undifferentiated gonad Scylla Testes barely noticeable Entire gonad is translucent and grey Smaller spermatophores present in AVD and MVD Sesarmidae Armases Gonad undifferentiated Trichodactylidae Sylviocarcinus Small and transparent testes and vas deferens Spermatogonia and spermatocytes present in seminiferous tubules of testes Gonadal maturation characteristics Family Genus Maturing Cancridae Cancer Visible and white testes Spermatozoa present Thin, partly filled testes and vas deferens Gecarcinidae Cardisoma Testes, AVD, and MVD similar to immature stage Longer and wider PVD Spermatophores observable in PVD Geryonidae Chaccon White, visible gonad Vas deferens lowly coiled and differentiated, with minimal sperm or spermatophores Majidae Anamathia Filamentous and opaque white vas deferens Portunidae Arenaeus Visible and translucent vas deferens Gonad:hepatopancreas size ratio =1:4 Gonad is white in color Callinectes Medium size testes and vas deferens All germ cells present in the seminiferous lobules of testes Portunus Developed and clearly differentiated testes and vas deferens Large coiled testes, enlarged AVD, and straight opaque MVD and PVD Scylla Small testes AVD, MVD, and PVD are small but recognizable Spermatophores still small in size in AVD and MVD Sesarmidae Armases Vas deferens appears filamentous, translucent, and somewhat entwined Trichodactylidae Sylviocarcinus Testes and vas deferens are white and increase in size and volume Spermatids and few spermatozoa present in addition to spermatogonia and spermatocytes in testes Family Genus Mature Cancridae Cancer Enlarged, whitish testes and vas deferens Spermatophores present in vas deferens Gecarcinidae Cardisoma Testes similar in size with other stages Larger and more developed AVD, MVD, and PVD More spermatophores in PVD Geryonidae Chaccon Milky-white, visible gonad Swollen testes Vas deferens are highly coiled and fully filled with sperm or spermatophores Majidae Anamathia Swollen testes, opaque vas deferens Portunidae Arenaeus Gonad (white in color) larger than hepatopancreas, occupying all cephahlothoracic cavity Callinectes Enlarged testes and vas deferens All germ cells present in the seminiferous lobules of testes Portunus Testes further enlarged Vas deferens are coiled and swollen Enlarged AVD and MVD (milky white), and PVD (opaque) Scylla Swollen, enlarged, and white gonad, except PVD (translucent and grey) Spermatophores significantly larger and found in AVD and MVD Sesarmidae Armases Fully developed gonad Whitish entwined vas deferens Trichodactylidae Sylviocarcinus Testes is milky white and vas deferens is yellowish brown Enlarged testes and vas deferens occupy whole thoracic cavity Spermatozoa present in all seminiferous tubules of testes Family Genus Source Cancridae Cancer Ungfors (2007); Haig et al. (2015a) Gecarcinidae Cardisoma Shinozaki-Mendes et al. (2012) Geryonidae Chaccon Biscoito et al. (2015) Majidae Anamathia Mura et al. (2005) Portunidae Arenaeus Pinheiro and Fransozo (1998) Callinectes Nascimento and Zara (2013) Portunus Soundarapandian et al. (2013) Scylla Waiho et al. (2017) Sesarmidae Armases Lima et al. (2006) Trichodactylidae Sylviocarcinus Silva et al. (2012) TABLE 2. Summary of the characteristics of the five ovarian maturation stages found in female brachyurans. Family Genus (a) Immature (I) Cancridae Cancer Thin, translucent, white, and pale No egg cells Majidae Anamathia Filamentous and translucent Ocypodidae Uca Undeveloped, thin, transparent, and filamentous Oogonia surrounded by follicle cells No primary and secondary oocytes Portunidae Scylla Thin, translucent to off-white Contain oogonia, primary oocytes with large nuclei Follicle cells present Portunus Small, thread like, flattened, smooth in texture without pronounced lobulation, and off-white to ivory color (b) Proliferation (I) Portunidae Callinectes Presence of previtellogenic oocytes with a layer of prefollicle cells Oocyte diameter = 16-24 [micro]m Scylla Translucent and ribbon like Oocyte diameter = 35-50 [micro]m Presence of cluster of oogonia (c) Immature (I) Platyxanthidae Platyxanlhus Only visible under magnification Translucent filament Family Genus Ovarian maturation characteristics (a) Early maturing (II) Cancridae Cancer Lobes