Invertebrate Reproduction and Development, 50:2 (2007) 67–74 67

Balaban, Philadelphia/Rehovot
0168-8170/07/$05.00 © 2007 Balaban

Morphology and chronology of embryonic development in

Macrobrachium acanthurus (Crustacea, Decapoda)

YARA MARIA RAUH MÜLLER*, CRISTIANE PACHECO, MARCOS SAWADA SIMÕES-COSTA, DIB AMMAR,
and EVELISE MARIA NAZARI
Downloaded by [Nova Southeastern University] at 10:10 27 December 2014

Departamento de Biologia Celular, Embriologia e Genética, Universidade Federal de Santa Catarina,

Campus Universitário–Trindade, Florianópolis, Brazil
Tel. +55 (48) 3331-9799; Fax: +55 (48) 3331-5148; email: yararm@ccb.ufsc.br

Received 30 August 2006; Accepted 3 April 2007

Summary
In palaemonids, the nauplius corresponds to the egg-nauplius stage, which is a crustacean
developmental marker of meroblastic development. The aim of this study is to establish the
embryonic staging based on the morphological and morphometrical features in living and fixed
embryos at intervals of 24 hours, defined as embryonic days (E) associated by percent staging.
Eggs were analyzed with a stereomicroscope to obtain stage descriptions and to determine egg
volume and embryonic structures measurements. Macrobrachium acanthurus presented an
incubation period of 16 days from spawning to hatching. From E1 to E8 (6 to 50% of development)
the intralecithal cell divisions and the establishment of the initial embryo shape were observed. The
period of embryonic processes that occurs from E8 until hatching is characterized by the
appearance and differentiation of structures that will form the tissues and the organ systems of post-
nauplius and zoea. During incubation, the mean egg volume was 0.075 mm3 (±0.014) and the mean
measurements of the optic lobe area and eye index were 0.462 mm2 (±0.168) and 90.929 (±34.467),
respectively. The association of morphological and morphometrical features during embryonic
development can be a accurate tools to study the chronology and the staging of M. acanthurus
embryogenesis.

Key words: Decapoda, yolky eggs, developmental landmarks, morphology, morphometry

Introduction
In palaemonids, the females incubate yolky eggs in
a brood pouch until hatching and the nauplius corre-
sponds to the egg-nauplius stage, which is a crustacean
developmental marker of meroblastic development
(Müller et al. 2004). Other relevant characteristics of
this embryonic pattern are the intralecithal cell division,
the formation of the syncytial blastoderm and the
blastoporal area, the presence of the superficial germinal
disc, the caudal papilla, the embryonic post-nauplius
and the incorporation of the yolk mass by the midgut
(Anderson, 1982; Scholtz and Kawai, 2002).
Several staging methods have been employed to
characterize the meroblastic developmental pattern and
to categorize progressive morphological change during
embryonic development (Perkins, 1972; Helluy and
Beltz, 1991; Sandeman and Sandeman, 1991; Nazari et
al., 2000; Müller et al., 2003). The embryogenesis of

