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

11 Pages·2002·5.2 MB·

by  Raymond T Bauer

Reference: Biol. Bidi 203: 347-357. (December 2002)
Tests of Hypotheses on the Adaptive Value of an
Extended Male Phase in the Hermaphroditic Shrimp
wurdemanni
Lysmata (Caridea: Hippolytidae)
RAYMOND BAUER
T.
Department of Biologv, University ofLouisiana at Lafayette, Lafavette, Louisiana 70504-2451
Abstract. Hypotheses on delayed sex change in the pro- Introduction
tandric simultaneous hermaphrodite Lysimitu wurdemanni
were tested with observations from population samples, Many organisms, both plant and animal, partition repro-
mating experiments, and experiments on sex change under ductive output into male and female components. Such sex
optimal and suboptimal breeding conditions. Male-phase allocation may occur before fertilization or during embry-
individuals (MPs) much larger than the minimum size of onic development. In hymenopteran insects (ants, wasps.
sex change were most frequent in a natural population from bees), haplodiploid sex determination allows females to
fall through early spring. The hypothesis was tested that produce male and female offspring in variable proportions
some MPs delay sex change to the simultaneous hermaph- (Wilson, 1976; Thornhill and Alcock, 1983). In turtles and
rodite female-phase (FP) becauseMPsare more competitive some other reptiles such as alligators, sex determination is
in obtaining copulations with parturial FPs than are FPs temperature dependent, so that females may control the sex
mating as males (MFPs). In different experiments, parturial ratioofoffspring by the seasonal timing ofegg laying orthe
FPs were maintained with two potential male mating part- location of nests (Bull, 1980; Ferguson and Joanen. 1982).
ners (large MPand MFP. small MPand MFP. large MPand Higher male fetal mortality may occur in mammalian fe-
small MP) through the parturial molt and spawning; activ- males under stressful conditions, resulting in female-biased
ities were recorded with time-lapse video. MFPs gained the litters (Wilson, 1976; see also Charnov, 1982). In other
single copulation with the parturial FPas frequently as MPs. organisms, sex allocation many occurafterbirth orhatching
large or small, but large MPs copulated with more FPs than in the sexually mature organism. Simultaneous hermaphro-
small MPs. The hypothesis ofFPreversion to large MP was dites may vary resources to male and female gamete pro-
tested experimentally and rejected. Rate ofchange ofMP to duction (Charnov, 1982). In sequential hermaphrodites, sex-
FP was much lower in large MPs maintained under subop- uianldivfiudnucatlifoinrstirseppraordtuicteisonaesdonoentsoegxenaentdictahlelnythbeeoctahuesre(saenx
timal (fall/winter) than optimal (spring/summer) breeding
changers; Ghiselin, 1969; Warner, 1975; Charnov, 1982;
ccounrdrietnicoenso.fTlharegereMsPulstsfprroemsetnhteedfalhletroeesaurglgyessptritnhgatisthbeetotce-r rPoodliitciasnmskiys,f1o9u8n2d).inSimmaunlytapnleaonutstaaxnad, sienqumeonsttiailnvheerrtmebarpaht-e
explained by abiotic proximate factors related to breeding groups (except insects), and in many fishes (Chan and
than by socially mediated sex change in different demo- Yeung. 1983; Ross. 1990). The direction of sex change
graphic environments. (female to male; protogyny; male to female; protandry) is
fairly well explained by the size-advantage model (Ghiselin,
Received 16 April 2002; accepted 6 September 2002. 1969). especially in fishes and crustaceans, two groups in
E-mail: [email protected] which sequential hermaphroditism is relatively common
Abbreviations: AG. androgenic gland; CL,carapace length; ESD. envi- (Warner. 1975). What is notoften wellexplained, especially
rhoenrmmeanptharlodistexeidnetLeyrsmmiantaatiownu;rdFePm.anfneim)a:leM-Pp.hamsaelei-npdhivaisdeuailndi(vsiidmuuallt:aMneFoPu,s in decapod shrimps, is variation in the timingofsex change.
a FP acting as a male mating partner; PFP, parturial FP: PSH. protandric i.e., the amount of time spent as male and female.
simultaneous hermaphroditism; TR, transitional individual. Protandric hermaphroditism occurs in several genera and
347
348 R. T. BAUER
families ofcaridean shrimps (Bauer, 2000). In the simplest hand, a male changing to female later in life would begin
form of caridean protandry, all individuals develop first as female production with larger broods, since female fecun-
males andthen laterchange to breeding females. The sexual dity is correlated with size in carideans including Pandalus
system may be more complex, with a mixture in the popu- spp. (Bauer. 1991; Bergstrom. 2000). However, a later
lation of primary females, which develop only as females, change to female might cause the loss of female breeding
and protandric individuals, as in Pandalusjonlani, P. bo- for an entire season, given only one brood per year, thus
realis. P. eons, P. montai>ui, and P. danae (Butler, 1980; countering the fecundity advantage oflatechangetofemale.
