Thanumalaya Subramoniam

Reproductive morphology and mating behaviour in the hingebeak shrimp Rhynchocinetes durbanensis Gordon, 1936 (Decapoda: Caridea: Rhynchocinetidae) in India

The present study tests hypotheses about sexual dimorphism in body size and morphology versus differential mating behaviours of three male ontogenetic stages (typus, intermedius and robustus morphotypes) of the hingebeak shrimp Rhynchocinetes durbanensis Gordon using canonical discriminant analysis. There is strong sexual dimorphism in this species, in that robustus morphotypes are greater in size and with larger appendages (extended third maxillipeds and major [first] chelipeds) than females. As typus males grow bigger in size, their third maxillipeds and major chelipeds become proportionately larger than those of females, and the numbers of corneous spines on the terminal segment of the maxillipeds are reduced. Although there is no sexual dimorphism in body size between typus and intermedius males and females, the robustus males are often substantially larger than females. During mating and spermatophore transfer, all male morphotypes performed similar behaviours (touching, overlapping and holding), but only intermedius and robustus morphotypes appeared to fertilize the broods of the females successfully. Robustus males were faster in approaching as well as mating with receptive females than subordinate males. When mating with robustus males, females spawned more quickly than after mating with typus and intermedius males. Additionally, the time taken for spermatophore transfer by typus males was longer. Rejection by females during the initial approach by typus males often resulted in unsuccessful spermatophore attachment. Results of this study suggest a dominance hierarchy in R. durbanensis similar to certain other rhynchocinetid species in which females appear to prefer mating with the larger robustus males.

New records of marine ornamental shrimps (Decapoda: Stenopodidea and Caridea) from the Gulf of Mannar, Tamil Nadu, India

Marine ornamental shrimps found in tropical coral reef waters are widely recognized for the aquarium trade. Our survey of ornamental shrimps in the Gulf of Mannar, Tamil Nadu (India) has found three species, which we identify as Stenopus hispidus Olivier, 1811, Lysmata debelius Bruce, 1983, and L. amboinensis De Man, 1888, based on morphology and color pattern. These shrimps are recorded for the first time in Gulf of Mannar, Tamil Nadu. Detailed information, including the description of specimens, habitat and distribution, is provided.

Chapter 3 – Sexual Systems

Crustaceans are well known for their unrivalled diversity of sexual systems that range from gonochorism to various hermaphroditic conditions, including a rare form of sexuality, termed androdioecy. The evolution of sexual systems in Crustacea has great relevance to the reproductive adaptation of different species to diversified ecological niches. By far, sequential hermaphroditism is the most common among the alternative sexual systems of crustaceans. In caridean shrimps, protandric hermaphroditism has given origin to another unique condition, called protandric simultaneous hermaphroditism. Protogynous reproductive pattern is prevalent among isopods, in which mate guarding habit of males is associated with the development of this sexual system. The androgenic gland plays a pivotal role in bringing about such varied sexual systems in malacostracan crustaceans. Sexual anomalies such as intersexuality and gynandromorphism are prevalent, particularly among nonmalacostracan lower crustaceans. Perturbations in hormone balance, together with variations in the environmental factors controlling sex determination are the causative agents for the appearance of such anomalous sexual patterns in the population.

