abstract.–growth and sexual maturation were studied in

8/14/2019 Abstract.Growth and Sexual Maturation Were Studied In

1/16

526

In nor thern South Amer ica , the

ghos t sh r imp Lepidopht halm ussinuensis Lemaitre and Rodrigues

ha s been foun d r estr icted t o oligo-

haline estuar ies on t he Caribbean

coast of Colombia (Lemaitre and

Rodrigues, 1991). From previous

st udy of a congener ic species, osmo-

r e g u l a t o r y c a p a c i t y a n d t o l e r -

a n c e o f h y p o x i a i n t h i s g e n u s

(Felder, 1978, 1979; Felder et al.,

1986) appear to exceed abilities re-

ported in most other callianassid

genera (Thompson and Pritchard,

1969; Forbes, 1974, 1978; Mukai

an d Koike, 1984; Posey, 1987). Su ch

ada pta tion has allowed members of

th e genus t o exploit exten sively low

salinity habitats, especially richly

organic s i l ty bars and banks of

lower r iver mouths or inter t idal

mudf l a t s (Fe lde r and Manning ,

1997). In L. s inuensis and some

eastern Pacific congeners (Nates

and Felder, 1998), this adaptation

also includes sedimen ts of tr opical,

estuarine ponds in which penaeidshrimp ar e cultured.

Dense accumulat ions of ghost

shr imp in these penaeid cul ture

ponds ar e favored by their abbr evi-

ated larval development (Nates et

al., 1997). At high levels of infesta -

tion by these bur rowers, metabolic

impacts and biotur bation appear to

decrease pena eid shrimp pr oduction

by reducing sur vival ra tes of post-

Growth and maturation of the ghost shrimpLepidophthalmus sinuensisLemaitre andRodrigues, 1991 (Crustacea, Decapoda,Callianassidae), a burrowing pest in

penaeid shrimp culture ponds*

Sergio F. Nates

Darryl L. Felder

Department of Biology and Laboratory for Crustacean Research,

University of Southwestern Louisiana

Lafayette, Louisiana 70504-2451

E-mail address (for D. L. Felder, contact author): [email protected]

* Contribution 57 from the University ofSouthwestern Louisiana, La borat ory of C r u s t a c e a n R e s e a r c h , L a f a y e t t e , L A70504-2451.

Man uscript a ccepted 14 August 1998.Fish. Bull. 97:526541 (1999).

Abstract.Growth an d sexual mat u-ra tion were studied in the ghost shrimp

Lepidophthalm us sinuensis , a pest spe-

c i es i n fes t i ng o l i gohal i ne penae id

shrimp culture ponds on the Caribbean

coast of Colombia . Sex ra tio was s ignifi-

cant ly fema le-biased over four years of

sam pling. Development of ovaries, in-dexed as relative width, peaked prior

to peak occurr ence of ovigerous fema les

and either coincided with or immedi-

ately followed the quarter of lowest

am bient sa linity. Ovigerous females oc-

curred in all months, but t he greatest

mean percentage occurred in th e first

or second qu art er of each year. Size an d

colora tion of ovar ies varied by mat ur a-

tional sta ge, and month ly counts of eggs

per female peaked in Februa ryApril .

Detection of recruits


2/16

527Nates and Felder: Growth and maturation of Lepidophthalmus sinuensis

1971; Poore and Suchanek, 1988; Witbaard and

Duineveld, 1989; Tamaki and Ingole, 1993; Rowden

an d J ones, 1994, 1995; Dumbau ld et al., 1996), and

th e importan ce of callianassids in sediment tu rn over

and nutrient cycling has been noted (Rowden and

J ones, 1993; Ziebis et al., 1996). Ecological impa cts

ofLepidophthalmus spp. can dominate t hose of oth erestuar ine infaun a, as n oted in recent studies of the

warm-tempera t e species L. louisianensis i n t he

northern Gulf of Mexico (Felder and Lovett, 1989;

Felder a nd Griffis, 1994) an d th e tr opical speciesL .

sinuensis on th e Car ibbean coast of Colombia (Nates

and Felder, 1998). Larval life histories for both L .

louisianensis and L. sinuensis have been described

(Nates et al., 1997), but lat er life stages and m at ur a-

tion remain little known for the tropical species L .

sinuensis. Objectives of the present study were to

analyze the periodicity and frequency of reproduc-

tive activity, to determine rates of growth in mor-

phological featu res, a nd to define allometr ic indica-tors of maturation for populations of L. sinuensis.

Resulting implications for management of penaeid

shrimp ponds are discussed.

Materials and methods

All animals were obtained at the Agrosoledad S.A.

shrimp farm on t he upper Cispata estuar y of the Ro

Sin, Departamento de Cordoba, Colombia, near

917'N, 7550'W. In order to a void overt effects of pond

harvesting, feeding, and other management activ-

ity, collections were restricted to bottom sediments

of earth en dra inage cana ls that extend for several

kilometers through the farm. Specimens were indi-

vidually extr acted from bur rows with yabby pumps

(Man ning, 1975), and sa mples included a ll an imals

retained when extracted sediments were washed on

coarse (5-mm) sieves. All population samples were

ta ken with in 500 m of th e upper end (origin) of the

dra inage canal system where colonized bott om muds

ra nged from about 3 to 6 m in width a nd populat ion

density ra nged from 15 to 40 an imals per m 2.