Bergstrom, 2000). In other species, the population may The relative proportions of males and females in the popu-
consist of protandric individuals and primary males, indi- lation, perceived by an individual through social interac-
viduals that never change to females, as in Thor manningi tions, would serve as the environmental factor stimulating
(Bauer. 1986) and Athnnas kuminatocnsis (Nakashima, or inhibiting male change to female.
1987). However, the hypothesis of ESD in Pandalus danae was
Throughout the last century, Lysmutii seticaudata was rejected by Marliave et al. (1993) after they conducted
described as a completely protandric species (Spitschakoff. extensive experiments involving the rearing ofa large num-
1912; Dohrn, 1950; Charniaux-Cotton and Payen, 1985). berofyoung males in different demographic environments.
Smaller individuals have external male characteristics, but They concluded that the sexual composition of the popula-
the gonads are ovotestes with immature oocytes in the tion has no effect on sex determination (change) in this
ovarian region. With increasing size, individuals lose exter- protandric species. Other mating and rearing experiments
nal male characters and change to breeding females that led Marliave etal. (1993) to conclude that the timing ofsex
incubate embryos. Unlike other protandric carideans, the change was under genetic control. They proposed that any
female-phase individuals (FPs) retain the male ducts and adaptive change in the proportions ofsexual morphs would
testicular portion of the ovotestes, and sperm production occur by between-generation selection on sexual genotypes
continues (Berreur-Bonnenfant and Charniaux-Cotton, rather than a within-generation, socially determined re-
1965; Charniaux-Cotton. 1975). The ability of L. seticau- sponse as proposed by Charnov et al. ( 1978) and Charnov
data FPs to function as males was not addressed in these (1981). Bergstrom (1997). on the basis of results of a
studies. However, FPs of Lvxinata wurdemanni (Bauer and demographic analysis, concluded that the variable type and
Holt, 1998) and L. wnhoim'nsix (Fiedler, 1998), with sexual size ofsex change in Pandalus borealis was best explained
changes during ontogeny similar to L. seticaudata, mate as by frequency-dependent selection on genotypes for sex
males and fertilize other FPs, although they are unable to change at different ages (sizes). According to this hypoth-
fertilize themselves. They are functional, outcrossing simul- esis, different combinations of mortality, recruitment, and
taneous hermaphrodites. Bauer (2000) termed this sexual growth favor different sex-change genotypes. Conover and
system "protandric simultaneous hermaphroditism" (PSH). Munch (2002) showed experimentally in the fish Menidia
in which male-phase individuals (MPs) function only as menidia (Atherinidae) that size-dependent selection, like
males, but FPs are functional simultaneous hermaphrodites. that acting on commercially fished populations, lowers the
Morphological and behavioral observations on these and age of sexual maturity. Charnov et al. (1978) and Charnov
other Lvsmata spp. indicate that PSH is widespread in the ( 1981 ) reported adecrease in the size (age) ofsex change in
genus (Bauer. 2000, 2001). fished pandalids. This might result from size-related mor-
The size (age) ofsex change in protandric species may be tality (selection) (Conover and Munch. 2002) rather than
variable (Charnov etal., 1978; Charnov, 1981; Charnov and from an adaptive response (decision) by individuals to de-
Anderson, 1989; Bergstrom, 1997. 2000). The size of sex mographic changes in the population. On the other hand,
change may be a phenotypically flexible trait governed by Zupo (2001) clearly showed that seasonal variations in diet
the demographic environment in which an individual occurs of newly recruited shrimps determine whether or not sex
(environmental sex determination, or ESD; Charnov et al.. change takes place in the protandric shrimp Hippolyte in-
1978; Charnov, 1981; Charnov and Anderson. 1989). In ennis.
Piimliilus spp, for example, a male in a population with In Lvsnuita \vunlcuuinni. individuals from a natural pop-
abundant females might gain more inseminations by delay- ulation vary in size from 3-14 mm carapace length (CD
ing change to female because males can potentially insem- (Bauer and Holt, 1998; Bauer. 2002). Individuals enter the
inate several females during the breeding season. A Panda- population as MPs and can change to FPs at a size as small
lus female, in contrast, produces only one brood per year. as 6 mm CL; the majority change by 7.5 mm CL. However,
When females are not abundant in the population, a male there is frequently considerable overlapbetween MPand FP
might benefit by early change to female because insemina- size-frequency distributions. Many MPs do not change sex
tion of a female's brood ofeggs is assured. As a male, the until a much larger size, with some MPs becoming as large
individual would have to compete with numerous other as the larger FPs (Bauer and Holt. 1998; Bauer. 2002).
males to inseminate one ofthe scarcerfemales. On the other Some MPs might never change to FP, although all are
EXTENDED MALE PHASE IN A HERMAPHRODITIC SHRIMP 349
morphologically capable ofdoing so (Bauer and Holt, 1998; maintaining (a) FPs and (b) MPs capable of sex change
Bauer. 2000; Lin and Zhang, 2001 1. Bauer and Holt ( 1998) under suboptimal (nonbreeding season) and optimal (breed-
and Bauer (2000, 2001) suggested that delayed change to ing season) conditions.
