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Invertebrate Reproduction and Development, 52:3 (2008) 123–130 123
Balaban, Philadelphia/Rehovot
0168-8170/08/$05.00 © 2008 Balaban
Reproductive strategy of the snapping shrimp Alpheus armillatus
H. Milne-Edwards, 1837 in the South Atlantic:
fecundity, egg features, and reproductive output
CAIO A.M. PAVANELLI1*, EMERSON C. MOSSOLIN2 and FERNANDO L. MANTELATTO3
Laboratory of Bioecology and Crustacean Systematics (LBSC), Department of Biology, Faculty of Philosophy,
Science and Letters of Ribeirão Preto (FFCLRP), University of São Paulo (USP),
Av. Bandeirantes 3900, CEP 14040-901, Ribeirão Preto (SP), Brazil
Fax: + 55 16 3602 4396, email: capavanelli@yahoo.com.br1; ecmossolin@yahoo.com.br2; flmantel@usp.br3
Received 18 April 2008; Accepted 28 January 2009
Summary
The family Alpheidae, composed by shrimps of relatively small size, popularly known as snapping
shrimps, is the one of the most diverse decapod groups. These shrimps are found worldwide and
occur in tropical and subtropical waters, from the intertidal zone to great depths. We investigated
reproductive aspects of Alpheus armillatus, in order to gather information on egg production,
aiming to enhance knowledge of its reproductive strategies in a population in an intertidal area of
the South Atlantic. Ovigerous females were collected under rocks, in May and July 2006 (dry
season) and in November 2006 and March 2007 (rainy season). Egg production and reproductive
output were analyzed and compared seasonally and during the period of embryonic development.
Females measured on average 11.28 mm CL, with a mean of 763 eggs and 0.11 mm3 egg volume.
The egg volume of this population was smaller than previous estimates for other species of
snapping shrimps, but the mean egg number was higher. The volume of eggs doubled during the
incubation period, but despite this increase, no significant loss of eggs was observed. Alpheus
armillatus invests on average about 12% of body weight in reproduction. The proportional
investment in egg production is significantly higher in the rainy season when compared with the
dry season (17.9% vs 4.8%), correlated with higher temperatures and increased food availability at
this time. Our results corroborated the hypothesis of a pattern of egg production influenced by
environmental conditions and intraspecific variability among the family Alpheidae, as a function
of the biogeographic region.
Key words: Egg mass, reproduction, reproductive output, Alpheus armillatus, shrimp
Introduction
Caridean shrimps of the family Alpheidae Rafi-
nesque, 1815 are one of the most important, numerous
and ecologically diverse groups among the decapods
(Anker and Dworschak, 2007). Alpheus Fabricius, 1798
is the largest genus of this family, and probably of the
order Decapoda Latreille, 1802; it currently contains
more than 250 species worldwide (Nomura and Anker,
2005). At least 40 of these species occur in the western
Atlantic, inhabiting tropical and subtropical waters,
from intertidal regions to great depths (Christoffersen,
1980).
C.A.M. Pavanelli et al. / IRD 52 (2008) 123–130
124
The shrimps pertaining to this genus possess, as one
of their main characteristics, one of the chelipeds of the
first pair of pereopods, well developed and endowed
with a complex mechanism of dactyl movement. This
structure is responsible for producing a snapping sound
and for emitting a small but powerful forward-directed
jet of water, which are important for intraspecific
communication and agonistic interactions (Versluis et
al., 2000).
Alpheus armillatus H. Milne Edwards, 1837 has a
wide geographic distribution in the western Atlantic
(Christoffersen, 1998) from the intertidal zone to 16.5 m
depth. It is common in estuarine regions, on reefs and
among rocks (Christoffersen, 1980). This species is
frequently found in pairs, and shows territorial behavior
(Nolan and Salmon, 1970).