*
Corresponding author.
 68 Y.M.R. Müller et al. / IRD 50 (2007) 67–74
yolky eggs enables all morphological changes to be
followed daily by the examination of gross morphology
and histological sections. However, some methodolo-
gies also permit the evaluation of development by
measurements of externally observed embryonic
structures such as eyes (Beltz et al., 1992), relating the
quantitative variables to the morphological descriptions.
Yolky eggs of palaemonid prawns exhibit diverse
incubation periods, as described for Palaemonetes
argentinus, 10 days (Nazari et al., 2000); Palaemon
pandaliformis, 13 days (Müller et al., 1999); Macro-
brachium olfersi, 14 days (Müller et al., 2003); M.
rosenbergii, 16 days (Clarke et al. 1990); and M.
potiuna, 21 days (Müller et al., 2004). If compared with
Downloaded by [Nova Southeastern University] at 10:10 27 December 2014
other decapods, the incubation period of palaemonids
can be considered short, since in the lobster, Homarus
americanus, it is 180 days (Helluy and Beltz, 1991), in
the crab, Erimacrus isenbeckii, 360 days (Nagao et al.,
1999) and in the crayfish, Virilastacus araucanius, 120
days (Rudolph and Rojas, 2003). Numerous studies
have described the main features of embryonic
development of species, but they have not reported the
developmental time of each embryonic stage.
Macrobrachium acanthurus is a palaemonid with a
broad geographical distribution, ranging from the east
coast of the United States to southern Brazil (Holthuis,
1980). This prawn inhabits the marginal vegetation of
shallow streams, and can be found in fresh or brackish
water (McNamara et al., 1985). The mean fecundity of
M. acanthurus has been reported to be 1932 eggs
(Müller et al., 1992) and it shows a considerable poten-
tial for aquaculture, having been exploited by popu-
lations living near streams (Valenti, 1985). Only a few
studies describe the reproductive biology and physio-
logy of adults and larvae of this species (Valenti et al.,
1986; Ismael and Moreira, 1997; Díaz et al., 2002),
although its embryonic development has been studied
by Bressan and Müller (1997, 1999). However, these
last two studies focused only on the specific morpho-
logical features of the naupliar and post-naupliar stages.
The objective of the present study is to establish the
embryonic staging based on the morphological and
morphometrical features of meroblastic development in
living and fixed embryos over the whole incubation
time. This work is of significance for decapod embry-
onic development studies, and also as a reference to
understand the chronology of the developmental
landmarks of species that carry yolky eggs.
Materials and Methods
Animal samples
Male and female adults of the prawn, M. acanthurus,
were obtained from freshwater streams on Santa
Catarina Island (southern Brazil) (48°36N–48°22N/
27°22N–27°50N) and placed in 60 L water tanks, under
constant aeration, with a temperature of 25EC (±1) and
a 14h:10h light:dark cycle.
Ovigerous females were monitored from spawning
until hatching of the larvae. All procedures used during
this study were performed after approval by the National
Environmental Committee (IBAMA 010/2004 Certi-
ficate), and every effort was made to minimize animal
suffering.
Embryonic staging
To establish the stages of embryonic development,
samples of 20 eggs were removed from the periphery of
the egg mass at 24-h intervals, which correspond to the
embryonic days (E). Living embryos were observed
with a stereomicroscope (48×) and recorded with a
video monitoring system, to describe the mobility and
morphological features presented by the majority of the
eggs on each embryonic day (Nagao et al., 1999; Müller
et al., 2003). The percent scale of the total develop-
mental time was also used, 0% being when eggs were
laid, and 100% at hatching (Sandeman and Sandeman,
1991).
Egg and embryo measurements
Eggs were fixed in 4% formol solution for 20 h prior
to measurement. Width (h) and length (l) of eggs, optic
lobes and lateral eyes were obtained with an ocular
micrometer in a light microscope at magnifications of
40× and 400×. Ten intact eggs of each stage were
randomly selected and measured. Egg volume was
obtained from the formula v = (πlh2/6) (Odinetz-Colart
and Rabelo, 1996). The area of the visible surface of the
optic lobes was calculated from the formula for an
ellipsoid [(l+h/2)π] where l and h correspond to long
and short eye axis, respectively. The eye index was
obtained from the formula ei= (l+h)/2, described by
Perkins (1972).
After measurements were completed, the eggs were
again analyzed in a stereomicroscope (48×) to obtain
complementary descriptions of morphological features
in fixed embryos at each embryonic day.
Differences in egg volume, eye index and the optic
lobe area were analyzed by one-way ANOVA, followed
by the Tukey test. The values of p, 0.01and 0.05, were
chosen as the levels of significance.
Results
In this investigation, 1600 eggs were analyzed,
having been obtained from five ovigerous females (n =
 Y.M.R. Müller et al. / IRD 50 (2007) 67–74 69

Table 1. Morphological features observed during the embryonic development time of M. acanthurus

Time Morphological descriptions

E1 Spawning egg was oval and closely surrounded by the transparent chorion. There was no evidence of embryonic
structure on the surface of the egg and at the end of the day the first two nuclear cleavages were observed due to
transparency in the deeper granular yolk mass (Fig. 1A).
E2 Intralecithal cleavage is observed and cleavage furrows can be seen at the surface of the eggs. The number of
blastomeres varies from 4 to 32 cells. Superficial blastoderm surrounds the yolk mass (Fig. 1B, Fig. 2A).
E3 Numerous and small blastomeres are observed on the egg surface. The blastoporal area is formed by a ring of
cells around a shallow depression (Fig. 1C). Some of these cells migrate to the inner part of the egg and organize
cell layers, forming the germinal disc, which takes on a V-shape (Fig. 1D). The superior and inferior extremities
of the germinal disc are formed by high cell concentration when compared to the intermediate region.
E4 Between the superior and inferior extremities of the germinal disc, buds of the three pairs of naupliar appendages
(antennulae, antennae and mandibles) are formed and the stomodeum is visualized in the central embryo region.
At the end of the day, a typical egg-nauplius can be superficially visualized (Fig. 1E).
Downloaded by [Nova Southeastern University] at 10:10 27 December 2014

