A case of hermaphroditism in the freshwater invading bivalve Limnoperna fortunei (Dunker, 1857) (Mytilidae) from Rio de la Plata, Argentina

6 Pages·1998·2.8 MB·English

by  Gustavo A Darrigran

©
SociedadEspañola deMalacología Iberus, 16 (2): 99-104, 1998
A
case of hermaphroditism in the freshwater invading
bivalve Limnopernafortunei (Dunker, 1857) (Mytilidae)
from Río de la Plata, Argentina
Un caso de hermafroditismo en el bivalvo invasor Limnopernafor-
tunei (Dunker, 1857) (Mytilidae) en el Río de la Plata, Argentina
Gustavo A. DARRIGRAN*, M. Cristina DAMBORENEA* and Pablo E.
PENCHASZADEH**
Recibidoel24-IX-1997.Aceptadoel19-XII-1997
ABSTRACT
The SoutheastAsian freshwater mussel Limnoperna fortunei (Dunker, 1857) was first repor-
ted living in the Americas at Río de la Plata, Argentina, ¡n 1991 . Still earlier, it had ¡nva-
ded the Hong Kong área ¡n the late 'óOs and Japan in the '70s. í. fortunei is dioecious,
and no case of hermaphroditism have been previously reported. While studying the repro-
ductiva cycle ofthe Río de la Plata population ofthis species, three cases among 545 spe-
cimens studied were hermaphrodite representing only 0.55% of the total. In this contribu-
tion, a gonadal description of these cases of hermaphroditism in L. fortunei is presented.
The histoiogical study gave three kind of follicles, and their proportion in a hermaphrodite
individual v/as 21% testis, 19% ovarles and 60% with both types ofgametes.
RESUMEN
Limnoperna fortunei (Dunker, 1857) es un bivalvo originario del sudeste asiático y se regis-
tró por primera vez para el continente americano en 1991 en el Río de la Plata, Argentina.
Afinales de la decada del '60 había invadidoel área de Hong Kong yJapón en la del 70.
L. fortuneies una especie dioica, y no existe registro de casos de hermafroditismo. Durante
el estudio del ciclo reproductivo de una población de esta especie en el Río de la Plata, se
hallaron tres ejemplares hermafroditas entre 545 estudiados, representando sólo el 0,55%
del total. En esta contribución, se presenta una descripción gonadal de los ejemplares her-
mafroditas. Atroves del estudio histológico se distinguen tres tipos de folículos y la propor-
ción de Estos en el ejemplar hermafrodita es 21% testículos, 19% de ovarios y 60% de fo-
lículos con ambos tipos de gametas.
KEYWORDS:Limnopernafortunei,hermaphroditism, invadingbivalve,Neotropicalregión; RíodelaPlata.
PALABRASCLAVE:Limnopernafortunei,hermafroditismo,bivalvoinvasor,regiónNeotropical,RíodelaPlata.
INTRODUCTION
The Southeast Asian freshwater 1857) was first reported living in the
mussel Limnoperna fortunei (Dunker, Americas atRío de la Platain 1991 (Pas-
*Depto. Científico Zoología Invertebrados, Museo de La Plata, Paseo del Bosque s/n (1900) La Plata,
Argentina,CONICET.e-mail: [email protected]
**FacultaddeCienciasExactasyNaturales, UBA, BuenosAires,Argentina, CONICET.
99
Iberus, 16 (2), 1998
TORINO, DaRRIGRAN, MaRTÍN AND RESULTS
LuNASCHi, 1993), where from a mean
m
densityof5individuáispersq in 1991 The gonad of Limnopernafortunei, as
it increased to 80.000 per sq ra in 1993 in other Mytilidae, is very simple con-
(Darrigran and Pastorino, 1995). Still sisting of numerous difuse follicles in
earlier, it had invaded the Hong Kong the mantle and in the visceral mass.
área in the late '60s (Morton, 1977) and Three cases among 545 specimens
Japan in the '70s (Kimura, 1994). The studied were hermaphrodite, represen-
Hong Kong population of L.fortunei is tingonlythe0.55%ofthetotal.
dioecious, and no case ofhermaphrodi- The proportion ofthe follicles inthe
tismhavebeenreported (Morton, 1982, hermaphroditeindividualwas21%testis,
1991). During a study on the reproduc- 19% ovarles and 60% withboth types of
tiva cycle ofthe Río de la Plata popula- gametes.Thesethreekindoffollicleswere
tion of this species, three cases of her- present mainly in the mantle, filling
maphroditism were found. In this con- between30and40%ofthetissue,therest
tribution, a description of these cases of ofwhich was connective tissue (Fig. 1).
hermaphroditisminL.fortuneiispresen- Only a low proportion of follicles was
ted. presentinthevisceralmass.