Monthly sampling of populations extended over

four years from December 1991 through December1995. Each monthly sample consisted of animals

obtained from burr ow openings encoun tered at r an -

dom during walks along transects that crossed ex-

posed mudflats at the sa mpling site dur ing a period

of redu ced pond discha rge. The sa mple consisted of

at least 60 an imals, and over 3200 an imals were col-

lected in the course of the study. Following collec-

tion, animals were transported in individual perfo-

ra ted vials (Felder, 1978) to th e farm laboratory for

morph ological a na lysis. Specimens lacking chelipeds,

having incompletely regenerated chelae, or with

other obvious appen dage deform ities were excluded

from the analyses that involved measures of those

appendages but included in analyses of population

size-class st ru cture. In th e laboratory, each individua l

was sexed on th e basis of an terior pleopod morpho-

logical features and evidence of ovaries visibleth rough t he integu ment . Wet weight (WW) was de-

termined to 0.1 g on a top-loading balance after

an imals were blott ed with tissue pa per. Dry weight

was estimated by drying the a nimals at 60C for 48

h, and ash content was estimated from weight a fter

ignition a t 500C for 6 h. When pres ent , eggs on pleo-

pods were include d in weight s of ovigerous fema les.

Morphometric measurem ents (Felder an d Lovett,

1989) were made with dial calipers to 0.05 mm.

Becau se carap ace length (CL) is usu ally less depen-

dent on gonadal development than are most other

s ize measurements (Har tnol l , 1982; Felder and

Lovett, 1989), it was s elected to repr esent body sizeand measur ed from the t ip of the rostrum t o the pos-

terior m ar gin of th e cardiac region. Total length (TL)

was measu red from t he tip of the r ostru m t o the pos-

terior margin of the extended telson. Major chela

height (ChH) was measu red as th e maximum h eight

of th e propodus, inferior m ar gin to superior ma rgin.

Major chela width (ChW) was mea sur ed as t he ma xi-

mum width of the propodus from the most convex

area on the internal surface to the opposite convex

area on the external surface. Major chela length

(ChL) was measu red as the m aximum length from

the superior proximal articulation of the propodus

with the carpus to the superior distal articulation

with th e dactylus. Between November 1992 and De-

cember 1995, ovarian width (OW) of females (the

width of th e right ovary visible dorsally through th e

integument of the third abdominal segment) was

determ ined. An in dex of relat ive ovarian developmen t

was estima ted from the ra tio OW/CL. Color and n um -

ber of eggs, color of the ovaries, evidence of para-

sites, an d occurren ce of dama ged or m issing chelae

were also recorded. Egg size was m easu red un der a

light microscope and ocular micrometer. Volume of

the eggs was calculated from the mean of the long

and sh ort a xes used as th e single diameter measur e-ment for a sp here (McEdwa rd a nd Chia, 1991).

Temperature and salinity were measured twice

daily (dawn a nd du sk) at t he sur face and bottom of

filled ponds. Tempera tu re was mea sur ed 1 C with

th e pr obe of a YSI model 57 temper at ur e-compen -

sated oxygen meter. Salinity 1 ppt was measured

with a temperat ure-compensat ed r efractometer.

All means were reported along with the 95% CI

(confidence interval). Monthly population samples

were pooled to compare quarterly variations in the


3/16

528 Fishery Bulletin 97(3), 1999

distribution of size cohorts and the occurrence of

ovigerous fema les in the popula tion. Tempora l tren ds

in both carap ace length s an d sex ratios for the over-

all four-year span of th e stu dy were an alyzed by lin-

ear-linear piecewise polynomial r egression to define

slope transition points. Percentile data for the sex

ra tios were ar csine-tran sformed prior t o these ana ly-ses. In order to remove effects of morphologically

an omalous postrepr oductive and sen escent individu-

als, animals >18.0mm CL (two females and three

males) were excluded from analyses of relat ive

growth. Linear-linear piecewise polynomial analy-

sis of un tr an sform ed dat a was u sed to optimize posi-

tioning of ontogenet ic tr an sition p oint s (0.05 mm )

in all relative growth comparisons. Except for this

alter na tive meth od of itera tively locating slope tr an -

sitions, methods complied with the recommended

pra ctice of fitting regressions to un tr an sform ed dat a

above and below tran sition points by reduced ma jor

axis (Lovett a nd F elder, 1989). Sta nda rd a llometr iccoefficient s (Huxley, 1932) were also deter min ed from

regressions of log-tr an sform ed dat a by least squ ar es

estimate, with dat a subdivided a t the previously es-

timated transition points. All statistical analyses

were performed with NCSS (Number Cruncher

Sta tistical System) 6.0 softwar e (Hintz, 1995).

Becau se generic revisions h ave yet to addr ess man y

of the confamilial taxa that are treated in our com-

parative discussions, it was necessary in compara-

t ive discussions to refer to some species under

Callianassa sensu lato (s.l.), while acknowledging

that Callianassa sensu stricto has been restricted to

a few eastern Atlant ic populations (see Mann ing and

Felde r, 1991).

Results

Sex ratio

Except for J anu ary t o Jun e 1992, March 1993, and

Febr ua ry 1995, sex rat ios were significantly female-

biased over t he four yea rs of sam pling (Fig. 1A). Over

the en tire study period, the mea n sex rat io was 2.4

0.3 females per male, with the lowest mean ratio(1.1) occurring in February 1992, and the highest

ratio (5.1) in October 1993. Trends in mean CL of

th e population (Fig. 1B) genera lly tr acked th ose in

sex ra tios, as defined by piecewise regression a na ly-

sis. Slopes over th e first two years revealed declin-

ing relative abun dance and increasing mean CL of

ma les, pat tern s th at differed significan tly from th ose

of the last two years of monitoring. An iteratively

optimized tr an sition point for sex rat ios occurred a t

23 months, whereafter mean sex ratios remained

nea r a symptotic. Ana lysis over t he full stu dy period

also defined an optimized tr an sition point or pea k in

CL of males at 23 months, beyond which male CL

was a symp totic. The CL of females, h owever, peak ed

late in t he first year of monitoring.

