Raymond T. Bauer

Simultaneous Hermaphroditism in Caridean Shrimps: a Unique and Puzzling Sexual System in the Decapoda

The sexual system of the caridean genus Lysmata has been described until recently as protandric hermaphroditism, in which individuals change sex from male to female with increasing size. However, recent studies by Bauer and Holt (1998) and Fiedler (1998) have shown that female-phase individuals of at least two species are outcrossing simultaneous hermaphrodites, a sexual system described here as protandric simultaneous hermaphroditism (PSH). There is considerable variation in the ontogeny of protandric carideans, revealing an underlying flexibility in sex determination and development which has made PSH possible in at least some Lysmata spp. Possible costs and benefits of retention of male reproductive function in female-phase hermaphrodites are proposed. The PSH appears to be unique (to date) within the Decapoda and other Malacostraca to the caridean genus Lysmata and perhaps the related genus Exhippolysmata. It is puzzling that PSH has evolved in a group with such considerable variation in socio-ecological attributes: some Lysmata species are warm temperate, highly aggregated, with unspecialized (facultative) fish-cleaning behavior while others are tropical species, occur at low density in hermaphrodite pairs associated with sea anemones, and are specialized fish cleaners. Description of sexual systems, costs/benefits of PSH, and socioecological attributes of Lysmata, considered in the context of a phylogeny of the group, will be necessary to understand how PSH evolved in Lysmata and why it has not evolved in other groups of protandric carideans.

Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species

Summary Study of latitudinal variation in seasonality of reproduction and recruitment of benthic marine invertebrates is useful in generating and testing hypotheses about causal factors acting on reproduction such as temperature and larval food supply that might be altered by changes in world climate. Analysis of latitudinal variation in reproductive patterns might be made with comparisons (a) among species with a common phylogenetic history from different latitudes and habitats and (b) among phylogenetically different taxa from the same location. Hypotheses on variation of reproductive seasonality with latitude are tested here with results of a study on nine species of caridean and two species of sicyoniid shrimp sampled from a tropical seagrass meadow in Puerto Rico. Breeding condition was determined by the presence or absence of incubated embryos (carideans) and the state of ovarian development in both carideans and sicyoniids. Recruitment was estimated from the percentage of individuals of monthly pop...

SEX CHANGE AND LIFE HISTORY PATTERN IN THE SHRIMP THOR MANNINGI (DECAPODA: CARIDEA): A NOVEL CASE OF PARTIAL PROTANDRIC HERMAPHRODITISM

A population of Thor manningi sampled for one year was composed of 50% primary males, 49% protandric hermaphrodites, and 1% primary females. Primary males have prehensile third pereiopods, massive appendices masculinae, and life-long sperm production. Protandric hermaphrodites pass first through a male phase (non-prehensile third pereiopods, small appendices masculinae, sperm production) and a transitional phase (reduction of appendices masculinae and sperm ducts, development of female incubatory flanges, ovarian development) before maturing into breeding (embryocarrying) females.Eighty-six to 100% of females (female-phase hermaphrodites and primary females) in monthly samples carried embryos. Breeding females produced new embryo clutches approximately every nine days. Although reproduction was continuous, recruitment chiefly occurred in the summer. Measurements of density, size-specific dry weight, and cohort analysis indicate average life spans of approximately 4-5 months, production of 35 mg dry weight...

Continuous reproduction and episodic recruitment in nine shrimp species inhabiting a tropical seagrass meadow

Abstract Breeding and recruitment patterns were analysed and compared in a group of nine caridean shrimp species from seagrass meadows in a tropical locale, Puerto Rico. Embryo production took place throughout the year in populations of all species. No multispecies pattern in breeding intensity was detected. Most females sampled that carried embryos near hatching also had an ovary filled with vitellogenic oocytes ready for a new spawning. Laboratory observations on females incubating embryos confirm that they spawn again after incubated embryos hatch and the female undergoes a posthatching molt. Median period of embryo incubation ranged from 5–10 days in females of eight species maintained in the laboratory. Reproduction thus appears to be continuous in these tropical shrimps, with females producing successive broods at short intervals after they reach maturity. Increases and decreases in the smaller size classes of species size-frequency distributions suggest that recruitment intensity was variable throughout the year of sampling. Most importantly, the monthly highs and lows of recruitment strength were concordant among species with no apparent seasonal pattern. Given that larval production was continuous, the episodic recruitment pattern observed indicates that similar environmental (mortality) factors acted simultaneously on either the planktonic larvae or newly recruited juveniles of all species.