present, greyish pink Previtellogenesis Majidae Anamathia Ovaries start to swell Pale yellow-orange coloration Ocypodidae Uca Yellow to orange-reddish Gonad:hepatopancreas ratio is 1:10 Oogonia and previtellogenic oocytes surrounded by follicle cells Portunidae Scylla Yellow and small yolk globules started to appear in larger oocytes Portunus Relatively large, light yellow in color and anterior lobes marginally displaced hepatopancreas, posterior lobes convoluted (b) Previtellogenesis (II) Portunidae Callinectes Swollen seminal receptacles in the oviduct Ooplasm intensely basophilic and has distinct perinuclear yolk complex Oocyte diameter = 30-60 [micro]m Scylla Off white to creamy (2-3 mm thick) Occupy 1%-2% of cavity Oocyte diameter = 45-100 [micro]m Visible follicle cells (c) Maturing (II) Platyxanthidae Platyxanlhus Visible to naked eye Creamy to pink filament Family Genus (a) Late maturing (III) Cancridae Cancer Slight pink coloration Covers <50% body cavity Majidae Anamathia Occupied most of the dorsal part of cephalothoracic cavity Yellow-orange coloration Oocytes not visible Ocypodidae Uca Lobate shape and dark red coloration Gonad:hepatopancreas ratio is 1:2 Abundance of vitellogenic oocytes Follicle cells surround secondary oocytes Portunidae Scylla Light orange and lobules apparent Yolk globules occurred in the cytoplasm with larger globular inclusions toward the periphery Follicle cells hardly recognizable Portunus Large, yellow with rough nodulations Anterior lobes displaced the hepatopancreas, central and posterior lobes covered the gastric and intestinal cavities (b) Primary vitellogenesis (III) Portunidae Callinectes Perinuclear yolk complex disappeared Ooplasm contained eosinophilic yolk bodies Presence of stage 2 previtellogenic oocytes Oocyte diameter = 60-100 [micro]m Scylla Pale or light yellow (3-7 mm thick) Occupy 10%-20% of cavity Oocyte diameter = 80-150 [micro]m Presence of yolk globules (c) Mature (III) Platyxanthidae Platyxanlhus Swollen, voluminous Dark pink to purple coloration Presence of detectable vitellogenic oocytes Family Genus (a) Fully mature (IV) Cancridae Cancer Orange, red coloration Large, obvious ovaries Covers >50% body cavity Majidae Anamathia Fully developed Yellowish coloration Occupied anterior abdominal region too Oocytes visible Ocypodidae Uca Occupied whole thoracic cavity, very dark red coloration Gonad: hepatopancreas ratio =9:10 Abundance of mature secondary oocytes Oogonia and previtellogenic oocytes are rare Portunidae Scylla Orange to deep orange and had swollen lobules Large yolk globules apparent in oocytes Follicle cells were hardly seen Portunus Very large, highly nodulated and dark orange in color Occupied almost entire carapace's space. (b) Secondary vitellogenesis (IV) Portunidae Callinectes Ooplasm full of eosinophilic bodies Oocyte diameter = 103-160 [micro]m Scylla Yellow to orange (7-12 mm thick) Occupy 20%-75% of cavity Oocyte diameter = 120-200 [micro]m Yolk globules occupied cytoplasm (c) Spent (IV) Platyxanthidae Platyxanlhus Lax, creamy, flattened Few or no vitellogenic oocytes Family Genus (a) Spent (V) Cancridae Cancer Loose, whitish ovaries Some remnant eggs present Majidae Anamathia Reduced in size Similar to a thick filament Pale yellowish coloration Ocypodidae Uca Thin, flaccid, filamentous, and transparent Gonad: hepatopancreas ratio =1:10 Oogonia and primary oocytes present Portunidae Scylla Similar to the early-maturing and late-maturing stage in partially spawned females Portunus Small, off-white, and thread like Similar to immature stage (b) Tertiary vitellogenesis (V) Portunidae Callinectes Similar to stage IV Oocyte diameter = 168-288 [micro]m Scylla Visible individual eggs Yellow orange to red orange (10-20 mm thick) Occupy >75% of cavity Oocyte diameter = 150-250 [micro]m Nucleus barely visible (c) Recovering (V) Platyxanthidae Platyxanlhus Swollen and partly vacuous Light cream to pink in color Abundant of vitellogenic and scattered atretic oocytes Family Genus Source (a) Cancridae Cancer Haig et al. (2005a) Majidae Anamathia Mura et al. (2005) Ocypodidae Uca Castiglioni et al. (2007) Portunidae Scylla Quinitio et al. (2007) Portunus Ravi et al. (2012) (b) Portunidae Callinectes Lee et al. (1996) Scylla Islam