E5 The optic lobe is organized in the areas of high cell concentration at the upper extremity of the egg-nauplius (Fig.
1F). This region corresponds to the anterior region of the embryo body that indicates the early nervous system
development is occurs internally. The caudal papilla begins your growth and bent (Fig. 2B).
E6 The caudal papilla is organized in the area of high cell concentration at the lower extremity of the egg-nauplius
and indicates the posterior region of the embryo. By the end of the day, the embryo acquires the main features of
the embryonized post-nauplius, where the naupliar appendages are bifurcated, the buds of post naupliar
appendages can be seen, the optic lobes and caudal papilla correspond to the anterior and posterior region of the
embryo, respectively (Fig. 1G).
E7 There is a large increase in the embryo's size, mainly on the antero-posterior axis and the embryo acquires the
characteristic “C” shape. The optic lobes bend antero-laterally towards the yolk. The caudal papilla grows and
reaches the base of the optic lobes. Five buds of post-naupliar appendages are arranged laterally along the caudal
papilla. Some chromatophores are visible in the distal portion of the optic lobes (Fig. 1H).
E8 The lateral eye is formed and it consists of a thin-pigmented area located in the distal region of the optic lobe
adjacent to the chromatophores (Fig. 1I, Fig. 2C).
E9 Few embryonic morphological changes are observed in the last 24 hours. The heart is visible in the dorsal region
and an irregular heartbeat can be seen. The eyes present an oval shape and ommatidia sketch (Fig. 1J).
E10– Telson originates from the caudal papilla and covers as far as the optic lobes. The abdominal segments become
E12 visible, and the abdomen is individualized from the rest of the body. Naupliar and post-naupliar appendages are
segmented and better defined. A regular heartbeat with pauses is observed. Some chromatophores are observed in
different regions of the embryo, mainly near to the optic lobes. Muscular contractions are observed throughout the
embryo (Fig. 1K, Fig. 2D).
E13– Ommatidia are clearly visible. The carapace covering the dorsal part of the embryo can be seen. The
E14 cephalothorax and the abdomen are easily recognized. The appendages are more differentiated and folded towards
the abdomen. A regular and vigorous heartbeat with pauses is noted. The midgut is visible by transparency of the
dorsal carapace. Yolk granules, which present variable size, are observed inside and outside the midgut (Fig. 1L).
E15– The embryo occupies all the space of the egg and all the yolk granules are inside the midgut. The eyes are round
E16 and very pronounced. At the extremities of the appendages and telson, a large quantity of setae can be observed.
The cephalothorax and abdomen have increased in size. The embryo acquires a rhythmic heartbeat and regular
muscular contractions (Fig. 1M).

320 eggs/female) that underwent courtship, fertilization
and embryonic development in the aquaria. Under the
chosen laboratory conditions, M. acanthurus show an
incubation period of 16 days from spawning to hatching.
The main morphological features of living and fixed
embryos, which were observed by external view, are
presented in Table 1 and Figs. 1 and 2.
On the earliest embryonic days the most important
observations were cell division at E1 to E3, the latter
corresponding to 18% of development, and the estab-
lishment of the initial embryo shape, which was evident
by E7 and E8, corresponding to 43 and 50% of develop-
ment, respectively, and the appearance of the thin-
pigmented lateral eye. The morphological features
involved in these events were easily recognizable due to
the sparse cell layers, the low degree of complexity of
the structures, and also by the superficial position of the
embryo in the egg. In the period between E8 and E16,
very significant embryonic events were observed which
contribute to organization of the zoeal body structures
that permit larvae eclosion and survival. Visualization of
the final events became more difficult since, at this
stage, the embryos are more opaque due to the greater
number of cells, more complex organization of
structures, and the greater degree of internal localization
of these structures. The chronology of the most relevant
embryonic events of M. acanthurus, from spawning to
hatching, is given in Fig 3.
 70 Y.M.R. Müller et al. / IRD 50 (2007) 67–74
Downloaded by [Nova Southeastern University] at 10:10 27 December 2014