Considering the great diversity and ample geo-
graphic distribution of the members of the family
Alpheidae, there are still relatively few studies on this
group. Researchers concerned with species of this
family have focused mainly on taxonomy (Christof-
fersen 1979, 1980, 1982; Anker, 2000; Nomura and
Anker, 2005; Anker and Dworschak, 2007), geographic
distribution (Christoffersen, 1998; Coelho et al., 2006)
and ecology (Fernández-Muñoz and Garcia-Raso, 1987;
Bauer, 1989, 1991; Corey and Reid, 1991; Mossolin et
al., 2006).
Despite the importance of reproductive aspects of
alpheids, there is little essential information on their life
history. The diversity of this group makes it important to
more fully understand intraspecific variations and the
adoption of different strategies for the maintenance of
natural populations in certain areas, especially in highly
variable environments such as intertidal rocky shores. In
the South Atlantic, investigations on alpheids are even
scarcer, with no previous studies on the reproduction of
this group.
We evaluated the reproductive strategy of A. armil-
latus on São Francisco Beach on the northern coast of
São Paulo State, Brazil. We analyzed egg production,
reproductive output, the seasonal variation of these
features, and the variation in volume and number of
developing eggs during the different stages of the
incubation period in order to enhance our knowledge of
the life-cycle strategies of a population of this species
living in an intertidal area.
Materials and Methods
Collection and analysis of specimens
Ovigerous female snapping shrimp were sampled
in May, July and November 2006 and March 2007
from the intertidal zone of São Francisco Beach
(23E44N53.6OS, 045E24N33.6OW), on the northern coast
of the state of São Paulo, Brazil. Samples were taken
during low tide, and the shrimp were collected by hand,
by two people, moving all rocks of the exposed
substratum in an area of approximately 600 m2.
After collection, the shrimp were frozen and trans-
ported to the laboratory where they were thawed just
before analysis. The carapace length (CL), from rostrum
tip to the posterior dorsal margin, of each specimen, was
measured with a caliper rule (0.1 mm). The animals
were fixed in 70–80% EtOH. Voucher specimens were
deposited in the Crustacean Collection of the Depart-
ment of Biology, Faculty of Philosophy, Sciences and
Letters of Ribeirão Preto (CCDB/FFCLRP/USP) and in
the Museum of Zoology of São Paulo University
(MZUSP), under catalogue numbers CCDB 1974 and
MZUSP 18008, respectively.
Egg production and reproductive output
Ovigerous females were classified according to the
developmental stage of the eggs, following the
methodology proposed by Mossolin et al. (2006):
CInitial Stage I: no evidence of compound eye
development, and yolk occupying 75–100% of egg
volume;
CIntermediate Stage II: eyes small and elongate, and
yolk occupying 50–75% of egg volume;
CFinal Stage III: well-developed compound eyes, and
yolk occupying 25–50% of egg volume.
To avoid possible egg loss and change in egg volume
during incubation and embryonic development, only
females with recently produced eggs (Stage I) were
included in the fecundity analysis.
Eggs were carefully removed from the pleopods and
counted in their totality under a stereomicroscope. A
sub-sample of 15 eggs of each female had the minimum
and maximum diameters measured, to calculate the
mean volume, using the formula v = 1/6 × π x (d1)² × d2
where v = embryo volume (mm³), d1 = lesser diameter
and d2 = greater diameter (Bauer, 1991). Measurements
were taken under a stereomicroscope with the aid of a
camera lucida. This methodology was applied to eggs at
the three developmental stages to verify changes in the
number, volume and shape of eggs during the incu-
bation period.
The samples were washed in distilled water, and the
wet and dry weights of females and egg masses at the
initial stage were determined using an analytical
balance. Dry weights were obtained after 48 h for
females, and 24 h for egg masses, in an oven at 50EC
(Mantelatto et al., 2002).
The reproductive output index (RO: weight of total
egg mass of the female/weight of the female) was
C.A.M. Pavanelli et al. / IRD 52 (2008) 123–130 125
calculated for dry weight of females with eggs at the
initial stage, according to Clarke et al. (1991).