Mean size of both males and females increased

slight ly but significan tly from th e first t hr ough four thqua rt er of each year except for 1994, a year in which

th e presen ce of first qu ar ter recruits wa s offset by a

cohort of large individua ls sur viving from th e pr evi-

ous year (Fig. 2). When t rea ted separ at ely, mat ur e-

sized individuals (>11 mm CL) of both male and fe-

ma le populat ions increased in m ean CL over th e year,

usua lly peaking in the fourt h qua rter prior t o maxi-

mu m abu nda nce of ovigerous fema les in t he follow-

ing year (Fig. 3, B and D). Mean CL of males ap-

pear ed to exceed slight ly tha t of females over th e full

stu dy period, and m ales dominated lar ge size classes

(Figs. 1B, 2, 3B). Only 4.3% of the collected females

were >15.0 mm CL, wherea s 12.4% of ma les att ainedthis size. The largest animal collected was a 20.7-

mm-CL male. Detection of recruits


4/16


Figure 1

Sex composition (A) and mean carapace length (CL) (B ) in sampled Colombian populations of

Lepidophthalmus sinuensis, December 1991 thr ough December 1995. Mean CL is shown separa tely

for males (closed circles) and females (open circles); vertical lines define 95% CI. The transition

point at which dat a a re subdivided, estimat ed by piecewise linear-linear polynomial regression, was

selected to minimize the sum of squa res of residua ls.

Development of ovaries reached maxima in the

quarter prior to peak occurrences of ovigerous fe-

ma les an d eith er coincided with or immediat ely fol-

lowed the quarter in which lowest ambient salini-

ties occur red (Fig. 3, A, C, an d D). Examin ed a s a

month ly value pooled over the t hree years t hat it was

monitored (Fig. 5C), this index of ovarian develop-

ment was at m inimum values in Jun e and J uly when

ovaries of many spent and immature females, al-

though evident for the full length of the abdomen,

were limited in width to na rr ow tr an slucent-yellow

strands. Ovaries became deep yellow to yellow-or-

ange as relative ovarian width began to increase

mar kedly in August, concurrent with an ann ual de-

cline in am bient sa linity. By October, ovar ies of most

mat ure females were somewhat lobate in sha pe and

yellow-orange to reddish orange in color, and ova-

rian index reached high values th at persisted through


5/16


Figure

2

Quarterlysizeclass(CL)frequencydistributionsformales(openbars),nonovigerousfemales(hatchedbars),andovigerousfemales(solidbars)insam

pledColombian

populationsofLepidophthalm

ussinuensis,January1992throughDecember1995(n=samplesize).

Febru ar y. Highest values for

the ovarian index, in F ebru-

ary (0.139 0.012), were sig-

nificant ly greater tha n were

preceding values in Decem-

ber or t hose th at followed in

M a r c h t h r o u g h M a y . D e -creasing m easur es of relative

ovarian width during April

through June (Figs. 3C and

5C) were coincident with t he

second quar ter maxima in

abundance of ovigerous fe-

males (Fig. 3D and 5B) be-

cause ma ny of th ose fema les

had spent ovaries.

Shape of the eggs was al-

most spherical in recent ly

deposited pa le yellow to yel-

low-orange clut ches an d be-came more oblong as color

faded to t rans lucent gray-

brown in lat e-sta ge eggs just

prior to hatching. Mean egg

volum e in live lat e sta ge eggs

was 0.81 0.07 mm 3 (n=7 6

eggs, from 5 different fe-

ma les), an d th e coefficient of

variat ion in volum e with in a

single egg clutch was 5.09%

(n =30) ; mean d imens ions

were 1.22 0.04 mm by 1.05

0.02 mm. The t otal n umber

of eggs per female ranged

from 182 44 in small fe-

ma les (


6/16


Figure 3

Quarterly measures of salinity, growth, and reproductive indices in sampled Co-

lombian populations of Lepidophthalmus sinuensis, January 1992 through De-

cember 1995; for AC, vertical lines define 95% CI; for DE, vertical lines define

ran ge. (A) Morning surface salinity (ppt) at th e farm inta ke pump stat ion in t he

upper estua ry, expressed as m ean of daily measures t hroughout ea ch quarter; (B )

mea n CL of mat ur e (>11 mm CL) males (closed circles) an d females (open circles)in sampled populations; (C) relat ive ovar ian developmen t (OW/CL); (D ) percent-

age of ovigerous individuals a mong females; (E ) percenta ge of juveniles (10.00

mm CL).

abundance per clutch (Fig. 5, B

and D), was maintained at par-

t icularly elevated levels from

Februa ry thr ough at least April

and perhaps Ma y.

Growth and sexual maturation

Size at sexua l matu rat ion in both

ma les and females of th e sampled

population was evident in rela-

tive growth chan ges of th e ma jor

chela. Asymmetry of the f i rs t

pereopodal chelae was clearly

evident in both sexes an d did not

show bias for right or left han d-

edness in random subsamples

(left:right ha ndedn ess 23:27 for

males, 25:25 for females; n =50

per sex). The value of th is feat ur eas a seconda ry sex cha ra cter was

suggested initially by the much

heavier general appearance of

the appendage in la rge males

th an in females of approxima tely

th e sam e size, an d sexual differ-

ences in allometric growth were

docum ented su bsequent ly by re-

gress ion a na lyses of morp hologi-

cal measu remen ts (Fig. 6; Tables

1 an d 2).