Fig. 1. Schematic sketches of embryonic development of M. acanthurus. A–C. External morphology of cleavage stages.
D–G. Dorsal view of naupliar embryonic organization. H–M. Lateral view of post-naupliar embryonic organization.
a, antennulae; an, antennae; as, abdominal segment; b, blastomeres; ba, blastoporal area; c, chorion; ca, carapace; ch,
chromatophore; cp, caudal papilla; e, eye; gd, germinal disc; h, heart; m, mandible; mg, midgut; na, naupliar appendages;
o, ommatidia; ol, optic lobes; pa, post-naupliar appendages; pe, pigmented eye area; s, stomodeum; se, setae; t, telson; ym,
yolk mass. Scale bars = 0.13 mm.
 Y.M.R. Müller et al. / IRD 50 (2007) 67–74 71

Fig. 2. External view of living embryos of the M. acanthurus. A. Cleavage stage observed in E2. B. Typical egg nauplius in
E5, showing the optic lobes, caudal papilla and naupliar appendages. C. Embryonized post-nauplius in E8 presents the
pigmented eye. D. Embryo between E10–E12 with segmented naupliar and post-naupliar appendages. b, blastomeres;
c, chorion; ch, chromatophore; cp, caudal papilla; e, eye; h, heart; na, naupliar appendages; ol, optic lobes; pa, post-naupliar
appendages; pe, pigmented eye area; ym, yolk mass. Scale bars = 0.15 mm.
Downloaded by [Nova Southeastern University] at 10:10 27 December 2014

Fig. 3. Timing of appearance of embryonic structures and embryo mobility visualized on development of M. acanthurus.