the reproductively advantageous FP, a simultaneous her-
maphrodite, might be selected for in certain demographic Materials and Methods
situations if large MPs were competitively superior to FPs
(mating as males) and small MPs in inseminating FPs near Population samples and live specimens were collected
spawning. Lin and Zhang (2001) reared MPs of L. wurdc- from a population of Lysmata wurdemanni inhabiting the
iiiiiiini singly and in groups of from 2 to 10 individuals, rock jetty at Mustang Island, Port Aransas, Texas (27 50'
finding that change to FP increased with increasing MP N, 97 03' W). Collection was during low tides at night
group size. Replicate size was quite small in this experi- (Bauer, 2002): when tides are lower than 0.5 ft mean sea
ment, varying from 2 to 9 replicates per treatment. The level, the rock ledge and tidepool habitats of these shrimps
authors concluded that these results demonstrated social are exposed, and the shrimps are active at night, moving out
control of sex ratio. Furthermore, they proposed that per- into pools and the perimeter of the jetty rocks where they
sistence of MPs in some treatments suggested a mating can be taken with dipnets. Hand dipnets were used to take
advantage for large MPs in certain demographic situations. the shrimps from tidepools; long-handleddipnets were more
Other explanations are possible for large MP size in effective in sweeping deep under rock ledges. All nets had
Lysmatii wurdemanni. Large MPs might be FPs that have a I-mm mesh and were effective in collecting the smallest
reverted to the male phase. Bidirectional sex change is (= newly recruited) individuals of the population (Bauer.
known in some animals, such as gobiid fishes (Munday, 2002). In any particular location, groups of individuals
2002) and polychaetes (Berglund, 1986). A secondary showed no apparent segregation by sexual morph or size,
change back to male purportedly takes place in some fe- and the samples are assumed to represent a random sample
males of the protandric alpheid At/minis indicns (Suzuki, of the population. Population samples were taken monthly
1970). In L. wurdemanni, abiotic factors related to female from June 1999 through June 2000, and then bimonthly
breeding might account for the seasonally related occur- from August 2000 through June 2001 (Bauer, 2002).
rence of large MPs. The largest MPs. including transitional Shrimps collected in population samples were first pre-
MPs changing to FP, are found in winter and early spring served in ]Q% seawater formalin and later transferred to
(Bauer, 2002). Suboptimal conditions for breeding (lower 70% ethanol for permanent storage. Live specimens for
water temperatures, short daylength) and presumably larval experiments were collected separately frompopulation sam-
survival (planktonic food supply) occur during the late fall ples and transported in sealed collecting bags containing
through early spring in this primarily tropical species stud- seawater oxygenated just before the 8-10-h trip from the
ied near the northern edge of its range (Bauer and Holt. collecting site to the home institution.
1998; Bauer. 2002). Abiotic environmental conditions un- Sexual morphs were identified and classified as in Bauer
favorable for female breeding might cause a decrease in and Holt (1998). Male-phase individuals (MPs) have cin-
female hormone levels, resulting in a shift in female/male cinnuli (coupling hooks) on pleopod 1 endopods and appen-
hormones in favor of the male system. Female-phase indi- dices masculinae on pleopod 2 endopods. Transitionals
viduals, with both male and female reproductive systems, (TRs) are MPs in which the ovarian portion ofthe ovotestes
might molt back into a male phase, with male external sex is filling with vitellogenic oocytes, which is easily observed
characters. Alternatively, suboptimal breeding conditions through the carapace in living and preserved specimens. At
might delay change to FP in MPs that reach the size ofsex the next molt, TRs change to FPs and spawn for the first
change during the fall, resulting in growth to the very large time. Female-phase individuals (FPs) lack pleopod 1 cin-
MPs observed by Bauer (2002) in the late winter and early cinnuli and appendices masculinae. They are typical carid-
spring. ean females in external morphology, and they brood em-
The objective of this study was to examine components bryos. However, they can mate as males (simultaneous
of hypotheses explaining the presence of large MPs in hermaphrodites) (Bauer and Holt. 1998). As in females of
Lysmata wurdemanni. The male mating abilities of large othercarideans, FPsofL. wurdemanninearspawning (ovar-
MPs, small MPs. and FPs were compared to determine the ian portion of gonad full of vitellogenic oocytes) become
possible male mating advantages of delayed sex change. receptive to mating immediately after a prespawning (par-
The presence oflarge MPs might alternatively be explained turial) molt (Bauer and Holt, 1998; Bauer and Abdalla.
by factors not related to the sexual composition of the 2001). As in other carideans, the male deposits an external
population and socially determined sex change. The possi- spermatophore on the underside of the female, and there is
ble effects ofseasonal abiotic factors unfavorable to female no sperm storage (Bauer. 1976: Bauer and Holt, 1998). In
breeding resulting in either (a) reversion of FPs to large this report, FPs very near or just completing the parturial
MPs or (b) delayed MP change to FPs were examined by molt are termed parturial FPs (PFPs).