Sample months were grouped into two seasons, dry
(May and July 2006) and rainy (November 2006 and
March 2007), in order to assess the data in a seasonal
context. Nonparametric procedures were adopted when-
ever the premises of the parametric test were not
fulfilled. The analyses were carried out with the use of
the Sigma Stat® Windows software, version 2.03. A one-
way analysis of variance test (ANOVA) was used to
assess the seasonal variation in the females’ size.
Fecundity and egg volume variation during the incu-
bation period were tested using the analysis of
covariance test (ANCOVA) and Duncan’s multiple
range test a posteriori. The last test was also used to
assess the seasonal variation in fecundity, egg volume,
and reproductive output.
The Spearman correlation was used to analyze the
relationships of female size with fecundity and egg
volume, and between female weight and fecundity. All
statistical analyses were based on producers described
by Zar (1996).
Results
In total, 125 ovigerous females with eggs at different
developmental stages were collected. Of these, 56.0%
were at the initial stage, 21.6% at the intermediate stage,
and 22.4% at the final stage.
The mean size of all 125 ovigerous females was
11.3 ± 1.4 mm CL, ranging from 7.7 mm to 14.1 mm
(Fig. 1). The female’s size did not vary significantly
between seasons and among different stages of embry-
onic development (ANCOVA, F = 56.70; P <0.0001
and F = 21.84; P <0.0001, respectively).
Egg production
The mean fecundity of ovigerous females was 763
488 eggs (n = 70), ranging from 42 (CL = 7.7 mm) to
1979 (CL = 13.2 mm). Mean fecundity was significantly
higher in the rainy season (1061 408 eggs) than in the
dry season (388 278 eggs) (Mann–Whitney T = 601.0;
P #0.001). Egg number was correlated significantly
with CL (Spearman correlation r = 0.59) (Fig. 2) and
wet weight of females (Spearman correlation r = 0.73),
increasing with these dimensions.
For females that carried eggs at other stages of
development, the mean egg number decreased (Table 1).
However, these were not significant (Kruskal–Wallis
H = 0.606; P= 0.739), indicating that there were no
significant egg losses during the incubation period.
The mean diameters of eggs at the initial develop-
mental stage were 0.57 ± 0.03 vs. 0.60 ± 0.04 mm, or a
mean volume of 0.10 ± 0.02 mm³. Egg diameters and
volume did not show a significant relationship with
either the CL of the females (Spearman correlation r =
0.00) or with seasonal variation (Mann–Whitney T =
1229.5; P = 0.129).
During the incubation period, the mass of eggs
changed significantly in shape, ranging from almost
spherical to ellipsoid; and also in volume (Kruskal-
Wallis H = 55,78494; P = 0.000) (Table 1). The egg
mass increased 33.3% from stage I to stage II, and
23.3% from stage II to stage III of development, with a
total increase in volume of 64.3%.
Fig. 1. Alpheus armillatus. Size–frequency distribution of ovigerous females from São Francisco Beach, São Sebastião (SP),
Brazil.
C.A.M. Pavanelli et al. / IRD 52 (2008) 123–130
126
Fig. 2. Alpheus armillatus. Correlation between carapace length (mm) and fecundity (only eggs at the initial developmental
stage) of ovigerous females from São Francisco Beach, São Sebastião (SP), Brazil.
Table 1. Alpheus armillatus. Fecundity and egg size variation
in the three developmental stages of embryogenesis of
females collected from São Francisco Beach, São Sebastião
(SP), Brazil
Fecundity Egg volume (mm³)
n Mean SD Mean SD
Stage I 70 763 488 0.10 0.02
Stage II 27 740 494 0.14 0.03
Stage III 28 670 441 0.17 0.04
Reproductive output
The RO of A. armillatus was 0.121 ± 0.094 or, on
average, 12.1% of body weight of females was invested
in egg production. The RO also was significantly dif-
ferent (Mann–Whitney T = 571.5; P # 0.001) between
the two seasons. In the rainy season, females invested
more in reproduction (17.9%) than in the dry season
(4.8%).