et al. (2010) (c) Platyxanthidae Platyxanlhus Leal et al. (2008) TABLE 3. Size ([CW.sub.50]) and length ([CL.sub.50]) at maturity, maturation range ([CW.sub.mature]), maximum ([CW.sub.max]) and minimum ([CW.sub.min]) maturation size, indicators used to estimate [CW.sub.50] or [CL.sub.50], sampling methods (SM), number of samples (N), and country and year of study of brachyurans based on different types of maturity (morphometric, physiological, and functional maturities). Maturity Family Species Sex Morphometric Cancridae Cancer bellianus F C. belliamus M Cancer borealis M Cancer pagurus F C. pagurus M C. pagurus M C. pagurus M C. pagurus F C. pagurus M Epialtidae Leueippa pentagona F L. pentagona M Geryonidae Chuceon affinis F C. affinis F C. affinis M C. affinis M C. affinis M C. affinis M Chaceon bicolor M Goneplacidae Carcinoplax vestita F C. vestita M C. vestita M C. vestita M Grapsidae Grapsus grapsus F G. grapsus M Pachygrapsus F transversa P. transversus M Homolidac Paromota cuvieri F P. cuvieri M P. cuvieri M P. cuvieri M P. cuvieri M Hymenosomatidae Halicarcinus planatus F H. planatus M Hypolhalassiidae Hypothalassia M acerba Lithodidae lAthodes aequispina M Lithodes ferox M Majidae' Leurocyclus F tuberculosa L. tuberculosus M Maja squinado F M. squinado M Microphrys F bicornutus M. bicornutus M M. bicornutus M M. bicornutus M Mithraculus forceps F M. forceps M Menippidae Menippe spp. F Menippe spp. F Menippe spp. M Menippe spp. M Mithracidae Mithrax Tortugae F M. Tortugae M Ocypodidae Uca thayeri F U. thayeri M Panopeidae Panopeus austrobesus F P. austrobesus M Platyxanthidae P. patagonicus F Platyxanthus M patagonicus Portunidae Arenaeus cribrarius F A. cribrarius M Callinectes danae F C. danae M Liocarcinus F depurator L. depurator F L. depurator F L. depurator F L. depurator M L. depurator M Necora puber F N. puber M Ovalipes trimaculatus F O. trimaculatus M Portunus pelagicus M P. pelagicus M P. pelagicus M P. pelagicus M P. pelagicus M P. pelagicus M Portunus F sanguinolentus P. sanguinolentus M P. sanguinolentus M Scylla olivacea F Scylla paramamosain F S. paramamosain F S. paramamosain M Scylla serrata F S. serrata M S. serrata M S. serrata M Potamidae Potamon fluviatile F P. fluviatile M Pseudothelphusidae Eudaniela garmani F E. garmani M Sesarmidae Perisesarma F guttatum P. guttatum M P. guttatum M Sesarma rectum F S. rectum M Trichodactylidae Trichodactylus F borellianus T. borellianus M Trichodactylus F petropolitanus T. petropolitanus M T. petropolitanus M Ucididae Ucides cordatus F U. cordatus F U. cordatus M U. cordatus M Physiological Cancridae C. pagurus F C. pagurus M C. pagurus M C. horealis M Dorippidae Medorippe lunata F Epialtidac L. pentugona M Geryonidac C. affinis F C. affinis F C. affinis M C. affinis M C. bicolor M Geryon maritae M Grapsidae G. adscensionis M G. grapsus F G. grapsus M Homolidae P. cuvieri F P. cuvieri M Hymenosomatidae H. planatus M Hypothalassiidae H. acerba M Majidae Anamathia rissoana F Ocypodidae Peypode F ceratophthalmus P. ceratophthalmus M Oregoniidae Chionoecetes bairdi F Platyxanthidae P. patagonicus F P. patagonicus M Portunidae A. crihrarius F A. crihrarius M A. crihrarius F A. cribrarius M Callinectes bellicosus F C. danae F C. danae M Charybdis affinis F C. affinis M Liocarcinus F depurator N. puber M Ovalipes trimacutatus F O. trimaculatus M P. pelagicus F P. pelagicus F P. pelagicus M P. pelagicus M P. pelagicus M P. pelagicus M P. pelagicus M P. pelagicus M P. sanguinolenlus F P. sanguinolentus M S. paramamosain M S. serrata F S. serrata M S. serrata M Potamidae Candidiopotamon M rathbunae Sesarmidae P. guttatum F P. guttatum M Functional Cancridae C. pagurus F C. pagurus F C. pagurus F C. pagurus F Epialtidae Acanthonyx F scutiformis A. scutiformis M L. pentagona F Geryonidae C. affinis F C. affinis F C. fenneri F G. maritac F G. maritac M Grapsidae G. adscensionis F Homolidae P. cuvieri F P. cuvieri F Hymenosomatidae II. planatus F Lilhodidae L. aeguispina F L. ferox F Majidae A. rissoana M L. luberculosus F M. squinado F Schizophrys aspera F Menippidae Menippe spp. F Menippe spp. M Ocypodidae P. ceratophthalmus F Oregoniidae C. bairdi F C. bairdi M C. bairdi F C. bairdi M Platyxanthidae P. patagonicus F P. patagonicus F Portunidae