350 R. T. BAUER
Mating experiments tested the hypothesis of no differ- toperiod of 14-h day: 10-h night. Shrimps were fed shrimp
ence in male mating ability among FPs (mating as males = pellets daily.
MFPs), small MPs, and large MPs. In three experiments, The hypothesis that FPs may revert to large MPs was
competition for inseminating the PFP was between a large tested by an experiment in which FPs were maintained
MP and a MFP. a small MP and a MFP, and a large MP and underfavorable and less favorable breeding conditions for9
a small MP. Parturial FPs near the prespawning molt were weeks. In the "optimal" treatment (2 September through 2
identified by gonad condition (vitellogenic oocytes filling November. 2000), 50 FPs with embryos were maintained in
the cephalothoracic space behind the eyes and above the groups of 10 individuals occupying 38-1 aquaria at a water
cardiac stomach) and developmental state of brooded em- temperature, controlled by aquarium heaters, of26 C and a
bryos (near hatching, with large eyes and little or no yolk). photoperiod of 14-h light: 10-h dark. In the "suboptimal"
MFPs carried embryos but, unlike PFPs, were not close to a treatment (22 Septemberto24November, 2000). another50
parturial molt. Small and large MPs were defined as MPs < FPs with embryos were similarly maintained except without
6.5 mm CL and > 6.5 mm CL, respectively. The size of6.5 heaters so that water temperatures would be cooler than
mm CL was chosen to define "large" MP because MPs can those in the optimal treatment. The ambient temperature of
change to FPs above this size (Bauerand Holt, 1998; Bauer, the aquatic laboratory during this period was 19 C; the
2002). photoperiod was set at 10-h light: 14-h dark. Prior to the
In each replicate, a premolt PFP was placed with two experiment, individuals used in both treatments were main-
potential mating partners. The median duration of repli- tained at a salinity of33-36 ppt and an optimal temperature
cates, from placement of individuals into the experimental (26 C) and photoperiod (14-h light: 10-h dark). They were
chamber until spawning by the PFP, was 2days (1-9 d. n = fed daily, and the aquarium water was partially changed
90). The MP or MFP that copulated with and inseminated weekly. To reduce cannibalism of newly molted shrimps,
the PFP was identified from time-lapse video recordings. which was an observed source of mortality during this
Replicates in which the PFP copulated with more than one experiment, small concrete block shelters were placed in
male mating partner (4 of 94 replicates) were not included each aquarium for this thigmotactic species. Molts (exuvi-
in the data analyses. In all other replicates, there was only a ae) readily visible in the aquariawereremovedandrecorded
single copulation, except for one replicate in which a MFP daily. Absolute counts of molts were not feasible because
copulated twice with the PFP. Spawned PFPs were main- (a) the shrimps may pick apart and eat some exuviae before
tained alive for 5 days to determine ifthe attached brood of they are observed, and (b) other exuviae are hidden by
eggs had been fertilized and contained developing embryos shelters and aquarium tubing and could not be observed
(Bauer and Holt, 1998). without majordisturbance ofthe aquarium environment. At
Replicates of mating experiments were conducted in the end of the experiment, all individuals were preserved
aquariapartitioned intoaspace 20cmwide X 25 cm long X and checked for sexual condition.
15 cm high to allow for sufficient magnification using the The hypothesis that sex change of large MPs to FPs is
CCD surveillance video camera, which was equipped with greater under optimal (spring/summer) than suboptimal
an 8-mm lens sensitive to both low-intensity white and (fall/winter) breeding conditions was tested with an exper-
infrared light. Activities were recorded with a time-lapse iment using a setup similar to that just described for the
video at a speed of 5 pictures per second (24-h recording previous experiment. The MPs used in both treatments (all
mode). Fluorescent and infrared (880 nm) lamps provided nontransitional) were maintained at optimal temperature
day and night illumination, respectively. In replicates with a and photoperiod priorto the beginning ofthe experiment. In
large and a small MP, individuals had to be marked to the optimal treatment (n = 46 MPs), watertemperature was
distinguish between them in videotapes, especially at night maintained with heaters at 26 C, and photoperiod was 14-h
when most mating occurred. Small pieces ofreflective tape light: 10-h dark. In the suboptimal treatment (n = 45 MPs),
were fixed with cyanoacrylate glue on the carapace of one coolerwater temperatures were obtained by not using water
MP and the posterior abdomen of the other, with position heaters, with water temperature following the ambient air
assigned at random. No marking was needed in replicates temperature of the laboratory, which was not under control
with a MP and a MFP because the latter could be identified of the investigator. The experiment was begun when a
by its brood ofembryos. After hatching ofembryos priorto decrease in ambient laboratory temperature was predicted
the mating molt, the PFP was identified by the absence of from outside weather conditions. Water temperature in the
embryos and the presence of vitellogenic ovotestes. Reflec- suboptimal treatment was 23 C at the beginning of the
tive tape, embryo broods, and vitellogenic gonads show experiment and decreased to 18-19 C (weekly median
=
clearly on videotapes recorded with infrared (nighttime) temperature 20 C): photoperiod was 10-h light: 14-h
illumination. As in Bauer and Holt (1998), shrimps were dark. After 14 weeks (20October2001 to 23 January 2002).