The 55% of male follicles were at a
late developmental stage with full of
MATERIALAND METHODS mature spermatozoa, and with eviden-
ces of partial emission. In the other 45%
The hermaphrodite specimens (shell of male follicles, no spermatozoa were
length 17.0, 0.9 and 14.0 mm) were distinguishable, and a proliferation
sampled onFebruary28* April 24* and stagewas recognizable.
September 28* 1994, at Balneario The 63% offemale follicles were ina
Bagliardi (34° 55' S, 57° 49' W), Río de la proliferation stage or partially spent. In
Plata, Argentina, Neotropical región. the other 37% clear signs ofnecrosis of
Thematerialwasfixed inZenker-forma- nonevacuated gametes and resorption
lin solution, dehydrated and embedded were seen, especially onthose inthe vis-
in paraffin; sections were cut at 7.5 ceralmass.
microns, and stained with hematoxylin- The presence of male and female
eosinstandards. cells in the same follicle, was the most
Sixty-six (66) microscope fields common situation. In these follicles
(lOOX) were examined, and the propor- were male zones with maturing sperm
tion of male and female follicles as well and some with mature spermatozoa, as
as the presence ofboth male and female in the male follicles described above, as
gametes within a follicle were estima- well as female zones showing different
ted. The maturation stages were recog- degrees of development, with a preva-
nized using Lubet's (1959) scale. The lence of young oocytes and some
present description is based on the middle size oocytes attached tothefolli-
Febreruary's specimen. Its body was cle wall. In very few cases, oocytes
divided into three regions: one anterior bigger than 50 microns were observed,
to the byssus gland, a middle región alwaysfreeinthefolliclelumen.
with byssus filaments and other poste- From 66 fields of visión, 53 of which
riortothebyssus. present follicles with both male and
The oocyte size of the hermaphro- female cells. Nevertheless, differences in
dite individual was compared with the the relative proportions of the three
sizes observed in the females of the kindsoffollicleswererecognizedinrela-
same sample (length range from 11.0 to tiontothepositionintheanimal (Fig. 2).
18.0 mm), measuring the largest diame- In the anterior and middle región, and
terofeachoocytewith a distinctnucleo- especially in the mantle, follicles with
lus, for this comparative purpose a both male and female cells dominated
Studentttestwasused. (75and82%respectively),butinthepos-
00
Darrigran ETAL.: Hermaphroditism in Lhnnopernafortuneifrom Río de la Plata
í^^^r
*©*^
V
V
. ,
Figure 1. Limnopernafortimeifrom Río delaPlata.Transverse sections ofan adult male, an adult
femaleandanhermaphroditespecimen;fromasampletakenonthe28thFeb. 1994.A:welldevelo-
pedmalewithfoUiclesfillingthemandetissue;B:welldevelopedfemalewithfolliclesfillingtheman-
de tissue; C: hermaphroditespecimenshowingawelldevelopedfemalefollicleandsmall male folli-
cles; D: hermaphroditespecimen showingsepáratewell developed male and female follicles; E: her-
maphroditespecimensshowingmaleandfemalegametes inthesamefollicles. Scalebars 100pm.
Figura 1. Limnoperna fortuneidelRíodelaPlata. Seccio7íestransversalesdeun machoadulto, una
hembraadultaydelejemplarhermafrotita;deunamuestradel28defebrerode1994.A:machomaduro
confolíctdosocupandoeltejidodelmanto;B:hembramaduraconfolículosocupandoeltejidodelmanto;
C:espécimenhermafoditaconunfolículofemeninobiendesarrolladoyfolículosmasculinospequeños;D:
espécimenhermafoditamostrandofolículosfemeninosymasculinosseparadosybiendesarrollados;E:espé-
cimenhermafoditamostrandogametosfemeninasymascidinasenelmismofolícido. Escalas100¡im.
Iberus, 16 (2), 1998
anteriorregión posteriorregión
Figure 2. Limnopernafortunei from Río de la Plata. Distribution ofgonadic follicles in the her-
maphroditeanimal body.
Figura2. LimnopernafortuneidelRío de laPlata. Distribución delosfolicidosgonadalesen elcuerpo
delanimalhermafrodita.
terior part of the animal they represen- zed environment in the Rio de la Plata.
ted only 8%, while the female follicles This report of hermaphroditism is the
49% andthemalefollicles43%. firstoneforthespecies.