C. betlicosus F C. bellicosus M C. danae F C. danae F C. danae M C. danae F Callinectes sapidus F C. sapidus F C. sapidus F Carcinus aestuarii F N. puber F P. pelagicus F P. pelagicus F P. pelagicus F P. pelagicus F P. pelagicus F P. pelagicus F S. olivacea F S. olivacea F S. olivacea M S. serrala F Scylla tranquebarica F S. tranquebarica F S. tranquebarica M Potamidae C. rathbuuae F C. rathbunae M Pseudothelphusidae E. garmani F [CW.sub.50] [CW.sub.mature] Maturity (mm) (mm) Morphometric 101.2 ([CL.sub.50]) - 103.5 ([CL.sub.50]) - 127.6 - 103.7 - 122.5 - 122.3 - 119.5 - 115.9 - 101.6-109.5 - 18.5 ([CL.sub.50]) - 28.1 ([CL.sub.50]) - 98.2 - 103.0 - 103.6 - 103.2 - 113.1 - 111.4 82.7 - 13.9 ([CL.sub.50]) - 15.0 ([CL.sub.50]) - 15.8 ([CL.sub.50]) - 16.0 ([CL.sub.50]) - 33.8 - 51.4 - 55 ([CL.sub.50]) - 5.0 ([CL.sub.50]) - 73.6 - 92.1 - 92.2 - 91.7 - 91.3 - 9.55 - 9.8 - 83.1 - 114.0 ([CL.sub.50]) - 108.0 ([CW.sub.50]) - 47.9 - 48.9 - 130.4 ([CL.sub.50]) - 132.7 ([CL.sub.50]) - 13.6 ([CL.sub.50]) - 16.5 ([CL.sub.50]) - 16.9 ([CL.sub.50]) - 17.7 ([CL.sub.50]) - - 8.5-16.0 - 6.7-13.9 59.6 - 61.1 - 68.0 - 71.1 - 22.4 - 13.0 _ - 10.7-16.8 13.8 - 13.0 - 14.6 - 50.0 ([CL.sub.50]) - 44.0 ([CL.sub.50]) - 59.7 - 52.0 - 67.8 - 88.4 - 29.4-31.5 - 28.3-30.8 - 27.4-28.9 - 28.1-30.1 - 34.4-35.0 - 31.4 35.7 - 52.3 - 53.3 - 44.6 - 52.3 - 87.2 - 87.1 - 86.2 - 86.2 - 96 - 82 - - 64.0-72.0 ([SCW.sub.mature] - 64.0-70.0 ([SCW.sub.mature] 64.0-71.0([SCW.sub.mature] 108.0 - 138.0 - 112.0 - 106.4 - 132.4 - 150.7 - 149 - 146 - 35.0 ([CL.sub.50]) - 35.0 ([CL.sub.50]) - 67.0 - 48.0 - 15.3 - 9.3 - 9 4 - 23.0 - 27.1 - 6.9 - 6.6 - 23.0 - 25.0 - 25.0 - 45.0 - 43 - 52.0 - 44 Physiological 132.0 - 117.0 - 104.3 - 68.5 - 21.0 ([CL.sub.50]) - 16.7 ([CL.sub.50]) - 110.5 - 104.7 118.9 - 113.8 - 68.1 - - >80.0 - [greater than or equal to]38.0 33.4 - 38.4 - 71.7 - 91.0 - 3.6 - 94.3 - 9.4 - - - - - 68.0 - 66.4 - 54.7 - 59.7 - 63.4 - 56.3 - 50.1 -- 107.8 -- 67.0 -- 86.5 -- 42.1 -- 36.0 -- -- 30.0-34.0 (CTW) 54.8 -- 54.6 -- 46.6 -- 58.5 -- 103.0 -- 98.0 -- 88.3 -- 88 -- 86.5 -- 88.4 -- 97 -- 63.5 ([SCW.sub.50]) -- 60.8 ([SCW.sub.50]) -- 109.0 ([ICW.sub.50]) -- 70.0 -- 75.0 -- 92.0 -- -- >21.5 10.4 -- 8.9 -- Functional 107.0 -- 118.0 -- 122.9 -- 143.7 100.0 (MOS) 8.9 -- 10.7 -- 18.3 ([CL.sub.50]) -- 104.4 79.6-158.0 109.3 74.0-169.0 -- 85.0-100.0 84.0 -- -- [greater than or equal to]76.0 -- [greater than or equal to]43.0 72.0 -- 74.0 -- 9.6 -- 105.5 ([CL.sub.50]) -- 83.3 ([CL.sub.50]) 75.0 (MOS) 97 -- -- 42.7 (MOS) 103.6 -- 36.0 -- -- 38.2 (MMS) -- 49.5 (MMS) -- -- -- 80.0-100.0 (MMS) -- 50.0-60.0 (MMS) 83.0 -- -- 90.0 (MMS) 66.8 -- -- 42.7 (MOS) 111.6 -- 118.8 -- 80.5 -- -- 75.5 (MOS) 91.3 -- 70.5 -- 118.5 -- 123 (1988) -- to 112 (2000) 103.3 -- 26.8 -- 49.8 -- -- 91.6 (MOS) 98 -- 86.9 -- 97.5 -- 86.4 -- 92 -- 96 -- 86 -- 113 -- 123.0 -- 108 -- 92 -- 13.1 -- -- [greater than or equal to]22.3 (MMS) -- [greater than or equal to]23.1 (MMS) -- [greater than or equal to]69.0 [CW.sub.max] [CW.sub.min] Maturity (mm) (mm) Morphometric 129.0 (CL) 68.0 (CL) 136.0 (CL) 59.0 (CL) 184.8 49.7 - - - - - - - - - - - - - - 158.0 35.1 169.1 44.0 184.8 38.0 184.8 38.0 187.0 42.0 187.0 42.0 - - 23.7 (CL) 7.7 (CL) 23.9 (CL) 6.8 (CL) 23.9 (CL) 6.8 (CL) 23.9 (CL) 6.8 (CL) 57.3 9.1 69.5 14.2 16.8 2.4 19.6 2.4 109.0 34.0 164.0 38.0 164.0 38.0 164.0 38.0 164.0 38.0 - - 13.6 1.8 - - 188.0 (CL) 62.0 (CL) 153.0 (CL) 24.0 (CL) 77.3 10.2 88.0 12.4 - - - - 27.2 4.5 33.2 4.1 33.2 4.1 33.2 4.1 - - - - - - - - - - - - 25.5 4.5 25.6 3.7 34.5 3.1 44.8 40 - - - - 92.8 28.4 107.7 22.1 113.1 19.9 117.2 19.8 - - - - - - - - - - - - - - - - 98.3 18.2 104.5 14.9 - - - - - - - - - - 130.0 28.0 125.0 24.0 125.0 24.0 170.6 69.2 156.0 65.2 147.5 72.0 145.0 72.0 159.2 97.3 193.5 101.0 - - - - - - - - - - - - - - - - - - 32.9 13.4 36.1 15.0 12.4 2.7 104 2.9 29.2 10.5 29.1 10.4 29.1 10.4 71.1 26.6 73.3 30.6 80.6 20.5 83.5 35.5 Physiological - - - - - - 184.8 49.7 29.0 (CL) 10.0 (CL) - - 169.1 44.0 158.0 35.1 187.0 42.0 184.8 38.0 - - - - 74.0 25.0 57.3 9.1 69.5 14.2 109.0 34.0 164.0 38.0 13.6 1.8 - - - - 39.9 25.4 43.6 27.1 - - 126.6 18.9 145.3 14.5 92.8 28.4 107.7 22.1 94.5 - 103.2 -- -- -- 113.1 19.9 117.2 19.8 -- -- -- -- -- -- -- -- 98.3 18.2 104.5 14.9 -- -- 173.2 74.1 181.2 71.3 -- -- -- -- -- -- -- -- -- -- 130.0 (SCW) 28.0 (SCW) 125.0 (SCW) 24.0 (SCW) 128.0 (ICW) 60.0 (ICW) -- -- -- -- -- -- 29.8 11.7 -- -- -- -- Functional -- -- -- -- -- -- -- -- 12.7 4.2 15.8 3.7 -- -- -- -- -- -- -- -- -- -- -- -- 74.0 30.0 109.0 34.0 109.0 34.0 -- -- 174.0 (CL) 59.0 (CL) 126.0 (CL) 19.0 (CL) -- -- 77.3 10.2 140.2 -- -- -- -- -- -- -- 39.9 26.9 -- -- -- -- -- -- -- -- 126.6 18.9 -- -- -- -- -- -- 118.6 23.1 118.6 23.1 128.0 24.9 113.1 19.9 -- -- -- -- -- -- -- -- -- -- 173.2 74.1 -- -- -- -- -- -- -- -- -- -- 153.0 62.0 153.0 63.0 115.0 67.0 -- -- 157.0 68.0 157.0 68.0 139.0 69.0 -- -- -- -- -- -- Maturity Indicator Morphometric Left PRW/CL Left PRW/CL PRH/CW AW/CW Right PRL CW Right PRH/CW Right PRW/CW AW/CW - AW/CL PRL/CL 5AS/CW 5AS/CW Left PRL/CW Right PRL/CW Left PRL/CW Right PRL/CW PRL/CL AW/CL PRL CL DL/CL PRH/CL AW/CW PRL CW AW/GL GL/CL 5AS/CW Left PRL/CW Right PRL/CW Left PRW/CW Right PRW/CW AW/CW Right PRL CW PRL CL Right PRH CL Right PRH/CL AW/CW PRL/CW AW/CL Right PRH/CL and PRL/CL AW/CL PRL/CL PRW/CL GL/CL AW/CW PRL/CW PRL/CW PRL/CW PRL/CW PRL/CW AW/CW GL/CW AW/CW PRL/CW AW/CW GL/CW AW/6AS PRL/CL AW/CW PRL/CW AW/CW Major and minor PRL CW 4AS/CW 5AS/CW 6AS/CW 5/6AS/CW Right PRL/CW GL/CW AW/CW GL/CW PRW/CW PRH/CW DSL/CW DSL/CW DSL/CW DSL/CW DSL/CW PRL/CW AW/SCW PRL/SCW GL/SCW AW/CW AW/CW AW/CW PRH/CW AW/CW PRH/CW PRH/CW PRH/CW AW/CL PRL/CL AW/CW PRL/CW AW/CW PRL/CW GL/CW AW/CW Right PRL/CW AW/CW GL/CW AW/CW AW/CW GL/CW AW/CW AW/CW PRL/CW Major PRL/CW Physiological Developing/ripe ovaries Mature gonad - Presence of SPH Stage III OMS Presence of SPH [greater than or equal to]Stagel V OMS [greater than or equal to]Stage IV OMS Stage III MGM Stage III MGM Enlarged MVD and PVD Presence of SPH Large, opaque white VD Large, orange ovaries Enlarged, white testes [greater than or equal to]Stage II OMS [greater than or equal to]Stage II MGM Presence of SPZ in VD Enlarged MVD and PVD [greater than or equal to]Stage III OMS Vitellogenesis in oocytes Presence of SPZ Orange ova [greater than or equal to]Mature OMS Presence of SPH. increased VD volume [greater than or equal to]Stage III OMS [greater than or equal to]Stage III MGM [greater than or equal to]Stage III OMS [greater than or equal to]Stage III MGM [greater than or equal to]Stage II OMS [greater than or equal to]Developing OMS [greater than or equal to]Developing MGM [greater than or equal to]Stage III OMS Presence of testes Advance OMS -- [greater than or equal to]Stage III OMS Presence of SPH in VD Visible ovaries under magnifying glass [greater than or equal to]Stage III OMS Stage III MGM Stage III MGM Stage III MGM Stage III MGM Stage III MGM Stage III MGM Large, orange, nodulated ovaries Enlarged AVD and MVD Presence of SPH and visibility of VD [greater than or equal to]Stage II OMS Stage III MGM Presence of SPM in VD Presence of SPM in VD [greater than or equal to]Stage III OMS [greater than or equal to]Stage III MGM Functional Presence of SPM in SPTC Presence of SP in OD Presence of SP Ovigerous state Cheliped morphology Cheliped morphology Ovigerous state Open vulvae Open vulvae Ovigerous state, OMS, types of gonopores Open vulvae Presence of MS Presence of SPM in spermathecae, ovigerous state Ovigerous state Open vulvae Ovigerous state Ovigerous slate Ovigerous state Cheliped morphology Ovigerous state Mature abdomen Ovigerous state Engaged in mating Engaged in mating Presence of SPZ in SPTC Ovigerous state Successful fertilization Mature abdomen Successful fertilization Ovigerous state Ovigerous state Presence of SPH in SPTC Detached abdomen Detached abdomen Ovigerous state Detached abdomen Ovigerous state Broad abdomen Broad abdomen Ovigerous state Ovigerous stale Ovigerous state, presence of SPM in SPTC Ovigerous state Pubertal molt Pubertal molt Pubertal molt Pubertal molt Pubertal molt Presence of MD Mature abdomen Presence of MS Mature abdomen Presence of MD Mature abdomen Presence of MS Ovigerous state Engaged in mating Ovigerous state Country Maturity SM N (location) Morphometric BT, ST 156 Spain (Canary Islands) BT, ST 251 Spain (Canary Islands) BTl 540 Canada (Scotian Shelf) - - Sweden (Skagerrak coast and Kattegat) - - Sweden (Skagerrak coast and Kattegat) - - Sweden (Skagerrak coast and Kattegat) - - Sweden (Skagerrak