maintained prior to and during experiments at water tem- the laboratory air temperature and thus the water tempera-
peratures of 25-28 C, salinities of 33-36 ppt, and a pho- ture ofthe suboptimal treatment began to rise. Heaters were
EXTENDED MALE PHASE IN A HERMAPHRODITIC SHRIMP 351
then placed in aquaria of the suboptimal treatment to in-
crease water temperature to that of the optimal treatment,
and photoperiod was changed to 14-h light: 10-h dark,
simulating a change from fall/winter to spring/summercon-
ditions. Theexperiment then continued foranother8 weeks.
The shrimps were maintained and checked for molts as in
the previous experiment. Male-phase individuals that
changed to FP (brood ofembryos observed) were removed
from the experiment and preserved. When only one MP
remained in an aquarium, it was removed when it reached
the late transitional stage (mature vitellogenic ovotestes),
with the assumption that it would have transformed to FP at
the next molt. This was done because it could not have
produced a brood of embryos (visible evidence of sex
change) upon molting to FP without a mating partner.
Results
Occurrence oflarge MPs
Large MPs. denned as MPs > 6.5 mm CL. composed
17.6% to 100% of the MP population (Fig. 1 ). with higher
proportions of large MPs in the fall through early spring
largeMPs Jun 99 -May00
100
-,
22
5 Jun Jul Aug Sept Oct Nov Dec Jan Feb Mar Apr May
Jun 00 -Jun01
352 R. T. BAUER
Table 1
Sizedataforpotentialmale matingpartnersplaced with newly molted
parturialfemales in mating experiments
Potential Male Mating Partners
Experiment
EXTENDED MALE PHASE IN A HERMAPHRODITIC SHRIMP 353
this time, the two MPs ofthe original optimal treatment had
not changed sex (verified by examination of pleopods after
preservation). In the suboptimal treatment, after 6 weeks
without any sex change and 3 weeks after the switch to
optimal conditions, MPs began to change and continued to
do so until the experiment was terminated (Fig. 5). In the
last 8 weeks, 10 of 17 had changed to FP, while 2 others
were late-stage transitionals (close to FP change) when
removed from the experiment. Three ofthe original MPs in
the suboptimal experiment remained, including one mid-
stage transitional. Two others died during the last 8 weeks
of the experiment.
At the beginning ofthe experiment, the mean size ofMPs
= =
in the suboptimal (n 45) and optimal (n 46) treat-
ments was equal (7.5 mm CL; t test, P = 0.80) (Fig. 6).
The size of FPs (sex-changed individuals) was compared
mm =
between the suboptimal (9.2 CL; n 33) and optimal
mm =
treatments (9.1 CL; n 40) (Fig. 6), and the hypoth-
esis ofno difference is accepted (/test, P = 0.58). The size
of FPs from the suboptimal treatment that transformed in
= mm =
9 10 11 12 13 14 weeks 14-22 (mean 9.4 CL, n 10) was slightly
larger than that of FPs from the optimal treatment (Fig. 6),
27 T but the means of these two groups are not significantly
different (t test, P = 0.14).
r? 25 -
Discussion
23 -
raQc. 21 - This study addressed components ofdifferent hypotheses
about the timing and degree of sex change in Lysmata
Oi 19 - wurdemanni that might explain the presence of large MPs
(male-phase individuals) in this species. Lysmata spp. have
17 12345
7 8 9 10 11 12 13 14 a unique protandric sexual system in which sex-changed
Week "females" (FPs) retain the ability to mate as males that is,
are simultaneous hermaphrodites (Bauer, 2000). The size
conFdiigtuirones4.(treCahtamnengtes)ofdulrairngge M1P4sweteokFsP.s(uAn)deCrumoupltaitmailveanpderscuebnotpatgiemaolf (age) of change from MP to FP might be socially deter-
large MPs changed to FP; (B) relative molting rates; (C) water tempera- mined, resulting in considerable variation in sex change in
tures.
the molting frequency, the average individual in the optimal 100 -r
treatment molted every 3.2 weeks versusevery 7.7 weeks in $
the suboptimal treatment. Thus, during the first 14 weeks of a 80 -
the experiment, an average individual underwent at least 4
60
molts in the optimal and 1.8 molts in the suboptimal treat-
ment.