Rela t ive growth ra te in the

chela width of ma les increased in

animals that h ad reached a mean

carapace length of at least 11.3

mm, as estimated by linear-lin-

ear piecewise polynomial r egres-

sion analysis (Fig. 6A). Indepen-

dent regression an alysis of males

larger and sma ller tha n th is size

by reduced major axis revealed

significant differences in slopes

for t hose da ta sets (Table 1), even

though the two values for this

positive allometric growth didnot differ significan tly when com-

pared as allometric coefficients

(Table 2). When fitt ed by r educed

major axis, regression slopes for

both premat ura tion and postma-

tu ra tion pha ses of growth in female chela width (Fig.

6B) differed significan tly from th ose for both gr owth

phases in m ales, although th ere was far greater dif-

ference between the sexes in the postmaturation

pha se. Relat ive growth in th e chela width of females

became significantly less positive beyond a carapace

length n ear 10.8 mm . The negat ive allometr ic growth

(coefficient


7/16


Figure 4

Size class (CL) frequency distribut ion of all ovigerous females in s am pled

Colombian populations ofLepidophthalm us s inuensis , December 1991

through December 1995 (number by class appears above each bar).

Analysis of relative growth in ma-

jor chela h eight for ma les (Fig. 6C) and

females (Fig. 6D), when s caled to car a-

pace length , produced remarkably

s imi lar resul t s to tha t for re la t ive

growth in chela width , sugges t ing

some interdependency of those mea-sures. Transi t ion points were opt i-

mal ly located a t a mean carapace

length of 11.0 mm for males and 11.2

mm for females, and postmaturation

growth differed significantly between

th e sexes (Table 1). On t he ba sis of al-

lomet ric coefficient s (Tab le 2), positive

prema tu ra tion a llometric growth once

again did not differ between t he sexes,

whereas nega t i ve pos tma tu ra t i on

growth in females differed signif i -

cantly from t he str ongly positive a llo-

m e t r i c g r ow t h i n p o s t m a t u r a t i onmales. Analysis of chela width scaled

to chela height in both sexes did not indicate signifi-

cant pr ematu rat ion differences between males an d

females, and gr owth in both sexes was isomet ric or

nea rly so (Tables 1 a nd 2 ). However, following t ra n-

sition to the postmaturation phase in males, rela-

tive growth in chela width exceeded th at of height.

The opposite effect was seen in postmaturation fe-

ma les; negat ive allometric growth was seen in chela

width, when compa red to chela h eight.

Ana lysis of total lengt h s caled to car apa ce length

revealed large mea sur es of err or (Tables 1 an d 2), as

expected in size measurements that include the

lengt h of a soft, str etcha ble abdomen . Allometr ic co-

efficients indicated t ha t s lopes did n ot significan tly

differentiate premat ura tion growth from an isomet-

ric pattern in either sex, whereas postmaturation

growth on the basis of this par ameter appeared t o

be negat ively allometr ic but similar in r at e for both

males an d females.

Large mea sur es of error a ssociated with wet weight

measur ements in relation t o cara pace length, espe-

cially at sm all sizes, limited det ection of possible sex

differen ces in allometr ic coefficient s based u pon th is

par amet er a nd did not r esolve significan t d ifferencesbetween growth pha ses of eith er s ex (Table 2). Only

in th e postmat ur at ion ph ase were allometric coeffi-

cient s based u pon wet weight significan tly more posi-

tive in males than in females. The more sensitive

analyses of wet weight based upon regressions by

red uced ma jor a xis (Fig. 7, A an d B; Table 1) detected

highly s igni fican t d i fferences between pos tma-

turation males and females, regardless of whether

ovigerous females were included or excluded from

th e an alysis, and a lso resolved significan t differen ces

in ra tes of mass accumulat ion between prema-

turation and postmaturation growth phases. Opti-

mized tra nsition point s in piecewise regression a na ly-

ses of wet weight to length r elationships were n ear

9.8 mm CL for females and near 11.3 mm CL for

males. These regression break s suggest tha t m atu -

ra tion in males occurs at slight ly higher wet weights

(1.5 to 2 g) tha n in fema les (usu ally near 1 g).

Dry weights a nd as h free dry weights were deter -

mined for limited subsets of our sample and were

not subjected to regression a na lysis. The proport iona l

relation of dry to wet weight in ovigerous females

(0.47 0.06; n=8) was slight ly but significan tly higher

th an in n onovigerous females (0.36 0.03; n=76) an d

ma les (0.33 0.05; n=12), whereas th e relation of ash

free dry weight t o wet weight in ovigerous fema les

(0.052 0.003; n=8) was not significantly different

from that of either nonovigerous females (0.059

0.011; n=41) or m ales (0.055 0.003; n=2).

Discussion

Sex ratio

Strongly female-biased sex ratios in the monitored

population of Lepidophthalmus s inuensis are in

mar ked contra st to those report ed in int ertidal popu-

lations ofL .louisianensis on th e Mississippi coast in

the northern Gulf of Mexico (Felder and Griffis,

1994), which were variable but averaged near 1:1.