Embryonic movements, such as heartbeat and
muscular contractions, were observed from E9 and E10
(c. 56–62%), respectively, and are fully established at
E15–E16 (c. 93–100%).
In this work, three morphometric variables were
selected to accompany the dynamics of embryonic
development of M. acanthurus: the egg volume, the eye
index and the optic lobe area. The egg volume varied
over the incubation period, during which the mean egg
volume was 0.075 mm3 (±0.014). The lowest value
observed, 0.052 mm3 at E1 (c. 6%), does not show a
significant difference from those at E2, E4, E8 and E9
(ANOVA, p >0.05). The highest value was 0.109 mm3
at E16 (c. 100%), which differs significantly (ANOVA,
p <0.0001) from all other days, except E15. However, a
slight decrease in the egg volume at E8 and again at
E12–E13 was observed (c. 75–81%).
The optic lobe area can only be measured from E6
(c. 37%), when the lobes are fully formed (Fig. 4).
During development the mean size of this structure was
0.462 mm2 (± 0.168). At E6 the area of the optic lobe
was 0.108 mm2, which differs significantly from all
other embryonic days (ANOVA, p <0.0001). From this
point (E6) a marked increase of the optic lobe was
 72 Y.M.R. Müller et al. / IRD 50 (2007) 67–74
Downloaded by [Nova Southeastern University] at 10:10 27 December 2014
Fig. 4. Optic lobe area measurements and eye index from E6 to E16 developmental time of M. acanthurus.
recognizable, reaching its maximum value of 0.624 mm2
at E11 (c. 68%) after which it slowly decreased.
Significant differences (ANOVA, p < 0.0001) in optic
lobe area were observed between E11 and E12 to E16.
In contrast, the eye index (Fig. 4) does not decrease
over the incubation period. It increased rapidly from
E10 (52.2), when the eyes establish their long and short
axis. At E13 a rapid increase in the eye index is
observed, reaching its maximum value of 150.3 in pre-
hatching embryos (E16), which do not only differ from
E15 (ANOVA, p >0.05). The mean value of the eye
index over the course of embryogenesis was 90.929
(±34.467).
Discussion
Embryonic morphological characteristics of M.
acanthurus observed in the present study were similar to
those described for other yolky decapod species such as
Cherax destructor (Sandeman and Sandeman, 1991),
Homarus americanus (Helluy and Beltz, 1990, 1991),
M. carcinus (Müller, 1984) and M. olfersi (Müller et al.,
2003; Simões-Costa et al., 2005). These species present
common developmental features related to their intra-
lecithal cell division, that allow the migration and
aggregation of blastoderm cells, gastrulation and
germinal disc formation, as well as the egg-nauplius and
post-nauplius organization.
A typical landmark of all crustacean development is
the nauplius larvae for holoblastic cleavage and egg-
nauplius stage for meroblastic cleavage (Dahms, 2000;
Scholtz, 2000). In this work, we also propose to better
characterize the embryonic development of meroblastic
cleavage as M. acanthurus, two additional morpho-
logical markers, the germinal disc and early post-
nauplius stages. As complementary developmental
markers, we employed the morphometric analysis of
some embryonic structures, such as the optic lobe area
and eye index. Optic lobes and lateral eyes were chosen
since both structures are externally visible and their
development can be followed chronologically. The
germinal disc and early post-nauplius stages, as well as
the optic lobes and lateral eyes, are also present in other
decapods with meroblastic cleavage (Müller, 1984;
Talbot and Helluy, 1995; Nagao et al., 1999), enabling
these features to be recognized as developmental
landmarks in yolky egg crustaceans.
A comparison of our results with decapods with
analogous development times reveals that M. olfersi
(Müller et al., 2004; Simões-Costa et al., 2005) and Uca
lactea (Yamaguchi, 2001) present similar timing of the
appearance of the germinal disc, embryonized nauplius
and lateral eyes, while P. argentinus (Nazari et al.,
2000) only showed related timing of the appearance of
the germinal disc. When compared with other decapods,
such as Cherax destructor (Sandeman and Sandeman,
1991) and H. americanus (Helluy and Beltz, 1991),
which present a more prolonged development time, it is
clear that these landmarks appear later than in M.
acanthurus.
During the development of M. acanthurus, tempo-
rary embryonic structures such as the blastoporal area,
the germinal disc and the stomodeum are mainly
observed until E6, being products of the initial morpho-
genesis and organogenesis process. These processes
underlie the appearance of definitive structures that will
form the tissues and organ systems of the post-nauplius
and the zoea. The definitive embryonic structures can be
observed from E8 and they maintain their organization
until hatching (E16).
Heartbeat and muscular contractions, as reported in
other studies (Valdes et al., 1991; Yamaguchi, 2001;
 Y.M.R. Müller et al. / IRD 50 (2007) 67–74
Pinheiro and Hattori, 2002), are also relevant embryonic