Discussion
The reproductive strategy adopted by A. armillatus is
marked by extrusion of small but numerous eggs, with
optimization of this production during the Rainy season.
At this time of year, conditions are extremely favorable
for egg production, with higher temperatures and greater
food availability.
Egg production
The fecundity estimated for this southwestern
Atlantic population of A. armillatus is almost three
times higher than estimates for other, related species in
the family Alpheidae (Table 2). Among many variables,
the number of eggs exteriorized by the female can vary
due to genetics and environmental factors such as
temperature, salinity, food availability, photoperiod,
lunar cycle, and latitude (Thorson, 1950; Sastry, 1983;
Clarke et al., 1991; Lardies and Castilla, 2001; Lardies
and Wehrtmann, 2001; Litulo et al., 2005).
The size of females is another very important
component correlated with egg number production
(Mantelatto and Fransozo, 1997). Female size influ-
ences the physical space available for the egg mass in
the abdomen and in the cephalothoracic space (which
influences the ovary development), which are limiting
factors for egg production in decapods (Bauer, 1991;
Corey and Reid, 1991). The mean size of females
collected on São Francisco Beach was larger than
described in the literature (Table 2), which confirms that
an increase in female size permits an increase in egg
production as well. This relationship was previously
reported by several authors for members of the Caridea
Dana, 1852 (Shakuntala, 1977; Balasundaram and
Pandian, 1982; Corey and Reid, 1991; Lardies and
Wehrtmann, 1997) and other groups including
Brachyura Latreille, 1802 (Hines, 1988; Mantelatto and
Fransozo, 1997; Pinheiro and Terceiro, 2000; Litulo et
al., 2005) and Anomura MacLeay, 1838 (Mantelatto and
Garcia, 1999; Hernáez and Palma, 2003; Miranda et al.,
2006; Torati and Mantelatto, 2008).
In the present study, we observed that practically all
the females were ovigerous in both seasons and carried
eggs at different stages of development. Moreover,
females containing eggs near to hatching had already
mature ovaries (ECM, unpublished data) and it can
C.A.M. Pavanelli et al. / IRD 52 (2008) 123–130 127
Table 2. Size, fecundity, egg volume, and reproductive output of females of species of the family Alpheidae, from literature sources
and the present study (CL = carapace length; FEC = fecundity; EV = egg volume; RO = reproductive output)
Species N CL (mm) FEC EV
(mm3)
RO Locality Reference
Min Max Min Max
Alpheus armillatus 4 7.4 8.8 146 504 0.18 — Florida, USA Corey and Reid (1991)
Alpheus armillatus 31 7.7 14.1 42 1979 0.1 0.121 São Paulo, Brazil Present Study
Alpheus dentipes — — — — 836 — — Malaga, Spain Fernández-Muñoz and
Garcia-Raso (1987)
Alpheus heterochaelis 5 10.2 13,4 133 336 0.91 — Florida, USA Corey and Reid (1991)
Alpheus normanni 35 — — — — 0.03 — Puerto Rico Bauer (1991)
Alpheus normanni 7 4.1 7.4 68 584 0.09 — Florida, USA Corey and Reid (1991)
Alpheus saxidomus 5 10.1 17.4*— — 0.25 0.44 Pacific Costa Rica Wehrtmann and Graeve
(1998)
Betaeus emarginatus 38 9.0 16.3*94 615 0.21 0.09 Valdivia, Chile Lardies and Wehrtmann
(1997)
Betaeus truncatus 25 5.3 11.7*— 1067 0.06 0.07 Guanaquero, Chile Lardies and Wehrtmann
(2001)
Betaeus truncatus 19 — 8.9*— 498 0.09 0.13 Metri, Chile Lardies and Wehrtmann
(2001)
Betaeus truncatus 57 6.54 —*— 731 0.1 0.18 Putemún, Chile Lardies and Wehrtmann
(2001)
Synalpheus agelas 5 4.2 5.6 16 65 0.27 — Gulf of Mexico Corey and Reid (1991)
Synalpheus brooksi 10 3.4 4.5 3 11 0.5 — Florida, USA Corey and Reid (1991)
Synalpheus fritzmuelleri 13 3.8 6.5 39 484 0.09 — Florida, USA Corey and Reid (1991)
Synalpheus herricki 4 3.5 5.1 11 81 0.22 — Florida, USA Corey and Reid (1991)
Synalpheus longicarpus 21 5.5 8.0 27 349 0.17 — Florida, USA Corey and Reid (1991)
Synalpheus pectiniger 31 3.5 4.6 4 17 0.75 — Florida, USA Corey and Reid (1991)
*Including all stages of embryonic development.