coast and Kattegat) - 412 Scotland (Shetland Islands) - 402 Scotland (Shetland Islands) SD 315 Argentina (Bustamante Bay) SD 297 Argentina (Bustamante Bay) BT 427 Portugal (Madeira) BT 1,403 Spain (Canary Islands) BT 1,964 Portugal (Madeira) BT 1,957 Portugal (Madeira) BT 1,316 Spain (Canary Islands) BT 1,321 Spain (Canary Islands) RLT 723 Australia (South coast of western Australia) BMT 340 Japan (Tokyo Bay) BMT 372 Japan (Tokyo Bay) BMT 372 Japan (Tokyo Bay) BMT 372 Japan (Tokyo Bay) CN, HC 321 Brazil (Saint Peter and Saint Paul Archipelago) CN. HC 384 Brazil (Saint Peter and Saint Paul Archipelago) - 227 Brazil (Praia Grande. Ubatuba) - 240 Brazil (Praia Grande. Ubatuba) BT 431 Spain (Canary Islands) BT 243 Spain (Canary Islands) BT 243 Spain (Canary Islands) BT 243 Spain (Canary Islands) BT 243 Spain (Canary Islands) HC 1,147 Chile. Argentina (Beagle Channel) HC 694 Chile, Argentina (Beagle Channel) RLT 571 Australia (South coast of western Australia) BT 395 Canada (Northern British Columbia) TN 1,139 Namibia BT, SC. HC 303 Argentina (Patagonian Gulfs) BT, SC, HC 116 Argentina (Patagonian Gulfs) GB 1,172 Spain (Ria de Arousa) (Hi 1,981 Spain (Ria de Arousa) HC 733 Venezuela (lsla Margarita) HC 666 Venezuela (Isla Margarita) HC 666 Venezuela (Isla Margarita) HC 666 Venezuela (Isla Margarita) SD 188 Brazil (Couves Island) SD 248 Brazil (Couves Island) BT 2,384 United States of America (Tampa Bay) BT 2,384 United States of America (Tampa Bay) BT 2,527 United States of America (Tampa Bay) BT 2,527 United States of America (Tampa Bay) SD 104 Brazil (Vitoria Island) SI) 64 Brazil (Vitoria Island) HC 419 Brazil (Comprido and Escuro rivers. Ubatuba) HC 390 Brazil (Comprido and Escuro rivers. Ubatuba) HC 124 Brazil (Comprido and Escuro rivers. Ubatuba) HC 138 Brazil (Comprido and Escuro rivers. Ubatuba) BMT 538 Argentina (Patagonia) BMT 568 Argentina (Patagonia) OT 1,313 Brazil (Ubatuba littoral) OT 685 Brazil (Ubatuba littoral) TN 504 Brazil (Guaratuba Bay) TN 398 Brazil (Guaratuba Bay) BMT 581 Spain (Ria de Arousa) BMT 581 Spain (Ria de Arousa) BMT 581 Spain (Ria de Arousa) BMT 581 Spain (Ria de Arousa) BMT 865 Spain (Ria de Arousa) BMT 864 Spain (Ria de Arousa) - - Spain (Ria de Arousa) - - Spain (Ria de Arousa) TN 588 Argentina (coast of Mar del Plata) TN 724 Argentina (coast of Mar del Plata) BS, OT, BT 160 Australia (Leschenault Estuary) BS. OT. BT 97 Australia (Koombana Bay) BS, OT, BT 498 Australia (Peel-Harvey Estuary) BS, OT, BT 811 Australia (Cockburn Sound) US. OT, BT 602 Australia (Shark Bay) BS, OT 1,287 Australia (Cockburn Sound) - 224 Pakistan (Karachi) - 233 Pakistan (Karachi) - 233 Pakistan (Karachi) BT 835 Thailand (Ban Don Bay) BT 780 Thailand (Ban Don Bay) BT, GN 70 Thailand (Bandon Bay) BT, GN 114 Thailand (Bandon Bay) BT, GN 54 Japan (Iriomote Island) BT, GN 64 Japan (Iriomote Island) BT - Australia (Van Diemen Gulf) BT - Australia (Gulf of Carpentaria) - 235 + 27 UJ Italy (Florence) - 212 + 42 UJ Italy (Florence) HC 74 Trinidad (Maracas, Aripo, Arima, Guanapo valleys) HC 71 Trinidad (Maracas, Aripo, Arima, Guanapo valleys) HC 353 Mozambique (Inhaca Island) HC 504 Mozambique (Inhaca Island) HC 542 Mozambique (Inhaca Island) HC 230 Brazil (Coco River Ecological Park) HC 262 Brazil (Coco River Ecological Park) - 182 Argentina (Parana alluvial valley) - 155 Argentina (Parana alluvial valley) S 64 Brazil (Caeapava) S 65 Brazil (Cacapava) S 65 Brazil (Cacapava) BT 383 Brazil (Jaguaribe River) HC 232 Brazil (Laranjeiras Bay) BT 594 Brazil (Jaguaribe River) HC 323 Brazil (Laranjeiras Bay) Physiological - 399 Sweden (Skagerrak coast and Kattegat) - 631 Sweden (Skagerrak coast and Kattegat) - 73 Scotland (Shetland Islands) BT 540 Canada (Scotian Shell) BMT 725 Italy (eastern Ligurian Sea) SD 297 Argentina (Bustamante Bay) BT 1,714 Spain (Canary Islands) BT 2,056 Portugal (Madeira) BT 2,161 Spain (Canary Islands) BT 2,122 Portugal (Madeira) RLT 723 Australia (South coast of western Australia) BT, TN - Namibia HC 35 Ascension Island (English Bay) CN, HC 321 Brazil (Saint Peter and Saint Paul Archipelago) CN, HC 384 Brazil (Saint Peter and Saint Paul Archipelago) BT 431 Spain (Canary Islands, BT 243 Spain (Canary Islands) HC 198 Chile, Argentina (Beagle Channel) RLT 571 Australia (South