An Update on Reproduction in Ghost Shrimps (Decapoda: Axiidea) and Mud Lobsters (Decapoda: Gebiidea)

4.1. Gonopores and primary sexual characters

The location of the male and female sexual openings in Axiidea and Gebiidea is similar to described universally for the reptant decapods [57]. Males possess prominent gonopores on the ventral coxal segment of the fifth pereiopod, whereas females have oval gonopores on the ventral coxal segment of the third pereiopod [40, 58, 59] (Figure 3A).

Information about internal anatomy of the reproductive system is virtually nonexistent in most species of ghost shrimps and mud lobsters. Scarce information published point out that male reproductive system involves paired testes dorsally to the hepatopancreas and the intestine and is located between first and second abdominal somites, whose connection with genital openings (gonopores) is produced through a pair of translucent or whitish vas deferens [60] (Figure 3B). Secreting epithelium of the vas deferens is responsible for forming the gelatinous spermatophoric mass [61], as observed in other decapods [62]. Female sexual system is composed of paired orange or dark red ovaries (depending upon developmental stage), one ovary shorter than another, both visible through pleonal region and a pair of short and translucent oviducts linking the ovary to gonopore [59, 60] (Figure 3C). Seminal receptacle or spermathecae have not been described for any Axiidea and Gebiidea, despite attempts to find them [63]. Laboratory observations show that females of callianassid shrimps are not able to store sperm [64], as reported in most brachyuran crabs [65].

4.2. Secondary sexual characters

Males of most ghost shrimps and mud lobsters can be identified by the absence/presence and morphology of the first pleopod. The first pleopod is absent in most males of Axianassidae, Laomediidae, Strahlaxiidae, and Upogebiidae and in numerous Callianassidae [15, 16, 66, 67]. When present, the male first pleopod is uniramous and can be unsegmented as in Thalassina [68], bisegmented as in Callichirus [58], or composed of four articles as in Ctenocheles [69]. Male first pleopod in some species as Callianidea mariamartae Hernáez and Vargas, 2013, and Marcusiaxius lemoscastroi Rodrigues and de Carvalho, 1972, is morphologically similar to gonopods of Brachyura [70, 71], showing a tiny size and function totally unknown [15]. First pleopod plays an important role during the mating behavior of caridean shrimps [72] and brachyuran crabs [65]; however, their function is not clearly defined in Axiidea and Gebiidea.

Female first pleopod is present in all females of Axiidea and Gebiidea [15]. It is uniramous and consists of one article in Axianassidae, two articles in most families, or three articles in Callianassidae, with the distal part sometimes appearing as a shovel (Callianassidae) or flagellum (Laomediidae, Callianideidae) [58, 59, 66, 73]. Depending upon species, sometimes the first two pairs or all female pleopods are used for carrying the eggs during the incubation of embryos [55, 74, 75, 76]. Females use pleopods 3–5 to generate strong water currents during the spawning and so help the larvae release from the burrow [76].

Ghost shrimps constitute a promising group for growth studies because many of them show marked differences between relative growth of chelipeds of males and females during postpuberty phase. In Callianideidae and Callianassidae, for instance, males show a positive allometric growth of the major cheliped in relation to body size, whereas this morphometric relationship is isometric in females of both families [40, 77]. According to Rodrigues and Höld [78], hypertrophied chelipeds in males of ghost shrimps are often used to defend galleries against invasion from other shrimps from the same or opposite sex. Also, Felder and Lovett [51] suggest that antagonistic interactions among males of callianassid shrimps might cause a high mortality of adult males, thus creating a bias toward females in these populations. Consequently, development of extremely larger chelipeds in callianassid species not only includes morphometric changes during sexual maturity but also can provide some advantages to males, a competition for sexual partners, as were widely documented in several species of Caridea Dana, 1852 [72].

4.3. Sexual systems

Sexual system varies considerably in Decapoda. Most caridean shrimps and brachyuran crabs are gonochoric, that is, all individuals in the population exhibit separate sexes throughout their lifetime [65, 72]. Other species are sequential hermaphrodites in which the individual changes sex at some point in the life history [79, 80, 81, 82, 83, 84]. If the initial sex is male, the condition is known as protandry; the converse situation is protogyny [85]. Finally, several species have been reported as simultaneous hermaphrodites sensu Ghiselin [86], that is, an organism has both male and female sexual organs at the same time [72, 87, 88].

While the sexual system of most groups of Decapoda is well known such as Caridea [72], Astacidea [89], Anomura [90], and Brachyura [65] for most axiideans and gebiideans, the distribution of the sexes among individuals is not clear. This is because many researchers have omitted to report explicitly the sexual system of their focus species, wrongly accepting that most ghost shrimps and mud lobsters are gonochoric. Secondly, because in ghost shrimp and mud lobster studies, the sex ratio as a function of size is rarely reported, which is crucial to determine any sex changing through the ontogeny of one species [91].