therefore be inferred that the females of this population
are continuously reproductive.
Several authors have reported egg losses of up to
36% in caridean shrimps during the developmental
process (Balasundaram and Pandian, 1982; Corey and
Reid, 1991; Lardies and Wehrtmann, 1996, 1997). In
contrast, we did not observe similar levels of egg losses
in this population of A. armillatus. This evidences the
presence of efficient parental care, probably related to
female morphology, in which the space available for the
eggs under the abdomen is sufficient to accommodate
the number of eggs produced until they hatch, and also
as a function of the presence of a male with the female,
as a territorial behavior for protection.
A. armillatus has noticably small eggs within the
genus, being that only A. normanni has a lesser embryo
volume. Compared to other alpheids of tropical and
subtropical waters, this population also show a small
embryo volume (Table 2). Egg size is not determined
only by genetics, but may also be affected by many
selective environmental pressures, which can influence
the reproductive investment and larval development of
each species (Bauer, 1991). These several limiting
features for the production of eggs in decapods can be
modified by adoption of different reproduction strate-
gies within the same group (Corey and Reid, 1991). One
of the reported mechanisms is the inverse relationship
between egg volume and fecundity. For the same
amount of energy invested in egg production, a species
can produce smaller but more numerous eggs, or larger
and fewer eggs (Christiansen and Fenchel, 1979), which
was reported for Chilean snapping shrimps by Lardies
and Wehrtmann (2001).
During the incubation period, the eggs of A. armil-
latus showed changes in form and a constant increase in
volume. In many decapods, recently extruded eggs are
spherical (Yamaguchi, 2001; García-Guerrero and
Hendrickx, 2004), and become ellipsoidal by the end of
development, also increasing in volume. The total
percentage increase (64.3% from the first to the final
stage of development) is moderate compared with other
alpheids such as A. normanni, Synalpheus brooksi
Coutière, 1909, S. fritzmuelleri and S. longicarpus
Herrick, 1891 (Corey and Reid, 1991), B. emarginatus
and B. truncatus (Lardies and Wehrtmann, 1997 and
2001, respectively) from different regions, with reported
increases up to 274%.
The increase in egg volume occurs in response to the
C.A.M. Pavanelli et al. / IRD 52 (2008) 123–130
128
increase in size of the embryo itself, and to the chamber
pressure (Wear, 1974), which is controlled by the
thickness and resistance of its membranes (Lardies and
Wehrtmann, 1996). During the final developmental
stage, the eggs take up water more quickly, because of a
change in the permeability of the membranes, regulating
the osmotic pressure and facilitating the rupture of the
membranes during hatching. In decapods that inhabit
intertidal regions, where they are subject to desiccation
at certain phases of the tidal cycle, this mechanism is of
great importance. It would offer an ecophysiological
advantage in protecting the embryo from environmental
variations, being responsible for the regulation of the
balance between internal and external fluids, acting as
an internal buffer (Pandian, 1970; Hernáez and Palma,
2003).