coast of western Australia) TN 248 Italy (Sardinian Sea) ~ 192 Hawaii (Oahu) 161 Hawaii (Oahu) TN, BT, SD, FS 98 United States of America BT 1,061 Argentina (northern Patagonian gulfs) BT 710 Argentina (northern Patagonian gulfs) OT 1,369 Brazil (Ubatuba littoral) OT 952 Brazil (Ubatuba littoral) DRN - Brazil (Ubatuba) DRN -- Brazil (Ubatuba) RN 255 Mexico (Santa Maria) TN 504 Brazil (Guaratuba Bay) TN 398 Brazil (Guaratuba Bay) TN 480 China (Zhujiang estuary) TN 377 China (Zhujiang estuary) BMT 1,561 Spain (Ria de Arousa) -- -- Spain (Ria de Arousa) TN 124 Argentina (coast of Mar del Plata) TN 26 Argentina (coast of Mar del Plata) BT, T 159 Australia (South Australia) GN 752 Indonesia (East Lampung) GN 545 Indonesia (East Lampung) BS, OT, BT 56 Australia (Leschenault Estuary) BS, OT, BT 76 Australia (Koombana Bay) BS, OT, BT 67 Australia (Peel- Harvey Estuary) BS, OT, BT 1,065 Australia (Cockburn Sound) BS, OT, BT 813 Australia (Shark Bay) -- 472 Pakistan (Karachi) -- 635 Pakistan (Karachi) ---- 72 Thailand (Pak Phanang Bay) BL, HP 141 Kenya (Malindi) BL, HP 108 Kenya (Malindi) BT 4,910 South Africa (Natal) HC 75 Taiwan (Tsaohu stream) HC 353 Mozambique (Inhaca Island) HC 504 Mozambique (Inhaca Island) Functional -- 1,128 Sweden (Skagerrak coast and Kattegat) -- 446 Sweden (Skagerrak coast and Kattegat) -- 812 Scotland (Shetland Islands) -- 1,025 Scotland (Shetland Islands) HC 206 Brazil (Ubatuba) HC 165 Brazil (Ubatuba) SD 315 Argentina (Bustamante Bay) BT 2,122 Portugal (Madeira) BT 1,714 Spain (Canary Islands) XLT 347 United States of America (Florida) BT, TN 3,077 Namibia BT, TN -- Namibia HC 60 Ascension Island (English Bay) BT 431 Spain (Canary Islands) BT 431 Spain (Canary Islands) HC 1,166 Chile, Argentina (Beagle Channel) BT 395 Canada (Northern British Columbia) TN 1,118 Namibia TN 221 Italy (Sardinian Sea) BT, HC 303 Argentina (Patagonian Gulfs) LR 70 France (North Western coast of Corsica) GN, TMN, 603 Egypt (Suez CN, BS, SD Canal) BT 2,384 United Stales of America (Tampa Bay) BT 2,384 United States of America (Tampa Bay) -- 192 Hawaii (Oahu) -- -- United States of America -- -- United States of America TN, BT, SD, FS 98 United States of America (Gulf of Alaska) TN, BT, SD, FS 371 United States of America (Gulf of Alaska) BT 1,061 Argentina (northern Patagonian gulfs) BMT 538 Argentina (Patagonia) -- 821 Mexico (Gulf of California) -- 1,842 Mexico (Gulf of California) OT 2,537 Brazil (Vitoria Bay) OT 318 Brazil (Vitoria Bay) OT 1,339 Brazil (Vitoria Bay) TN 504 Brazil (Guaratuba Bay) FN, BT 1,342 Turkey (Beymelek Lagoon) -- -- Chesapeake Bay BT 307 Brazil (Southeast coast) TMN, FN, 539 Turkey (Homa BS, FT Lagoon) -- -- Spain (Ria de Arousa) GN 267 Indonesia (East Lampung) BS, OT, BT 194 Australia (Leschenault Estuary) BS, OT, BT 358 Australia (Koombana Bay) BS, OT, BT 2,081 Australia (Peel-Harvey Estuary) BS, OT, BT 1,361 Australia (Cockburn Sound) BS, OT, BT 518 Australia (Shark Bay) -- 1,129 Malaysia (Sematan mangrove forest) -- 1,129 Malaysia (Sematan mangrove forest) -- 895 Malaysia (Sematan mangrove forest) BT 2,141 South Africa (Natal) -- 595 Malaysia (Sematan mangrove forest) -- 595 Malaysia (Sematan mangrove forest) -- 335 Malaysia (Sematan mangrove forest) HC 309 Taiwan (Tsaohu stream) HC 43 Taiwan (Tsaohu stream) HC 74 Trinidad (Maracas. Aripo, Arima, Guanapo valleys) Maturity Year Reference Morphometric 1974-1998 Quiles et al. (2001) 1974-1998 Quiles et al. (2001) 1996-1997 Moriyasu el al. (2002) 2001-2002 Ungfors (2007) 2001-2002 Ungfors (2007) 2001-2002 Ungfors (2007) 2001-2002 Ungfors (2007) 1999-2001 Tallack (2007) 1999-2001 Tallack (2007) 2006-2008 Varisco and Vinuesa (2011) 2006-2008 Varisco and Vinuesa (2011) 2005-2011 Biscoito et al. (2015) 2005-2011 Biscoito et al. (2015) 2005-2011 Biscoito et al. (2015) 2005-2011 Biscoito et al. (2015) 2005-2011 Biscoito et al. (2015) 2005-2011 Biscoito et al. (2015) 2000-2003 Hall et al. (2006) 2002-2003 Doi et al. (2007) 2002-2003 Doi et al. (2007) 2002-2003 Doi et al. (2007) 2002-2003 Doi et al. (2007) 2003-2005 Freire et al. (2011) 2003 2005 Freire et al. (2011) 1994 Flores and Ncgrciros- Fransozo (1999) 1994 Flores and Negreiros-Fransozo (1999) 2010-2011 Triay-Porlella et al. (2014) 2010-2011 Triay-Porlella et al. (2014) 2010-2011 