After 14 weeks, only 2 MPs remained in the optimal 40 -
treatment, but there were still 17 MPs in the suboptimal
20
treatment. There had been no change to FP in the subopti-
mal treatment for 3 weeks (Figs. 4A, 5). At this time, the o
ambient laboratory temperature ofthe suboptimal treatment 10 13 16 19 22
began to rise (Fig. 4C). To simulate a switch from subop- Week
timal (fall/winter) tooptimal (spring/summer) breedingcon-
ditions, the temperature and photoperiod of the suboptimal durFiinggur2e2 5w.eekCsh,afnigrset uonfdelrargseubMopPtsimtaolFtPesmpeirnatthueresuabnodptpihmoatlopterreiaotdmefnotr
treatment was changed to equal that of the optimal. The 14 weeks (as in Fig. 4A) and then after a change to optimal conditions
experiment was followed for another 8 weeks. At the end of (arrow) forthe next 8 weeks.
354 R. T. BAUER
10 small, and (b) whose reproduction as a female is not only
10 33 assured but, given spawning every 2 weeks, would be more
?95-
productive if change to FP occurred as early in life as
t morphologically and physiologically possible. In a popula-
85 45 46 tion with few FPs, large MPs would have the mating ad-
vantage over small MPs, but there would be few FPs to
Q. exercise that advantage with. In a population with abundant
275-
FPs. large MPs would have more parturial FPs to mate with,
but also more FPs, mating as males, to compete with forthe
same parturial FPs. Not surprisingly, the percentage oflarge
MPs in the population was not significantly correlated with
MP MPOptimal FP FPOptimal FP either low or high percentage of FPs. These results are not
Suboplimal Suboplimal Subopttmal
(all22 (last8 concordant with a hypothesis of socially determined sex
Treawtemekesn)ts weeks) change in L. wurdemunni. However, only large-scale exper-
iments in which sex change in different demographic envi-
ninudmFiibvgieudruraeolfs6i.n(dFiPvSsii)dzueaisnlsotfihseMgiPlvasergnebaebgMoiPvnenitenoagcFhePxgprseoeruxipm.ceEhnratrnogarenbdaerxospferrseipemrxee-nsctehn.atnToghneeed wrhoentmheenrtsorisnomtesaoscuiraleldy cmaendiagtievde EaSdDefoincictuersaninswLe.rwuarbdoeu-t
standard deviation. munni or other Lysmata spp. Based on such large-scale
experiments and parentage studies. Marliave et ai (1993)
rejected the hypothesis ofsocially determined sexchange in
different demographic environments, as hypothesized for the protandric hermaphroditic shrimp Pandalus danae.
protandric pandalid shrimps (termed environmental sex de- The hypothesis that FPs may change back to MPs in
termination, or BSD; Charnov et ai, 1978; Charnov. 1981; Lvsmuta undercertainconditions, accounting forlarge MPs.
Charnov and Anderson, 1989). In ESD, the frequency of was suggested by the anecdotal observations of colleagues
sexual morphs in the population (demographic environ- rearing L. wiirdenumni and by work on Atlumas indicus
ment), presumably perceived by contacts among individuals (Suzuki, 1970) in which reversion ofprotandric FPs to MP
(socially mediated), influences the size and age at which was reported. Control of sexual differentiation by the an-
males change to females. Delayed sex change might be drogenic glands (AG), located on the distal vas deferens
advantageous to males in populations in which females are (ejaculatory duct), has been demonstrated in various mala-
abundant. A sexually successful male might inseminate costracan crustaceans (Charniaux-Cotton and Payen, 1985;
several females during the same period in which a female Hasegawa et nl.. 1993). Both males and females have pri-
can produce only onebrood ofeggs, although thoseeggs are mordia of the AG, but its development in genetic males
assured of fertilization by males. causes growth of male external characters and testes. How-
However, "females" (FPs) of L. wurdemunni are simul- ever, it is still not established that AG hormone is the only
taneous hermaphrodites that can mate as males (Bauer and factor controlling sex differentiation in Crustacea (Sagi et
Holt, 1998). The delayed sex change ofMPs would only be til., 1997). Study of AGs in caridean shrimps is limited.