characteristics for the comparative analysis of living
embryos.
In the studied species, the intervals between E8–E9,
E10–E11 and E12–E13 presented few visible morpho-
logical changes, suggesting an apparent external
developmental plateau. However, before E8 and after
E13 the morphological and morphometrical changes are
more readily recognizable in external view. Periods of
high and low intensity of growth and differentiation
throughout embryonic development are predictable in
view of the fact that these processes are concomitant,
but take place at different intensities.
Eye index (Perkins, 1972) provides an accurate
Downloaded by [Nova Southeastern University] at 10:10 27 December 2014
method of assessing embryonic growth and has been
used in investigations of crustacean development
(Sasaki et al., 1986; Helluy and Beltz, 1991), although it
can only be applied after the appearance of eye pigmen-
tation. In this study we attempted to use earlier stages,
measuring the optic lobe area as an additional morpho-
metric criterion that would contribute to the assessment
of the rhythm of development, associating external
changes with those occurring internally.
Analysis of morphological and morphometric
changes of specific embryonic structures can be
employed as individual or joint parameters for the iden-
tification of developmental dynamics. In this work, the
association between morphological and morphometrical
criteria proved to be an interesting method for quali-
tative and quantitative analysis of embryogenesis.
Our study on M. acanthurus embryology brings
together knowledge obtained on embryonic develop-
ment in other palaemonid species and provides a
significant contribution to our understanding of crusta-
ceans with yolky eggs. The definition of stages is
essential to better understand the complete embryo-
genesis and to carry out comparative studies of decapod
groups, and is strongly dependent on the methods and
analysis employed.
Finally, we emphasize that the morphological
approach presented in this work is fundamental to
further studies, such as the characterization of the
cellular mechanisms and processes characterization of
embryonic development in this important palaemonid.
Conclusion
Our investigation demonstrates the dynamic of
intralecithal embryonic development of M. acanthurus
through the association of morphological and morpho-
metric analyses of crustacean landmarks. Early events
are easy recognizable due the superficial position of the
structures in the egg, that permit a direct observation of
73
the germinal disc and egg nauplius, as well as their
structures, as caudal papilla and optic lobes. In this
study we considered it appropriate to name these
structures as “crustacean landmarks”, since that they are
visualized in other crustacean species with intralecithal
cleavage and form a basis for comparative studies. Later
events are more internal and are hard to see in a
stereoscopic view. These events are associated to the
development of organ systems and facilitate their
functionality and larval survival after hatching. For a
more precise estimative of embryonic rhythms in final
development we correlated the eye index with an
analysis of the movements of living embryos.
In summary, this approach reveals the develop-
mental rhythms of this species and can provide useful
tools to analyse the chronology and staging details of
M. acanthurus embryogenesis. These findings contri-
bute to a better knowledge of this species, an important
American palaemonid, which participates in the food
chains of the many fishes and aquatic birds and has
potential for use in environmental recovery programs of
over-exploited areas.
References
Anderson, D.T., Embryology. In: Embryology, Morphology
and Genetics, L.G. Abele (ed.), Academic Press, New
York, 1982, pp. 1–44.
Beltz, B.S., Helluy, S.M., Ruchhoeft, M.L. and Gammill,
L.S., Aspects of the embryology and neural development
of the American lobster. J. Exp. Zool., 261 (1992)
288–297.
Bressan, C.M. and Müller, Y.M.R., Characterization of
embryonized nauplius development of Macrobrachium
acanthurus (Crustacea, Decapoda). Braz. J. Morphol.
Sci., 14 (1997) 243–246.
Bressan, C.M. and Müller, Y.M.R., Postnaupliar embryonic
development of Macrobrachium acanthurus (Crustacea,
Decapoda). Braz. J. Morphol. Sci., 16 (1999) 155–160.
Clarke, A., Brown, J.H. and Holmes, L.J., The biochemical
composition of eggs from Macrobrachium rosenbergii in
relation to embryonic development. Comp. Biochem.
Physiol., B 96 (1990) 505–511.
Dahms, H.U., Phylogenetic implications of the Crustacean
nauplius. Hydrobiologia, 417 (2000) 91–99.
Díaz, F., Sierra, E., Re, A.D. and Rodríguez, L., Behavioural
thermoregulation and critical thermal limits of Macro-
brachium acanthurus (Wiegman). J. Thermal Biol., 27
(2002) 423–428.
Helluy, S. and Beltz, B.S., Stages in the embryonic develop-
ment of the American lobster Homarus americanus with
special emphasis on its nervous system. In: Frontiers in