Endocrine Regulation of Vitellogenesis

Although the process of vitellogenesis in Crustacea is fairly understood, hormonal mechanisms controlling the synthesis as well as uptake of the yolk proteins are still under intensive investigation. The available information, however, posits a bihormonal regulation, by the existence of an inhibitory neuropeptide in the optic ganglia as well as a variety of stimulatory hormonal factors, originating from diverse sources. Two major inhibitory neuropeptides, molt-inhibiting hormone (MIH) and gonad-inhibiting hormone (GIH), both negatively controlling molting and reproduction, are the pivotal physiological regulators in crustaceans. Several studies have been made to elucidate the mechanisms underlying the inhibitory action of GIH/vitellogenesis-inhibiting hormone (VIH) on vitellogenin synthesis in different crustacean species. Uniquely, VIH exerts its influence directly on both ovary and hepatopancreas, the two organs purportedly involved in vitellogenin synthesis. In contrast, different gonad stimulatory hormones are implicated in the positive control of vitellogenin synthesis in different crustacean taxa. They are gonad stimulatory neurosecretory hormone, secreted from brain and thoracic ganglia, biogenic amines of both stimulatory and inhibitory nature, emanating from central nervous system, methyl farnesoate, originating from mandibular organ, the molting hormone, ecdysone synthesized by Y-organ, and the vertebrate sex steroids, estradiol and progesterone, secreted from as yet undetermined sources. While discordant opinions have been expressed on their regulatory role in vitellogenin synthesis in different crustacean species, a multihormonal control of these stimulatory factors is proposed in accomplishing vitellogenic processes. Nevertheless, our present understanding on the hormonal control of vitellogenesis would bolster development of protocols to improve egg maturation in the commercially significant species, reared under controlled conditions.

Chapter 8 – Oogenesis

There is great morphological diversity in the female reproductive system, with particular reference to ovarian organization among crustacean taxa. This is reflected in the egg cell formation and the mode of yolk accumulation. Since crustaceans produce large numbers of yolky eggs, the vitellogenic system in crustaceans has evolved many modes to produce the complex yolk materials that form the substrate for the rather extended embryogenesis. In Crustacea, yolk protein synthesis is accomplished by both the primitive autosynthesis and the heterosynthesis. Apart from ovary, which produces yolk proteins in the dendrobranchiate penaeiodean shrimps, hepatopancreas is the sole yolk-synthesizing organ in many crustaceans. Besides, in peracarids, like amphipods and isopods, fat body is the central organ of vitellogenin (Vg) synthesis. Gene expression studies have revealed the genetic control of vitellogenesis, clarifying doubts about the ultimate site of Vg synthesis. Endocytotic uptake of yolk precursor proteins is mediated by membrane receptors. However, the processing of yolk proteins in crustaceans is accomplished by endopeptidases, which cleaves the single polypeptide chain of Vg into several vitellin molecules. Crustacean lipovitellin is a high-density lipoprotein, conjugated to a variety of carotenoid pigments. Vitellogenesis also includes incorporation of several inorganic ions as well as steroidal hormones into the yolk proteins to serve important functions during embryogenesis.

Chapter 6 – Sex Pheromones

One of the hallmarks of crustacean reproduction is the timing of events like mating and spawning with reference to the process of molting that continues to occur in mature adults. In other words, molting intervenes the female reproductive cycle in such a way that vitellogenesis takes place during the intermolt stage, whereas the ovulation and fertilization are relegated to postmolt stage. Such a precise sequencing of reproductive events is possible with the use of sex pheromones which play a pivotal role in bringing together both male and female to achieve successful mating and egg fertilization. In general, sex pheromones of crustaceans are of two types, the distance or olfactory pheromone and the contact pheromone. Distance pheromones are released through the urine to attract the males toward the receptive females; subsequent to molting, copulation takes place under the influence of the same or a different pheromone found in the urine. On the other hand, contact pheromone refers to the water-insoluble compounds found on the surface of the cuticle of postmolt females. Special chemoreceptor organs are employed in perceiving the sex pheromones. Recent findings identified uridine diphosphate as the chief olfactory pheromone, whereas cuticular hydrocarbons serve as the contact pheromone. The mode of pheromone action in the aquatic medium is explained.

Chapter 4 – Mating Systems

Mating system refers to the general pattern by which males and females mate within a population or species. Mating systems as well as the factors that determine them are diverse among crustaceans. The basic types of mating systems in Crustacea are monogamy and polygamy. Although different subtypes of these two mating systems are widespread among crustaceans, caridean shrimps inhabiting coral reef niches exhibit a bewildering array of mating systems. Social monogamy, defined as the togetherness of two heterosexual adults forming a social system, is more prevalent among the shrimps living in symbiotic association with sedentary-living invertebrates such as sponges. In the sponge-dwelling synalpheid shrimps, social monogamy has attained the pinnacle of complexity, leading to community living and eusociality. The conditions for the evolution of eusociality among the synalpheid shrimps are discussed.