Adult males of the population from The observed percentage of her-
the same saniple (Feb. 28*, 1994) are maphroditismisaboutthesamefoundin
mature and had partially spent, howe- the other generally dioicious species of
ver abundant cell proliferation is obser- bivalves, i. e. Placopecten magellanicus
ved. The follicles filled mostofthe man- (Gmelin, 1791) 1.3% (Naidu, 1970); Cras-
tle tissue (70%).Adulttémales ofthe po- sostrea virginica (Gmelin, 1791) 0.4%
pulation, showed signáis of partial (Kennedy,1983);Anadaragranosa(Linna-
emission, and in some cases, maturing eus,1758)0.3%(Broom,1983);Pernaviridis
oocytes, the follicles occupe 60-70% of (Linnaeus,1758)0.1%(Lee,1988);Mytilus
themantletissue. The observedmodeof edulis(Linnaeus,1758)0.1%(Sunila,1981).
the oocyte size was larger in the normal The presence of intermingled male
animáis in comparison to the hermaph- and female follicles is one, among other
rodite one (Fig. 3). Inthehermaphrodite arrangement patterns, recorded in her-
specimen, the largest oocytes were maphroditebivalve species, i. e. inLaevi-
found in the exclusively female follicles cardium laevigatum (Linneaus, 1758)
(mean diameterof47microns, SD= 19.2, where male follicles first developed,
n= 154) while the oocytes in the mixed ovarían follicles appear from peripheral
follicles were much smaller (mean dia- points ofthe testicular follicles, resulting
meter27microns, SD= 11.1;n=227). The in a simultaneous hermaphrodite (Pen-
mean oocyte diameter in both kinds of CHASZADEH AND Salaya, 1983). In the
follicles was significantly different (F= case reported here, three kinds ofinter-
3.0073; d. f. = 177;P< 0.001). mingled follicles were found: male folli-
cles, female follicles and follicles with
both male and female gametes. Most of
DISCUSSION the male follicles and female follicles
werealreadypartially spent. Mixedfolli-
Limnoperna fortunei is a dioecious cles, on the contrary showed a prolifera-
species in its habitat at Hong Kong área tionofmalecells.Thedevelopmentstage
(MoRTON, 1982) and in its newly coloni- inthemalefolliclesandfemalefolliclesof
02
DarriGRAN ETal.: Hermaphroditism in Limnopernafortuneifrom Río de la Plata
H
adultfemalefoUicles;n=280
40
LJhermaphroditespecimen,femalefollicles; n=154
H
hermaphroditespecimen,mixedfollicles;n=227
KK
I
njl \ \ I Lll
\\ \ i^n ,1
o 10 20 30 40 50 60 70 80 90 100 110 120 130
Oocytesize(microns)
Figure 3. Limnopernafortuneifrom Río de la Plata. Oocyte size frequencydistribution in the her-
maphroditespecimen comparedwithooc)'tes in adultfemalessampledat thesamedate (Feb. 28'^,
1994).
Figura3- LirrMiopernafortunei delRíodelaPlata. Distribucióndefrecuenciasdelatallaoocitariadel
ejemplarhermafroditacomparado con ladelashembrasadultasdeigualfecha (28Feb. 1994).
the hermaphrodite, is coincident in Lee, 1988); and Limnopernafortuneiisnot
general terms, with the observations anexceptionamongthem.
made on the normal dioecious indivi- The observation of both male and
duáis of the same population sample. females gametes present in the same
Nevertheless the mantle occupation by follicle is similar to the observations
the follicles is lower in the hermaphro- made in unusual hermaphrodites of
dite,aswellastheoocytediametermean, Crassostrea glomerata (Dinamani, 1974)
especiallythosefrommixedfollicles. and Pectén maximus (Mason, 1958),
Many freshwater species of bivalves and is a rare phenomena in the protan-
are hermaphroditic and brooding (i. e. dric hermaphrodite Laevicardium laeviga-
Sphaeriidae,someCorbiculidae)butthere tiim (PenchaszadehandSalaya, 1983).
aresomespecieswhichshowwideintras-
pecificvariabilityinsexualexpression,as
ACKNOWLEDGEMENTS
Corbiculafliiminea (Müller, 1774) in the
Holartic;others,asAnodontawoodiana(Lea,
1863)(Unionidae)andLimnopernafortunei We thank Dr. Patricia Miloslavich
(Mytilidae)aredioecious(Morton,1991). and Dr. Gladys Muñoz, fromUniversity
The dioecious condition is the main Simón Bolívar, Caracas, for reviewing
fact in Mytilidae, which includes mostly the manuscript. CONICET and Funda-
marine and estuarine species (Lubet, ción Antorchas (Argentina) partially
1959; LuNETTA, 1969; Nascimento, 1971; grantedthisresearch.
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04