Crustacean Neurobiology, K. Wiese, W.D. Krenz, J.
Tautz, H. Reichert and B. Mulloney (eds.), Birkhäuser,
Basel, 1990, pp. 530–536.
Helluy, S.M. and Beltz, B.S., Embryonic development of the
American lobster (Homarus americanus): quantitative
 74 Y.M.R. Müller et al. / IRD 50 (2007) 67–74
staging and characterization of an embryonic molt cycle.
Biol. Bull., 180 (1991) 355–371.
Holthuis, L.B., FAO Species Catalogue. Shrimps and Prawns
of the World, Vol. 1, FAO Fisheries Synopsis, Rome,
125 (1980) 1–126.
Ismael, D. and Moreira, G.S., Effect of temperature and
salinity on respiratory rate and development of early
larval stages of Macrobrachium acanthurus (Wiegmann,
1836) (Decapoda, Palaemonidae). Comp. Biochem.
Physiol., A 118 (1997) 871–876.
McNamara, J.C., Moreira, G.S. and Moreira, P.S., Thermal
effects on metabolism in selected ontogenetic stages of
the freshwater shrimps Macrobrachium olfersii and
Macrobrachium heterochirus (Decapoda, Palaemonidae).
Comp. Biochem. Physiol., A 80 (1985) 187–190.
Downloaded by [Nova Southeastern University] at 10:10 27 December 2014
Müller, Y.M.R., Die Embryonalentwicklung von Macro-
brachium carcinus (L.) (Malacostraca, Decapoda,
Natantia). Zool. Jahr. Anat., 112 (1984) 51–78.
Müller, Y.M.R., Bressan, C.M. and Nazari, E.M., Dados de
Fecundidade de Macrobrachium acanthurus (Decapoda,
Palaemonidae) do Rio Capivari, Praia dos Ingleses,
Florianópolis, SC. Biotemas, 5 (1992) 123–132.
Müller, Y.M.R., Nazari, E.M. and Ammar, D., The charac-
terization of embryonic phases of prawn Palaemon
pandaliformis (Stimpson, 1871) (Crustacea, Decapoda).
Braz. J. Morphol. Sci., 16 (1999) 161–166.
Müller, Y.M.R., Nazari, E.M. and Simões-Costa, M.S.,
Embryonic stages of the freshwater prawn Macro-
brachium olfersi (Decapoda, Palaemonidae). J. Crust.
Biol., 23 (2003) 869–875.
Müller, Y.M.R., Ammar, D. and Nazari, E.M., Embryonic
development of four species of Palaemonid prawns
(Crustacea, Decapoda): pre-naupliar, naupliar and post-
naupliar periods. Revta. Bras. Zool., 21 (2004) 27–32.
Nagao, J., Munehara, H. and Shimazaki, K., Embryonic
development of the hair crab Erimacrus isenbeckii. J.
Crust. Biol., 19 (1999) 77–83.
Nazari, E.M., Müller, Y.M.R. and Ammar, D., Embryonic
development of Palaemonetes argentinus Nobili, 1901
(Decapoda, Palaemonidae), reared in the laboratory.
Crustaceana, 73 (2000) 143–152.
Odinetz-Collart, O. and Rabelo, H., Variation in egg size of
the freshwater prawn Macrobrachium amazonicum
(Decapoda, Palaemonidae). J. Crust. Biol., 16 (1996)
684–688.
Perkins, H.C., Developmental rates at various temperatures
of embryos of the northern lobster (Homarus americanus
Milne–Edwards). Fish. Bull., 70 (1972) 95–99.
Pinheiro, M.A.A. and Hattori, G.Y., Embriologia do siri
Arenaeus cribrarius (Lamarck) (Crustacea, Brachyura,
Portunidae). Revta. Bras. Zool., 19 (2002) 571–583.
Rudolph, E.H. and Rojas, C.S., Embryonic and early
postembryonic development of the burrowing crayfish,
Virilastacus araucanius (Faxon, 1914) (Decapoda,
Parastacidae) under laboratory conditions. Crustaceana,
76 (2003) 835–850.
Sandeman, R. and Sandeman, D., Stages in the development
of the embryo of the fresh-water crayfish Cherax
destructor. Roux’s Arch. Develop. Biol., 200 (1991)
27–37.
Sasaki, G.C., Capuzzo, J.M. and Biesiot, P., Nutritional and
bioenergetic considerations in the development of the
American lobster Homarus americanus. Can. J. Fish.
Aquat. Sci., 43 (1986) 2311–2319.
Scholtz, G., Evolution of the nauplius stage in malacostracan
crustaceans. J. Zool. Syst. Evol. Res., 38 (2000) 175–
187.
Scholtz, G. and Kawai, T., Aspects of embryonic and
postembryonic development of the Japanese freshwater
crayfish Cambaroides japonicus (Crustacea, Decapoda)
including a hypothesis on the evolution of maternal care
in the Astacida. Acta Zool., 83 (2002) 203–212.
Simões-Costa, M.S., Pacheco, C., Nazari, E.M., Müller,
Y.M.R. and Ammar, D., Estagiamento de embriões de
Macrobrachium olfersi (Wiegman) (Crustacea, Palae-
monidae) através de critérios morfológicos nos dias
embrionários. Revta. Bras. Zool., 22 (2005) 501–508.
Talbot, P. and Helluy, S., Reproductive and embryonic
development. In: Biology of the lobster Homarus
americanus, J.R. Factor (ed.), Academic Press, New
York, 1995, pp. 177–216.
Valdes, L., Alvarez-Ossorio, M.T. and González-Gurriarán,
E., Incubation of eggs of Necora puber (L., 1767)
(Decapoda, Brachyura, Portunidae). Volume and biomass
change in embryonic development. Crustaceana, 60
(1991) 163–177.
Valenti, W.C., Cultivo de camarões de água doce, Nobel,
São Paulo, 1985, pp. 1–82.
Valenti, W.C., Cardoso De Mello, J.T. and Lobão, V.L.,
Dinâmica da reprodução de Macrobrachium acanthurus
(Wiegmann, 1836) e Macrobrachium carcinus (Lin-
naeus, 1758) do Rio Ribeira de Iguape (Crustacea, Deca-
poda, Palaemonidae). Cienc. Cult., 7 (1986) 1255–1262.
Yamaguchi, T., Incubation of eggs and embryonic develop-
ment of the fiddler crab Uca lactea (Decapoda,
Brachyura, Ocypodidae). Crustaceana, 74 (2001) 449–
458.