adaptive, under an ESD hypothesis, iflarge MPs had a male Disappearance ofthe AGs afterchange to the female phase
mating advantage over the hermaphroditic FPs (Bauer and was reported, on the basis of stereomicroscopical and his-
Holt, 1998; Bauer, 2000). In this study. I tested the relative tological observations, in L. seticaudata (Berreur-Bonnen-
male mating success of MPs and FPs by presenting a fant and Charniaux-Cotton, 1965). In L. amboinensis, Fied-
parturial FP simultaneously to a pair of potential male ler ( 1998) reported an absence of AGs in FPs, but neither
mating partners. Surprisingly, MFPs (FPs mating as males) similar histological examination nor other observations on
were just as competitive as MPs, both large and small, in MP androgenic glands was given forcomparison. However,
obtaining copulations from parturial FPs. Although these as in L. wurdemunni, male ducts with sperm production are
experiments demonstrated no male mating advantage of retained in FPs ofboth species. Fiedler (1998) showed that
large MPs over FPs, large MPs were more successful than FPs ofL amboinensis, like those ofL wurdemanni, mate as
small MPs in obtaining the copulation of parturial FPs in a males and inseminate prespawning FPs. A small number of
competitive situation. If FPs were not simultaneous her- L. wunleiminni FPs show external male characters (reduced
maphrodites and thus could not mate as males, the superi- appendices masculinae) (Bauerand Holt, 1998). Obviously,
ority oflarge MPs over small MPs in inseminating parturial male function is maintained. Hormones maintaining male
FPs would agree with an ESD explanation of delayed MP characters in FPs might still be produced by remnants of
change to FP. However, there is no obvious benefit (selec- AGs retained from the MP stage but overlooked in histo-
tion pressure) favoring delayed change ofa MP to a FP (a) logical studies. There must be abalance ofmale and female
whose male mating ability is equal to that ofMPs, large and hormones in the FPs that allows simultaneous male and
EXTENDED MALI: PHASE IN A HERMAPHRODITIC SHRIMP 355
female function. Therefore, the possibility of change from cycles, sufficient opportunity for reversion to the male
FPs back to large MPs was tested in this study. phase, which did not, however, occur.
In the FP to MPsex change experiment, one groupofFPs The high relative abundance of large MPs from fall
was maintained under optimal breeding conditions of high through early spring might be bestexplained by suppression
water temperature and long day length (Bauer and Holt. of sex change to FPs because of suboptimal breeding con-
1998: Lin and Zhang. 2001 ) approximating those found in ditions. In the fall, MPs that have grown to and beyond the
late spring and summer at the collecting site (Bauer. 2002). minimum size of sex change may not transform as they
Given the hypothesis of socially mediated ESD proposed enter a period ofthe year not favorable for embryo produc-
for pandalid shrimps (Charnov. 1981 ). reversion to MP. if tion and larval survival. The proximate factors that retard
physiologically possible, might be expected in an all-FP sex change may be seasonally related environmental con-
group under optimal breeding conditions. However, mating ditions such as lower temperature or shorterday length. The
experiments in this study showed no strong selective advan- change of large MPs to FPs was much higher in conditions
tage for large MPs in a population with abundant FPs, and simulating spring/summer than in those simulating fall/
no reversion to the male phase was observed in the treat- winter conditions. Nearly all large MPs changed to FPs in
ment with optimal breeding conditions. the optimal treatment during the first 14 weeks of observa-
The suboptimal treatment tested the possibility that FPs tion. There was much less change to FP during the same
exposed to less favorable breeding conditions, such as lower time period (14 weeks) when MPs were maintained under
water temperatures and short day length, might revert to suboptimal (fall/winter) conditions. Molting rates were
large MPs. In many caridean species, females molt out of lower, but MPs of sufficient size to change to FP require
"breeding dress" (characters related to spawning and incu- only one molt cycle to do so (Bauer and Holt. 1998). The
MP
bation) outside ofthe breeding season. In the simultaneous average in this treatment molted twice during the first
hermaphrodite FP of L. wurdemanni. it was hypothesized 14 weeks.
that suboptimal breeding conditions might tip the balanceof After 14 weeks, the conditions of the suboptimal treat-
male/female hormones away from the female phase back to ment were changed to those of the optimal treatment to
the male phase. The FPs in this treatment were exposed to determine if the slower rate of sex change could be in-
water temperatures and a photoperiod approximating late creased in the surviving MPs. After 3 weeks (6 weeks
fall through early winter conditions in the natural habitat of without any MP to FP change), MPs began again to change
the population sampled (Bauer, 2002). The less favorable to FP, and a majority did change orwere changing to FP by
breeding conditions of the suboptimal treatment are appar- the end ofthe experiment. During the same period, neither
ent from a comparison of the reproductive condition and ofthe two MPs remaining in the original optimal treatment
molting rates between the suboptimal and optimal treat- changed. At the end of22 weeks two MPs from the original
ments. The percentage ofFPs brooding embryos or prepar- suboptimal treatment had neitherchanged nor showed signs
ing for spawning was only slightly higher in the optimal of change to FP in spite of a switch from suboptimal to
than in the suboptimal treatment. However, the molting rate optimal conditions during the last 8 weeks of observation.
of the optimal treatment, adjusted for number of FPs sur- Lin and Zhang (2001) found that all MPs reared individu-
viving, was more than twice that of the suboptimal treat- ally under optimal conditions became FPs; but when MPs
ment. In L. \\-iirileinanni FPs, spawning occurs at every molt were reared in groups of 10. as in this study, only 67%
(Bauer and Holt, 1998), so that the higher molting of the transformed to FP, much less than that observed in the
optimal treatment indicates that more broods were pro- present study. Lin and Zhang began with postlarvae (MPs).