However, female-biased ra tios have been reported in

populations of L. louisianensis from the Louisiana

coast in the northern Gulf of Mexico (Felder and


8/16


Figure 5

Pooled monthly mea sures for salinity, temper atu re, an d r eproductive indices in

sam pled Colombian populat ions of Lepidophthalmus sinuensis; for A, month ly tem-

perat ure da ta were pooled from December 1991 thr ough December 1993, and m onthly

salinity from Ja nua ry 1992 through December 1995; for B, monthly data were pooled

from Ja nu ar y 1992 through December 1995; for C, mont hly data were pooled from

J an ua ry 1993 thr ough December 1995; for A, C, and D, vertical lines define 95% CI;

for B, vert ical lines define ra nge. (A) Morn ing sur face salinity (solid circles, continu-

ous l ine) at farm intake pum p in upper estu ary, and a fternoon surface temperature

(open circles, broken line) at outlet in pond 1, expressed as mea ns of daily mea sur es;(B ) frequency of ovigerous individuals among mature (>11.0 mm CL) females of

populations; (C) relat ive ovar ian developmen t (OW/CL); (D ) mean number of eggs

in clutches of ovigerous females.

Lovett , 1989), as well as in

populations of western Pa cific

intertidal tha lassinideans such

as Trypaea australiensis Dana

(Hai l s tone and Stephenson,

1961), Callianassa s . l. filholi

Milne Edwards (Devine, 1966),and sexually matu re adult popu-

lations of Neotrypaea califor-

niensis (Dana) and Upogebia

pugettensis Dana (Dumbau ld et

al . , 1996). Populat ions were

male-biased in sam pled popula -

tions ofCallianassa s. l. subter-

ranea Monta gu from subtidal

Eu ropean water s (Rowden and

J ones, 1994).

Observance of skewed sex ra -

tios in tha lassinidean sa mples

may r eflect actual bias in th epopula tion or an ar tifact of col-

lect ing methods that do not

sample sexes equal ly within

the vertical profile of burrows

or ac ros s hor i zon t a l beach

transections, especially when

collections m ust be rest ricted to

readi ly accessed reaches of

shore l ine sediments . Move-

ment of ovigerous females to-

war d th e sur face for egg release

or to optimally ventilate eggs

could lead to great er pr obabil-

ity of their capture when bur-

rows ar e aspirated with yabby

pum ps. Likewise, sam pling re-

stricted to shorelines may re-

flect d ifferen tia l positioning of

sexes with in the bur row along

tidal or wave agitation clines.

Such effects could account for

pr evious observa tions in which

p o p u l a t i o n s o f C a l l i c h i r u s

islagrande were female-biased

on high wave-energy beachesbut not on nearby protected

beaches, or for r at ios th at dif-

fered ma rkedly from month to

month in some populations of

L. louisianensis from the Gulf

of Mexico (Felder and Griffis, 1994). In the present

study, mudflats along margins of drainage canals

were fully accessible to samp ling dur ing periods of

low pond discharge, samples were not limited to

shorelines, and bu rrows were not as deep as r eported

for a bove men tioned populat ions ofC. islagrand e and

L. louisianensis. From resin casts (Fig. 4 in Nates

and Felder, 1998), it was observed that almost all

burrows were


9/16


Table 1Formulae and statistics for linear regressions (by reduced major axis, with untransformed data) of chela width on carapace

length (ChW:CL), chela height on carapa ce length (ChH:CL), chela width on chela height (ChW:ChH), tota l length on cara pace

length (TL:CL), and wet weight on carapace length (WW:CL) for male and female populations of Lepidophthalmus sinuensis

sam pled at t he Agrosoledad S. A. shr imp farm , upper Cispat a est ua ry, Colombia, from December 1991 through December 1995.

Regressions were calculat ed for ent ire dat a set (All) and for dat a subdivided at t he tr an sition point (yielding separ at e regressions

for dat a points Xand dat a points >X, whereX= size at onset of sexual m atu rity estima ted by piecewise linea r-linea r polynomialregression), n = sample size, r2 = coefficient of determination, 95% CI = confidence interval of slope.

n r2 Formulae 95% CI

ChW:CL

Males

All 985 0.69 Ch W = (0.612 CL ) 3.474a 0.021

X 218 0.47 Ch W = (0.618 CL ) 3.179b 0.061

>X 767 0.49 Ch W = (0.789 CL ) 5.974a,b 0.039

Females

All 1998 0.35 Ch W = (0.273 CL ) 0.519a,b 0.009

X 125 0.62 Ch W = (0.454 CL ) 1.925a,b 0.049

>X 1873 0.12 Ch W = (0.304 CL ) 0.943a,b 0.013

ChH:CL

MalesAll 987 0.74 Ch H = (0.991 CL ) 4.843c 0.031

X 192 0.47 Ch H = (1.063 CL ) 5.012d 0.111

>X 795 0.57 Ch H = (1.198 CL ) 7.761c 0.054

Females

All 1998 0.49 Ch H = (0.513 CL ) 0.425c,d 0.016

X 177 0.64 Ch H = (0.842 CL ) 3.345c,d 0.075

>X 1821 0.20 Ch H = (0.513 CL ) 0.425c,d 0.021

ChW:ChH

Males

All 987 0.94 Ch W = (0.618 Ch H) 0.482e,f 0.009

X 274 0.85 Ch W = (0.605 Ch H) 0.354g 0.028

>X 713 0.88 Ch W = (0.655 Ch H) 0.831e,g 0.017

Females

All 2000 0.71 Ch W = (0.532 Ch H) 0.292e,g 0.013

X 71 0.88 Ch W = (0.550 Ch H) 0.175f 0.046>X 1929 0.53 Ch W = (0.588 Ch H) 0.646e 0.018