Several studies conducted in Axiidea and Gebiidea species have reported morphological evidences that aim for a sexual system more complex than simply the existence of separate sexes during the lifetime of these species. For instance, in the intertidal mud lobster Upogebia major (De Haan, 1841) (Upogebiidae) and in the ghost shrimp Callichirus major (Say, 1818) (Callianassidae), male has the gonad divided in a posterior ovarian section and an anterior testicular section [92, 61] (Table 3). In both species, ovarian section produces functional oocytes. In other species of ghost shrimps and mud lobsters have been reported specimens with male and female gonopores which have been classified as intersexed (Table 3). To summarize, for 21 species of Axiidea and 12 of Gebiidea, explicit information—or strong indirect evidence—on their sexual system was available. Of these, 26 species are gonochoristic (i.e., all individuals in the population exhibit separate sexes throughout their lifetime); 2 males are hermaphrodites, and 10 species present intersexed specimens (Table 3). Considering this information and given that reproductive biology has been studied in only a small proportion of the 781 ghost shrimps and 240 mud lobsters, it can be concluded that hermaphroditism might not be unusual in these organisms.

4.4. Mating systems

Overall, monogamous decapods usually live in heterosexual pairs as a form to ensure the mating and optimize the survival [93]. In most monogamous species, disproportionate sexual dimorphism of chelipeds is not observed because sexual selection is weak given that monogamy evolved from fidelity between heterosexual pairs [94]. On the contrary, in polygamous species there is no fidelity among individuals of the opposite sex, wherefore agonistic encounters are common between adult males during the search for receptive females [72, 95]. In these species, males invest heavily in structures, such as chelipeds, that are used as armament against other potential competitors [96, 97]. Considering this information, all species of ghost shrimp and mud lobster with solitary habits and remarkable sexual dimorphism in the major cheliped are expected to be polygamous.

In the intertidal ghost shrimp Callichirus seilacheri (Bott, 1955), the burrow is individually inhabited by one male or a female (Figure 2A), and adult male develops hypertrophied chelipeds which is a potential evidence of intense male-to-male competition for sexual partners and therefore an indirect evidence of polygamy [98]. In a study conducted in Callichirus islagrande (Schmitt, 1935), an intertidal species in that males possess highly developed chelipeds [59], the egg mass of females is fertilized by multiple males which denotes polyandry [63]. In both species, the authors assume that mating occurs when the male digs a straight and almost horizontal connection from its gallery to other nearby galleries in search of a receptive female (Figure 2A), such as one that is observed in Upogebia noronhensis Fausto-Filho, 1969 [98]. Unfortunately, information about mating system in Axiidea and Gebiidea is virtually nonexistent. Further studies including behavioral experiments between male and female specimens should be carried out to investigate a possible mating system in these species.

4.5. Sexual dimorphism in body size

In general, females of ghost shrimps attain, in average, a larger body size than males such as Biffarius filholi (A. Milne-Edwards, 1878) [99], C. major [100], and Lepidophthalmus siriboia Felder and Rodrigues, 1993 [56]. Females usually invest more energy into somatic growth than males when their reproductive success depends on reaching a larger body size [101]. In decapods, such evolutionary trend is explained by the fact that fecundity in females increases with body size [74, 102, 103, 104, 105]. Supporting this assumption, fecundity in species of callianassids increase with the female size, resulting in greater production of eggs in larger females [54, 74, 75].

4.6. Egg number and egg size

The considerable variability among Axiidea and Gebiidea species in view of fecundity and egg size (Table 4) may indicate important differences in the reproductive strategy and may also reflect a latitudinal trend, as was observed in other decapods [106, 107, 108, 109, 110]. In C. seilacheri, for instance, females produce the highest number of eggs compared to those axiideans and gebiideans where data are available. However, this ghost shrimp and mud lobsters are the largest species among those listed in Table 4, and it is assumed that the area available for egg attachment increases with female size [102, 111]. When compared to a similar-sized species Upogebia deltaura (Leach, 1816) (18.9 mm CL, 5304 eggs) [50], fecundity in C. seilacheri is still substantially higher (18.6 mm CL, 9612 eggs). Moreover, this species produces considerably larger eggs (0.884 mm) than U. deltaura (0.558 mm). It is speculated that these differences in egg numbers in similar-sized species are related to the elasticity of the abdomen, which provides more space for egg attachment.

Egg size is one of the most variable parameters in decapods and offers valuable information on a species’ reproductive strategy. It is a useful indicator of the duration of embryogenesis and larval size at hatching [112]. Moreover, several studies on ghost shrimps and mud lobsters showed a clear relation between egg size and type of larval development [113, 114, 115]. Such information, however, is restricted to just a few species of both clades.