Chapter 11 – Spermatogenesis

In Crustacea, the male reproductive system consists of the paired testes and vas deferens, the latter leading to the gonopore. Spermatogenesis occurs in the testis, whereas the sperm maturation is completed in the vas deferens. In the majority of the crustaceans, the sperm cells are enclosed in sperm packets, called spermatophores, before being transferred to the females. In the closed thelycal penaeid shrimps, the sperm undergoes capacitation in the female seminal receptacle. Crustacean spermatozoa are very diverse in their morphology, to the extent that they are useful in determining phylogenetic relationships among crustacean taxa. Common characteristics of decapod spermatozoa are (1) they are aflagellate and nonmotile; (2) acrosome vesicle is not Golgi-derived; (3) nuclear chromatin is uncondensed, and (4) mitochondria is degenerate or absent. In lower and primitive crustaceans like Remipedia and maxillopodeans, the spermatozoa are flagellate and show motility. Among the decapods, though the sperm cells lack tail, they possess variable numbers of spikes, which are, however, not homologous to the axial filamentous tail of typical sperm. The natantian (penaeiodean shrimps and caridean prawns) sperm are unistellate, whereas in the reptantians (crab, lobster, and crayfish), the sperm are multistellate. In the multistellate sperm, the spikes are extensions of nuclear materials, whereas in the unistellate sperm, the spike takes origin from the acrosomal region. Spermatogenesis in crustaceans is under the negative control of gonad-inhibitory hormone of the eyestalk ganglia. On the other hand, androgenic gland hormone has a positive influence on the spermatogenesis in malacostracans. Participation of other hormones such as methyl farnesoate, molting hormone, biogenic amines, and vertebrate-type steroids in the control of male gamete formation is possible but has not been investigated.

Yolk Utilization and Embryonic Nutrition

Excepting a few free-spawning crustaceans, the majority of them incubate their eggs in the pleopodal brood. This necessitates the accumulation of large reserves of organic substrates to meet the demands of protracted embryogenesis. Crustacean eggs contain large reserves of proteins, lipids, and carbohydrates in the form of a complex yolk protein. Hence yolk utilization is the central event of embryogenesis and is accomplished by a host of hydrolytic enzymes. Although lipids and proteins are the major components of the yolk, there is difference in their preferential use during embryogenesis. In general lipid forms the energy source for the embryonic as well as larval development. In addition, crustacean yolk protein characteristically contains a variety of carotenoid pigments. Significantly, β-carotene and astaxanthin undergo several metabolic changes to give rise to many intermediate pigment species. Astaxanthin is finally esterified to new pigmentary compounds. Embryonic ecdysteroids conjugated to lipovitellin molecules are released at specific stages in embryogenesis to trigger embryonic cuticle formation and molting.

Reproductive Cycle and Environmental Control

Environmental factors like seawater temperature, photoperiod, and salinity are known to control the reproductive cycle of marine crustaceans. In general, tropical species breed continuously throughout the year, whereas the temperate species breed annually, concentrating their reproductive activities to the warm summer months. For example, the mole crab Emerita asiatica breeds continuously in the tropical waters of Madras (Chennai) coast, India. On the other hand, species such as Emerita analoga and Emerita talpoida inhabiting the west and east coasts of the United States breed annually in the temperate seas. In addition, semiannual breeding cycles are found in tropical environments coming under the influence of seasonal monsoon rains. Different methods employed in the determination of the reproductive cycle are described. Some of the lower crustaceans such as the water flea, Daphnia magna , are increasingly used to test the toxicity of aquatic contaminants and pollutants. Most of them are endocrine disruptors, impairing the normal reproductive processes. The adverse effects of climate change factors like rising seawater temperature and ocean acidification on reproduction, larval development, and dispersal are discussed.