TL:CL

Males

All 1007 0.80 T L = (4.349 CL ) 1.033h,i,l 0.121

X 737 0.77 T L = (4.693 CL ) 4.695h, l 0.161

>X 270 0.15 T L = (6.374 CL ) 32.918h, j 0.703

Females

All 2158 0.64 T L = (4.641 CL ) 3.186i,j,k 0.117

X 1006 0.64 T L = (5.419 CL ) 11.495h,i,j 0.201

>X 1152 0.22 T L = (5.766 CL ) 19.813k 0.293

WW:CL

Males

All 937 0.70 WW = (0.751 CL ) 6.431l ,m,o 0.026

X 200 0.22 WW = (0.679

CL ) 5.250

n

0.084>X 737 0.60 WW = (0.998 CL ) 9.927 l ,n,s 0.046

Fem ales (including th ose with eggs)

All 1933 0.49 WW = (0.613 CL ) 5.053 l,p 0.019

X 50 0.32 WW = (0.508 CL ) 3.195m ,q 0.122

>X 1883 0.42 WW = (0.698 CL ) 6.204l,p,q 0.024

Fem ales (excluding those with e ggs)

All 1542 0.53 WW = (0.581 CL ) 4.680o 0.019

X 41 0.42 WW = (0.472 CL ) 2.933 l ,n,r 0.119

>X 1501 0.44 WW = (0.662 CL ) 5.767o,r,s 0.024

as = allometric coefficients with sa me super script ar e significant ly (P


10/16


Table 2

Allomet ric coefficients mea sur ed as s lopes for linea r regr essions (by least s quar es estima te, with log-tra nsformed da ta ) of chela

width on cara pace length (ChW:CL), chela h eight on cara pace length (ChH :CL), chela width on chela h eight (ChW:ChH), total

length on car apa ce length (TL:CL), an d wet weight on cara pace length (WW:CL) for male a nd fema le populations ofLepidophthalmus

sinuensis sampled at the Agrosoledad S. A. shrimp farm, upper Cispata estuary, Colombia, December 1991, through December

1995. Coefficients were determined for entire data set (All) and for data subdivided at the transition point (yielding separate

regress ions for dat a points Xand dat a points >X, whereX= size at onset of sexual mat urit y estimat ed by piecewise linear-linear

polynomial r egres sion), 95% CI = confidence inte rva l of coefficient . * *= allometr ic coefficient sign ifican tly (PX 0.441**a,b,c,d 0 .053 0 .491**e,f,g,h 0 .045 0 .864**i,j,k,l 0.033 0.693**p,q,r 0 .051 2 .064**s,t,u 0.122

This observat ion suggests th at t he detected sex bias

accurately characterizes the population sampled.

In t he course of previously report ed observations

on populat ions ofC. s. l.filholi, i t was noted that the

sex rat io was nea r 1:1 only when sm all anima ls were

included in the sample (Devine , 1966) . For L .

sinuensis there is also a correlation between mean

size of an imals in th e monitored populat ion a nd sex

ra tio over th e four years of monitoring. As n oted for

C. s. l. filholi, samples of smaller mean CL were

nearer 1:1 in sex ratio than were samples of larger

mea n CL. The tr end toward increa sing frequen cy of

females reached an approximat e asymptote after 23

months of observation, simultan eous with the trend

in increasing CL of ma les, and ma y indicat e a point

at which increasing nu mbers of larger m ales estab-

lished a sexua l equilibrium by displacing small males

from a limited habita t or maint ained ter ritory. This

increase corr esponds roughly to th e time when bu r-

row densities with in ponds on t he farm began expo-nential increase and when detrimental effects on

water quality and penaeid production became evi-

dent (equals month 38 in Figure 1 of Nates and

Felder, 1998). Sex ra tios and mea n cara pace length s

may thus serve to forecast potential for rapid in-

creases in infesting populations.

Both t he lar ge body size and t he robust chelipeds

of mature males could be of advantage in competi-

tion for limited space and available females wher-

ever L. sinuensis occurs in dense, mature aggrega-

tions. Such behaviors ha ve been su ggested previously

to account for large numbers of possibly displaced

juvenile males of L. louisianensis observed periodi-

cally in plank ton sa mples (Felder an d Lovett , 1989;

Felder and Rodrigues, 1993). Similar intraspecific

compet ition for s pace, in which juven iles are expelled

to the s ur face, has a lso been postulat ed to occur in

some popula t ions of Cal l i anas s a s . l . japonica

(Ort ma nn ), along with possible immigrat ion of juve-

niles to other habitats (Tamaki and Ingole, 1993).

While not docum ent ed t o occur in L. sinuensis , colo-

nization of ma ricultur e ponds by such displaced ju-

venile males pumped in with estu arine waters could

account for higher percentages of males observed

early in our stu dy. Such r ecru itmen t of juveniles could

potent ial ly supplement larval set t lement within

ponds to rapidly build early infesta tion densities.

Ovigerous females

The abbreviated life cycle in L. sinuensis includes

only two brief zoeal stages, large numbers of which

occur in nocturnal plankton samples taken at the

stu dy site (Nates et a l., 1997). The eggs of this spe-

cies an d its congen erL. louisian ensis are compa rable

in size to th ose ofCallianassa s. l. kraussi Stebbing,

another estuarine species that exhibits markedly

abbreviated development (Forbes, 1973), and are

larger th an those of many t halassinids with longer

larval hist ories and wider plank tonic dispersa l (see


11/16


Figure 6

Linear r egression (by least squa res estima te for u ntra nsformed da ta) of chela

width (ChW) on cara pace length (CL) for (A) males and (B ) fema les and chela

height (ChH) on CL for (C) males and (D ) females in sampled Colombian

populations of Lepidophthalmus sinuensis, December 1991 through Decem-

ber 1995. The tr ansit ion point at which da ta are subdivided, estimated by

piecewise linear-linear polynomial regress ion, was positioned t o minimize th e

sum of squares of residuals.