Experimental test of socially mediated sex change in a protandric simultaneous hermaphrodite, the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae)

In Lysmata wurdemanni, individuals begin benthic life in a male phase (MP) but later change to a female phase (FP) with female external morphology, but with both male and female reproductive capacity (protandric simultaneous hermaphroditism). Previous studies have demonstrated that the size (timing) of sex change varies considerably in natural populations. We experimentally tested for social mediation of sex change by rearing male-phase individuals (MPs) in both large and small social groups with different sexual and size composition. In the “large group” experiment, speed of sex change was inversely related to the abundance of female-phase individuals (FPs) in the group (sex-ratio induction). Increased allocation to female function (more rapid change to FP) may occur when male mating opportunities are lower because the simultaneous-hermaphrodite FP can immediately reproduce as a female while maintaining male mating capacity. When FPs are abundant, delayed sex change might be adaptive because the costs of female reproduction are considerable. An MP may gain reproductively by increased growth before changing to FP at a larger size (fewer but much larger broods). Size-ratio induction of sex change by small MPs was suggested but not confirmed. Experimental results from “small groups” (1–2 individuals) were qualitatively similar but not as conclusive as those from large groups. The number and complexity of social interactions in large groups may be necessary to stimulate labile sex change in this species. In L. wurdemanni, sex change may be influenced not only by abiotic factors related to breeding [Bauer (2002) Biol Bull 203:347–357] but also by social factors in certain demographic situations.

Temporal patterns of reproduction and recruitment in populations of the penaeid shrimps Trachypenaeus similis (Smith) and T. constrictus (Stimpson) (Crustacea: Decapoda) from the Northcentral Gulf of Mexico

The temporal pattern of reproduction and recruitment is described from monthly population samples (June, 1989 through November, 1990) of two penaeid shrimp species, Trachypenaeus similis (Smith) and T. constrictus (Stimpson), from an inshore location (Mississippi Sound near Horn Island) in the Northcentral Gulf of Mexico. The presence or absence of mating plugs (associated with mating and insemination) and ovarian maturity (an indicator of spawning) were used to examine breeding in adult females. Females with mature ovaries occurred in samples from April through October and November in T. constrictus and T. similis, respectively, with peak values in July to September in both species. The percentage of inseminated females fell to low or zero values in the late fall and winter, indicating a cessation of mating activity. Sexual maturity of males was indicated by fusion of the gonopodal endopods (petasma); mature males were present throughout the year in both species. Recruitment intensity was described as the percentage of juvenile individuals in monthly population samples of each species (“identifiable juveniles”). Very small Trachypenaeus juveniles, at a size closer to actual recruitment but too small to be identified to species (“unidentifiable juveniles”), were used in calculating another recruitment index based on combined monthly samples of both species. Both indices indicated that recruitment occurred throughout most of the year with no obvious seasonal pattern. The monthly spawning intensity of each species was highly correlated with water temperature at the month of sampling, indicating the possible importance of temperature as a proximate factor acting on gonadogenesis and spawning pattern. It is hypothesized that larval food supply may be an important ultimate factor or selective pressure acting on spawning seasonality in these penaeid shrimps. There were no statistically significant correlations between monthly estimates of spawning intensity and recruitment using lag periods from one to 3 months, indicating a complex stock-recruitment relationship in these species.

Life history migrations of the amphidromous river shrimp Macrobrachium ohione from a continental large river system

Abstract The hypothesis of an amphidromous life history pattern, with a female hatching migration from the river to an estuary, larval development in saltwater, and a return upriver migration by postlarvae (juveniles) was tested in the river shrimp Macrobrachium ohione in the Atchafalaya River, Louisiana, U.S.A. in 2006. A possible female migration from the river to the Atchafalaya Delta estuary (AD) to hatch incubated embryos was tested by comparing reproductive status of females sampled monthly from stations 146 km (Butte La Rose = BLR), 42 km (Berwick = BR), and 0 km from AD. Females only occurred in traps at AD only during the reproductive season (March to August) but were present throughout the year at other stations. The highest percentages of prehatching females occurred at the AD and BR stations while prehatching females were relatively rare at the upriver BLR station. Salt water requirements for larval development were tested by incubating first stage larvae from individual hatches in freshwater and saltwater (15 ppt) treatments (n = 10). The first stage (nonfeeding) larvae did not molt to second stage (feeding) larvae in freshwater, with significant mortality beginning after day 5. In saltwater, survival was high and most hatching larvae molted to stage 2 after 4-5 days of hatching. An upstream migration of juveniles began in mid-July 2006 and continued until October. Juvenile migrators were observed swimming near the surface from approximately one hour after sunset until at least early morning in a band of hundreds to thousands of individuals 1-2 m wide along the shore. Body size of migrators increased from downstream to upstream, suggesting that juveniles are feeding and growing during the migration. Hypotheses about whether formerly abundant far northern populations migrated to and from the sea are discussed. The decline of the species in the northern part of its range might be partially explained by human impacts on the juvenile migration and subsequent upstream recruitment.