duced. At the temperature and photoperiod of the optimal and the total period ofobservation was not specified. In the
treatment, molting and spawning may occur every 10-14 present study, the experiment began with MPs at or above
days (Lin and Zhang. 2001; Bauer, pers. obs.). Using a the minimum size ofchange to FP. Although Lin andZhang
figure of 12 days between spawning molts, a FP in the suggested that a rather high percentage ofindividuals never
optimal treatment could have molted and spawned five change sex (primary males), my results suggest that most, if
times during the 9 weeks ofthe experiment. Molting in the not all. will change to FP sometime during their lifetime if
suboptimal treatment was less than halfof that in the opti- they liveoutthe maximum natural lifespan (about 1.5 years;
mal treatment, so that the number of FP molts in this A. W. Baldwin and R. T. Bauer, unpubl.). However, in both
treatment was about two, with a maximum of two spawns experimental groups in my study, a low percentage of
possible. Although breeding conditions were poorer in the individuals (4%) never changed under laboratory condi-
suboptimal treatment, no reversion ofFPs to MPs occurred. tions.
Given that change from MP to FP takes place within a The adaptive advantage ofnot changing to FP during the
single molt cycle, reversion of FPs back to a male phase non-breeding season may be that reproductive effort will be
could have taken place within a single molt cycle as well. In wasted on embryo production during a period unfavorable
the suboptimal treatment, FPs passed through two molt to larvae. This energy might be channeled into maintenance
356 R. T. BAUER
and growth so that when spring arrives, the MP will change Bauer, R. T. 1986. Sex change and life history pattern in the shrimp
into a largerFP, with the benefit ofa larger brood produced Tharmtinningi(Decapoda: Caridea): anovelcase ofpartial protandnc
under conditions favorable to larval growth and survival. hermaphroditism. Riot. Bull. 170: 11-31.
Bauer, R. T. 1991. Analysisofembryoproduction inacaridean shrimp
Brood size in L. wurdemanni is highly correlated with body guildfromatropicalseagrassmeadow.Pp. 181-191 inCrustaceanEgg
size (Bauer, unpubl.), as in other carideans (Bauer, 1991). Production. A. Wennerand A. Kuris. eds. A. A. Balkema. Rotterdam.
Suboptimal conditions did slow and then stop sex change in Bauer, R. T.2000. Simultaneous hermaphroditism in caridean shrimps:
this study, explaining the presence of large and very large a uniqueandpuzzlingsexualsystemintheDecapoda.J. Cnistac. Biol.
MPs during the fall through early spring in field samples. 20 (Special Number 2): 116-128.
Hlaorwgeervesri,zelatrhgaenMlPasrgedidMPnost rcehaarnegdeutnodFerP aotptaimsiaglni(fsipcranitnlgy/ BBaauueesrru,,reRRl..acTTi..on2200c00o12n..atrHRieebrupmtroaosfdrusocodtciiivtoeeicsoemlcooogleioncgocysa.mofaIrnaotenprercsoi:etnaecnlidasnic2s6ts:eimm2au-l7st.eaxnueaoluys
summer) conditions. hermaphrodite, the shrimp L\smuta wurdemanni (Decapoda: Caridea:
In conclusion, mating experiments showed that FPs are Hippolytidae). J. Cnixtac. Biol. 22: 742-749.
competitive with MPs of any size in obtaining copulations Bauer, R. T., and J. H. Abdalla. 2001. Male mating tactics in the
with parturial FPs. There seems to be no mating advantage shrimp Palaemonetespugio (Decapoda, Caridea): precopulatory mate
for an individual to remain a large MP, and under optimal Bauegru,ardRi.ngT.,vsa.npdurGe.sJe.arHcohilntg..1E9t9h8o.logSyim1u0l7t:an1e8o5u-s20h0e.rmaphroditism in
breeding conditions, almost all change to FP. The propor- the marine shrimp L\\tata wurdemanni (Caridea: Hippolytidae): an
tion of large and very large MPs in the natural population undescribed sexual system in the decapod Crustacea. Mm: Biol. 132:
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laboratory, change from MP to FP is slowed under the Berglund, A. 1986. Sex change by a polychaete: effects of social and
suboptimal breeding conditions of these seasons. Seasonal reproductive costs. Ecology67: 837-845.
Bergstrom,B.I. 1997. Doprotandricpandalidshrimphaveenvironmen-
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Acknowledgments fluctuations in pandalid shrimp. Am. Nat. 134: 824-827.
This study was funded by the National Science Founda- Charnov. E. L.. D. W. Gotshall,and J.G. Robinson. 1978. Sex ratio:
tion (Biological Oceanography Program, grant OCE- eadnacpeti2v0e0:re2s0p4o-n2s0e6.to population fluctuations in pandalid shrimp. Sci-
99822466) and the Neptune Foundation. I thank student Conover. ()., and S. B. Munch. 2002. Sustaining fisheries yields over
assistants Aaron Baldwin and Sara LaPorte fortheircareful evolutionary time scales. Science 297: 94-96.
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Laboratory for Crustacean Research, University of Louisi- tidae). I. Le condizioni normali della sessualita in natura. Piibbl. Stn.
ana at Lafayette. Zool. Nupoli 22: 257-272.
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