Triay-Portella et al. (2014) 2010-2011 Triay-Porlella et al. (2014) 2010-2011 Triay-Portella et al. (2014) 2006-2008 Diez and Lovrich (2010) 2006-2008 Diez and Lovrich (2010) 1999-2002 Hall et al. (2006) 1983-1983 Jewell et al. (1985) 1983-1989 Abello and Macpherson (1992) 2002-2006 Baron et al. (2009) 2002-2006 Baron et al. (2009) 1992-1995 Sampedro et al. (1999) 1992-1995 Sampedro et al. (1999) 1998-1999 Lopez Greco et al (2000) 1998-1999 Lopez Greco et al. (2000) 1998-1999 Lopez Greco et al. (2000) 1998-1999 Lopez Greco et al. (2000) 2000 Cobo (2005) 2000 Cobo (2005) 1988 2003 Gerhart and Bert (2008) 1988-2003 Gerhart and Ben (2008) 1988-2003 Gerhart and Bert (2008) 1988-2003 Gerhart and Bert (2008) 2004-2007 Cobo and Alves (2009) 2004-2007 Cobo and Alves (2009) 1997-2000 Negreiros-Fransozo et al. (2003) 1997-2000 Negreiros- Fra nsozo et al. (2003) 2001 Negreiros-Fransozo and Fransozo (2003) 2001 Negreiros-Fransozo and Fransozo (2003) 1988-1989 Carsen et al. (1996) 1988-1989 Carsen et al. (1996) 1988-1993 Pinheiro and Fransozo (1998) 1988-1993 Pinheiro and Fransozo (1998) 2009-2010 Marochi et al. (2013) 2009-2010 Marochi et al. (2013) 1989-1990 Muiho et al. (1999) 1989-1990 Muino et al. (1999) 1989-1990 Muino et al. (1999) 1989-1990 Muino et al. (1999) 1989-1990 Muino et al. (1999) 1989-1990 Muino et al. (1999) n.d. Gonzalez-Gurriaran and Freire (1994) n. d. Gonzalez-Gurriaran and Freire (1994) 2006-2007 Vallina et al. (2014) 2006-2007 Vallina et al. (2014) 1997-2000 de Lestang et al. (2003) 1997-2001 de Leslang et al. (2003) 1997-2002 de Lestang et al. (2003) 1997-2003 de Lestang et al. (2003) 1997-2004 de Lestang et al. (2003) 1997-2000 Hall et al. (2006) 2004-2015 Rasheed and Mustaquim (2010) 2004-2005 Rasheed and Mustaquim (2010) 2004-2005 Rasheed and Mustaquim (2010) n.d. Overton and Macintosh (2002) n.d Overton and Macintosh (2002) 2006-2007 Hamasaki et al. (2011) 2006-2007 Hamasaki et al. (2011) 2010 Ogawa et al. (2011) 2010 Ogawa et al. 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(2008) 4AS, fourth abdominal segment width; 5AS, fifth abdominal segment width; 6AS, sixth abdominal segment width; 5/6AS, fifth/sixth abdominal segment width; AW, abdomen width; BL, baited line; BMT, beam trawl; BS, beach seine; BT, baited trap; CN, crab net; CTW, cephalothorax width; DL, dactylus length of largest eheliped; DRN, double--rig net; DSL, dorsal length of the largest cheliped; FN, fyke net; FS, fish stomach; FT, fence trap; GB, glass box; GL, gonopod length; GN, gill net; HC, hand capture; HP, hooked pole; ICW, internal carapace width; LR, laboratory reared; MD, mating depressions; MGM, male gonad maturation stage; MMS, minimum mating size; MOS, minimum ovigerous size; MS, mating scars; N, number of specimens examined; n.d., no date; NLT, Neilsen trap; OD, oviduct; OMS. ovarian maturation stage; OT, otter trawl; PRH, chela propodus height; PRL. chela propodus length; PRW, chela propodus width; RN, ring net; RLT, rock-lobster trap: S. sieve; SCW, short carapace width; SD, scuba diving; SM, sampling method; SP, sperm plugs; SPH, spermatophores; SPM, sperm; SPT, spermatids; SPTC, spermathecae; SPZ, spermatozoa; ST, shrimp trap; T, unspecified trawl; TL, thoracic length; TMN, trammel net; TN. trawl net; UJ, undifferentiated juvenilesVD, vas deferentia; Year, sampling year. TABLE 4. The relationships of SOM ([CW.sub.50]) with maximum size ([CW.sub.max]) for all cases, by sex, and for Portunidae. Equation SE n [R.sup.2] All cases (*) log[CW.sub.50] = 1.04 100 0.89 -0.37 + 1.041og[CW.sub.max] Male log[CW.sub.50] = 1.01 53 0.85 -0.28 + 1.011og[CW.sub.max] Female log[CW.sub.50] = 1.07 47 0.96 -0.35 + 1.081og[CW.sub.max] Portunidae log[CW.sub.50] = 1.32 33 0.69 -0.88 + 1.321og[CW.sub.max] (*) Maturity cases without [CW.sub.50] or [CW.sub.max] were excluded. Family with <15 cases was not analyzed. All relationships are statistically significant (P < 0.001). n, number of cases; [R.sup.2], coefficient of determination.
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|Author:||Waiho, Khor; Fazhan, Hanafiah; Baylon, Juliana C.; Madihah, Hashim; Noorbaiduri, Shaibani; Ma, Hongy|
|Publication:||Journal of Shellfish Research|
|Date:||Dec 1, 2017|
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