Tests of Hypotheses on the Adaptive Value of an Extended Male Phase in the Hermaphroditic Shrimp Lysmata wurdemanni (Caridea: Hippolytidae)

Hypotheses on delayed sex change in the protandric simultaneous hermaphrodite Lysmata wurdemanni were tested with observations from population samples, mating experiments, and experiments on sex change under optimal and suboptimal breeding conditions. Male-phase individuals (MPs) much larger than the minimum size of sex change were most frequent in a natural population from fall through early spring. The hypothesis was tested that some MPs delay sex change to the simultaneous hermaphrodite female-phase (FP) because MPs are more competitive in obtaining copulations with parturial FPs than are FPs mating as males (MFPs). In different experiments, parturial FPs were maintained with two potential male mating partners (large MP and MFP, small MP and MFP, large MP and small MP) through the parturial molt and spawning; activities were recorded with time-lapse video. MFPs gained the single copulation with the parturial FP as frequently as MPs, large or small, but large MPs copulated with more FPs than small MPs. The hypothesis of FP reversion to large MP was tested experimentally and rejected. Rate of change of MP to FP was much lower in large MPs maintained under suboptimal (fall/winter) than optimal (spring/summer) breeding conditions. The results presented here suggest that the occurrence of large MPs from the fall to early spring is better explained by abiotic proximate factors related to breeding than by socially mediated sex change in different demographic environments.

PROTANDRIC SIMULTANEOUS HERMAPHRODITISM IN THE MARINE SHRIMP LYSMATA CALIFORNICA (CARIDEA: HIPPOLYTIDAE)

Abstract To investigate the extent of protandric simultaneous hermaphroditism (PSH) in the genus Lysmata, observations were made on the sexual system of L. californica, a species from the warm-temperate eastern Pacific. Observations on a large number of female-phase individuals (FPs) from a museum collection indicated that FPs with broods containing advanced embryos spawn again (successively) soon after brood hatching. Female-phase individuals maintained in pairs went through successive cycles of embryo brooding concomitant with gonadal vitellogenesis, hatching, molting, and spawning. Time-lapse video observations confirmed that FPs are able to copulate as males and inseminate postmolt, prespawning FPs. Prespawning FPs maintained alone did not produce successful broods of embryos. Thus, FPs of L. californica are outcrossing simultaneous hermaphrodites. Size-frequency distributions of sexual phases showed that individuals develop first in the male phase (MP) and then change to the female phase. Individuals apparently change from MP to FP in a single molt, as shown by (a) “transitional” individuals that were fully MP externally but whose ovotestes were full of vitellogenic oocytes and (b) a distinct change in the presence/absence and growth of pleopod characters from MP to FP. Female-phase individuals retain male gonopores from the MP phase, and relative growth of male ejaculatory ducts is similar in MPs and FPs. Pleopod flanges related to embryo attachment and incubation are somewhat masculinized in FPs of L. californica. The sexual system of L. californica is similar to that of L. wurdemanni from the Gulf of Mexico and L. amboinensis from the Indo-West Pacific. Protandric simultaneous hermaphroditism is probably widespread if not ubiquitous in the genus Lysmata.

Adaptations of the branchial ectoparasite Probopyrus pandalicola (Isopoda: Bopyridae) for survival and reproduction related to ecdysis of the host, Palaemonetes pugio (Caridea: Palaemonidae)

ABSTRACT Survival of the branchial ectoparasite Probopyrus pandalicola through ecdysis of the host, Palaemonetes pugio, was studied by observing infected shrimps before and after ecdysis and directly with time-lapse video. The parasite pair retained its position through 97.3% of 112 host ecdyses. This observation and positive correlations between parasite and host size support the hypothesis that bopyrid isopods remain on and grow together with their host. Video recordings of shrimp ecdysis showed that the female and male maintain their position rather than being cast off and reentering the host branchial chamber. Observations on exuviae from parasitized shrimps and from video recordings suggest that the female parasite avoids being discarded with the molt skin by immediately attaching to the newly exposed inner lining of the gill cover as the shrimp backs out of its exuviae. Reproductive activities of the parasite relative to host molting were studied. Epicaridium larvae were released from the host branchial chamber several hours to 5 days before the host molt. Spawning by the parasite female took place within several hours (median = 12 h) after host ecdysis. Expulsion of exuvial fragments of female parasites from the host branchial chamber was observed in 2 video recordings prior to spawning. In several video recordings, the usually inactive male moved from its site on the female abdomen up to and inside the female marsupium after the host molt and before female spawning, presumably to inseminate the female. Females from which males had been removed failed to produce a brood after the next host molt, tentatively supporting the hypothesis that females must be inseminated prior to each spawning.