Reproductive output
The reproductive output of A. armillatus was similar
to that reported for other species of the family (Table 2).
This confirms the rule that snapping shrimps seem to
invest approximately 10% of the female weight in repro-
duction (Lardies and Wehrtmann, 1997). In decapods,
the same percentage is also found in Brachyura (Hines,
1988), although in Anomura, investment in reproduction
seems to vary widely inside of the group (Miranda et al.,
2006; Torati and Mantelatto, 2008).
However, the reproductive output in this population
is less than in other snapping shrimps living at lower
latitudes, such as A. saxidomus Holthuis, 1980 (0.44),
A. schmitti Chace, 1972 (0.30) and A. simus Guérin-
Méneville, 1857 (0.31) (Lardies and Wehrtmann, 1997).
The data are in agreement with the suggestion that the
RO of caridean shrimps shows a tendency towards
intraspecific reduction with increasing latitude (Jones
and Simons, 1983; Clarke, 1987; Lardies and Wehrt-
mann, 1997, 2001).
In this region, reproduction of A. armillatus is con-
stant throughout the year, i.e., is continuous (Mossolin
et al., 2006), which means continuous egg production.
Thereby, the success of reproduction of this species is
closely associated with the seasonal variations. The
higher number of eggs found during the rainy season
can be explained by the higher temperatures and more
available food during this period of the year. Other
alpheid shrimps, such as Alpheus dentipes (Fernández-
Muñoz and Garcia-Raso, 1987) and A. nuttingi Schmitt,
1924 (Pavanelli et al., submitted), also increase egg
output in this season.
According to Sastry (1983), the production of
gametes, and consequently the size of the egg mass, is
positively correlated with the amount of food available.
On the northern coast of São Paulo, the increase in
available food is influenced by the entrance of a
nutrient-rich oceanic current, the South Atlantic Central
Water (SACW) during the late spring and summer
(Castro-Filho et al., 1987), considered in this study as
the rainy season. Based on oceanographic data on
nutrients for primary production, we can infer that this
increase of nutrients probably resulted indirectly in a
larger amount of food not only for the studied popu-
lation, but also for all trophic levels of the area.
As far as we know, this is the first report of the
influence of season on egg production mechanisms in
snapping shrimps of the genus Alpheus. In conclusion,
we hypothesize that this population can vary its repro-
ductive effort in different seasons as a local adaptive
strategy, avoiding competition (females and larval
supplies) with another coexisting alpheid, A. nuttingi.
Additional comparative studies on reproductive aspects
for members of this subfamily need to be developed, in
order to enhance our current understanding of the
evolution of reproduction in this intriguing group of
decapods.
Acknowledgements
This report was part of the B.Sc. thesis of C.A.M.P.
and was supported by a Scientific Initiation Fellowship
from PIBIC/CNPq. E.C.M. was supported by a fellow-
ship from CAPES, Program of Qualification in Taxo-
nomy (#563934/2005-0). F.L.M. is grateful to CNPq for
research grant scholarships (PQ 301261/04-0;
301359/07-5). Special thanks are due to all members of
the Laboratory of Bioecology and Crustacean Syste-
matics of FFCLRP/USP for their help during field and
laboratory work. The support of the Postgraduate
Program in Comparative Biology of FFCLRP/USP and
the Centro de Biologia Marinha (CEBIMar/USP) during
field work is gratefully acknowledged. We thank Zilá
Luz Paulino Simões (FFCLRP) and Rogério Caetano da
Costa (UNESP) for commenting on an earlier version of
the manuscript during the thesis defense. We would also
like to thank the anonymous reviewers for their
suggestions and contributions toward the improvement
of this paper. All experiments conducted in this study
comply with current applicable state and federal laws.
Janet W. Reid (Virginia Museum of Natural History)
revised the English text.
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