Poh l, 1946; Forbes , 1973; Tunber g, 1986), with some

clear exceptions (see de Vau gelas et al., 1986). Given

abbr eviated development inL. sinuensis and t he like-

lihood of alm ost immedia te set tlemen t by decapodids

into th e vicinity of our sa mple site, we expected to

detect dist inct cohorts of sma ll recruits, from wh ich

we could estimate rates of growth to maturation.However, unlike th e population of the warm temper-

at e species L. louisianensis from t he Gulf of Mexico

(Felder an d Lovett, 1989), tr opical populations ofL .

sinuensis included ovigerous females in every mont h

of sampling. This potential for continuous recruit-

ment over the annual cycle, coupled with our lim-

ited su ccess in consistent ly captu ring sm all individu-

als, limits clear definition of repr oduction a nd gr owthcycles from collections of recruit s.

Vitellogenesis in L. sinuensis wa s

evident in coloration an d size cha nges

of ovar ies viewed through a t ra nslu-

cent r egion of th e cuticle, as in other

thalassinid species (Hailstone and

Stephenson, 1961; Forbes , 1977;

Felder a nd Lovett , 1989). The pat ter n

of change in L. sinuensis over the

course of matur ation is as m uch as

that reported for L . louisianensis ,

with ovar ies becoming more ma ssive

and opaque as mat ura tion advan ces(Felder and Lovett, 1989). However,

when tra cked as an a nnu al index of

repr oductive a ctivity, rela tive ovarian

width in L. s inuensis at no point

reached the highest mean values re-

ported for L. louisianensis (even af-

ter corr ecting m isplaced decimals in

t h e y-axis of Fig. 1 of Felder and

Lovett [1989]). We su ggest th at th is

reflects year-round repr oductive ac-

tivity in L. sinuensis , rather than in-

vestment in a more punctuated tem-

perature-modulated event as might

be expected in temperat e latitudes.

I t may also account for a greater

nu mber of eggs on ovigerous females

of L. louisianensis (598 212; n=4)

th an on ovigerous fema les of the year-

round reproducing L. sinuensis (251

18; n=444) (Nat es et al., 1997). Even

so, significant fluctuations in mean

values for r elative ovarian width did

occur over the three years that we

monitored th is value in L. sinuensis ,

with highest valu es preceding maxi-mu m abu nda nce of ovigerous females

by two to three months.

In tropical nearshore decapods, it

is comm on to ha ve extended periods

of r ep roduc t i on w i thou t d i s t i nc t

peaks defined by seasonal tempera -

ture (Sas t ry , 1983; Stee le , 1988;

Bauer, 1992; Mouton and Felder ,

1995). However, whether modulat ed

by temperatu re or other factors, an-


12/16


Figure 7

Linear r egression (by least squ ar es estima te for un tra nsformed data ) of wet weight

(WW) on car apa ce length (CL) for ma les (A) and females (B ) in sa mpled Colom-

bian populations of Lepidophthalmus sinuensis, December 1991 through Decem-

ber 1995. The transition point at which data are subdivided, estimated by piece-

wise linear-linear polynomial regression, was positioned to minimize the sum of

squares of residuals.

nu al cycles in a vailability of nu-

trition m ay determine potential

for vitellogenesis and success of

larvae (Zimmerman and Felder,

1991; Mout on an d Felder, 1995).

Although temperatur e was n ot

subject t o ma rked fluctuat ion inthe shr imp farm habi ta t of L .

s inuens i s, i t did vary sl ight ly

with the ann ual chan ges in rain-

fall patt erns tha t determined sa-

linity of the upper estuary (Fig.

4A). The a nn ua l decline in salin-

ity from April through October

reflected increased input of nu-

t r ient - loaded waters f rom the

nearby Ro Sin which was re-

ported t o result in per iodic eleva-

tion of penaeid shrimp growth

rates on the Agrosoledad farm(Mogolln1). Similarly, such low

salinity periods may have pro-

du ced improved condit ions for vi-

tellogenesis inL. sinuensis . Peak

development of ovaries in the

first quarter of the typical year

either coincided with or shortly

fol lowed lowest mean sal ini ty

during th e last qua rter of the pre-

vious year , and fel l markedly just af ter sal ini ty

peak ed. The abu nda nce of ovigerous females peak ed

almost simu ltan eously with salinity in most years of

the stu dy and a decrease in mea n ovarian width im-

mediately followed, indicating that the abundance

of fema les with sp ent ovar ies was n ot offset by other

females simulta neously under going vigorous ovar ian

development. Reduced vitellogenesis following the

high salinity period was also suggested by the ma rk-

edly reduced mean nu mber of eggs per clutch foun d

in th ose ovigerous females th at occurred from May

thr ough J uly.

Growth and sexual maturation

Among calliana ssids and other tha lassinid shr imp,th e ma jor chela is used comm only for aggressive in-

teractions between captured individuals th at are h eld

together or among individua ls encoun terin g one an -

other wh ere bur rows intersect in laborat ory fossoria

(MacGinitie, 1934; Pearse, 1945; Rodrigues, 1976;

Tunber g, 1986; Felder an d Lovett, 1989; Pillai, 1990;

Rowden an d J ones, 1994). Cont ra ry to th e case with

man y other genera, both males an d females ofLepi-

dophthalmus have one chela enlarged, but th e ma-

jor chela of mature males is much more strikingly

developed tha n t hat of matur e females (Felder an d

Rodrigues, 1993; Felder a nd Man ning, 1997). Sexual

dimorphism of the chelae in decapods is generally

th ought to reflect adapt at ions for th eir use, especially

by males, in comba t, display, and court ship (Har tn oll,

1974). The enlarged chela can play a r ole in inter ma le

competition during the precopulatory phase of the

life cycle, and m ar ked cha nge in its a llomet ric growth

rat e is frequently related to functional sexual m atu -

rit y (Grey, 1979; Aiken a nd Waddy, 1989; Claxt on an d

Govind, 1994; Gu et a l., 1994; Robert son an d Kru ger,

1994). This is likely also th e case in L. sinuensis , eventhough we can only speculate as to the exact role

th is appen dage plays in such fossorial populat ions.

A str iking tra nsition ta kes place in ra te of relat ive

growth for t he m ajor chela in L. sinuensis, and there

is an allometric divergence between males and fe-

males in the sh ape of this appenda ge at sizes th at

exceed a defined, transitional carapace length. For

th e most par t, th e relationships of slopes above an d

below these tra nsition or ma tu ra tion points are simi-

lar t o relationsh ips previously reported in m onitored1 Mogolln, J. V. 1995. Agrosoledad S. A., Playa de la Arti l lera

no. 3336, Car tagena, Columbia. Personal commun.


13/16


populations ofL. louisianensis from the n orth ern Gulf

of Mexico (Felder and Lovett, 1989). In relative

growth parameters of the major chela, when scaled

to carapace length , males and females of both

Lepidophthalmus species are much more similar to

one another a t sizes below tra nsition points tha n a t

sizes exceeding th ose point s.The estimated mat ura tional tr ansition size in male

L. sinuensis ra nges from 11.0 to 11.3 mm CL, whet her

based u pon regression an alysis of relative growth in

chela width, chela height, or wet weight . The ran ge

of these values is markedly less than tha t r eported

in L. louisianensis (15.5 mm CL), a warm -temper-

at e congener (Felder a nd Lovett, 1989). In a ll of these

measures, postmaturation growth rate in males is

more positively allometr ic and s ignifican tly great er

tha n postmatu rat ion growth r ate in females, as ha s

been shown in ma ny other decapods (Ha rt noll, 1978,

1982). Although relat ive weight increases wer e posi-

tively allometric in both males and females of ma-tu re size, th e positive allometr y of growth in size of

the major chela, accompanied by sex-dependent

chan ges in its sh ape, appea rs to account for postma -

tur ation rat es of weight increase in ma les that sig-

nificantly exceeding those of females. Weight ac-

cumulat ion d ue t o massive but episodic development

of ovaries in maturing females would appear to be

somewhat offset by the simultaneous trend toward

negat ive allometr ic growth of the m ajor chela.

Estimat ed from the ma jor chela measu rements, the

mean mat ura tional size in femaleL. sinuensis ranges

from 10.8 to 11.2 mm CL, or slightly less tha n t ha t of

ma les but very nea r th e values reported for females

of L. louisianensis, which ranged from 10.7 to 11.0

mm CL (Felder an d Lovett , 1989). Becau se over 99%

of th e ovigerous females we collected were 11.0 mm

CL, the general validity of this mean size estimate

for maturation appears to be confirmed on an inde-

pendent basis, even though two atypically small

ovigerous females


14/16


ticide Sevin , a practice unlikely to change in the

absence of proven alterna tive management stra te-

gies. Fr om our observat ions, such a pplicat ions h ave

usually been contained within drained or slightly

filled cult ur e ponds a nd limit ed only to contr ol of ex-

cessive thalassinid densities. It is possible that re-

ductions in frequencies of such app licat ions can beachieved by timing of tr eatm ent s to pre-empt r epro-

ductive peaks or by limiting pesticide applications

only to infestations that are found to include high

percenta ges of ma tu re or nea r-mat ur e females, such

as we observed in t his stu dy most often in t he four th

ann ual quar ter. Any measur e tha t r educes applica-

tion ra tes a nd frequ encies may lessen ecological risks

an d cont ribut e to effectiveness of carbar yl degra da-

tion prior to flushing treated ponds into surround-

ing environment s.

Acknowledgments

We thank G. T. Rizzuto, R. G. Jaeger, P. L. Klerks,

an d R. R. Twilley, Univers ity of Sout hwes ter n Loui-

siana , an d R. Lemaitr e, Smith sonian Inst itut ion, for

comm ents on earlier versions of th e ma nu script. We

are also grateful to many associates of the Agro-

so ledad S . A. sh r imp f a rm , pa r t i cu l a r l y J . V.

Mogolln , L. Mogolln, G. Moreno, and M. Torr a lvo,

who pr ovided a ccess t o sites in Colombia, an d A. Ar-

royo, D. Espitia, an d S. Gar cia, who a ssisted in col-

lecting population data there. Among others who

assist ed with field and laborat ory work, we tha nk L.Borda, R. Bourgeois , V. Fu ent es, R. Griff is , R.

Lemaitre, C. Moreau, S. de A. Rodrigues, and K.

Str asser. Fellowship su pport for th is project was pro-

vided to S. F. Nat es from t he In stitu to Colombian o

pa ra el Desar rollo de la Ciencia y la Tecnologa Fr an -

cisco Jos de Caldas (COLCIENCIAS), Colombia.

Logistical supp ort was provided th rough ACUANAL,

BANCOLDEX, and the efforts of C. M. Sann. Sup-

port was provided to D. L. Felder t hr ough U.S. Min-

erals Management Service Cooperative Agreement

14-35-0001-30470, U.S. Fish and Wildlife Service

Cooperative Agreement 14-16-0009-89-96Task

Order No. 6, NOAA Louisiana Sea Grant CollegeProgram Grant R/CFB-21, and U.S. Depart ment of

En ergy Gran t No. DE-FG02-97ER12220.

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