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BRAZILIAN CRUSTACEAN SOCIETY
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ORIGINAL ARTICLE
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Infestation by the epibiont Octolasmis
lowei in a portunid crab assemblage from
a subtropical coast
Lylian Marcia da Silva-Inácio1, Glauco Barreto de Oliveira
Machado2, Monique D’Assunção Fortuna3, Fabio Henrique
Carretero Sanches4 and Tânia Marcia Costa1
1 Laboratório de Ecologia e Comportamento Animal, Universidade Estadual Paulista
(UNESP), Instituto de Biociências, Campus do Litoral Paulista (CLP). Praça Infante
D. Henrique, s/nº, Parque Bitaru. 11330-900 São Vicente, São Paulo, Brazil.
LMS-I E-mail: lylian_inacio@yahoo.com.br
TMC E-mail: costatm@clp.unesp.br
2 Pós-Graduação em Ecologia, Universidade Estadual de Campinas (UNICAMP).
Avenida Bertrand Russell. 13083-970 Campinas, São Paulo, Brazil.
E-mail: gbomachado@gmail.com
GBOM
3 Pós-Graduação em Biodiversidade Aquática, Universidade Estadual Paulista
(UNESP), Instituto de Biociências, Campus do Litoral Paulista (CLP). Praça Infante
D. Henrique, s/nº, Parque Bitaru. 11330-900 São Vicente, São Paulo, Brazil.
MDF E-mail: mofortuna@gmail.com
4 Pós-Graduação em Ciências Biológicas (Zoologia), Universidade Estadual Paulista
(UNESP), Instituto de Biociências, Campus de Botucatu. Rua Prof. Dr. Antonio
Celso Wagner Zanin, s/nº, Rubião Junior. 18618-689 Botucatu, São Paulo, Brazil.
FHCS E-mail: fabiohcsanches@yahoo.com.br
ZOOBANK: http://zoobank.org/urn:lsid:zoobank.org:pub:0ADF105F-A101-4305-
A0C5-0CC8489BDE2D
CORRESPONDING AUTHOR
Tânia Márcia Costa
costatm@clp.unesp.br
SUBMITTED 29 February 2016
ACCEPTED 19 July 2016
PUBLISHED 21 November 2016
Guest Editors
Maria Lúcia Negreiros-Fransozo
and Adilson Fransozo
DOI 10.1590/2358-2936e2016022
Nauplius, 24: e2016022
ABSTRACT
We investigated the infestation by Octolasmis lowei Darwin, 1851 in branchial
chambers of the portunid Achelous spinimanus (Latreille, 1819), Arenaeus
cribrarius (Lamarck, 1818), Callinectes danae Smith, 1869, and Callinectes
ornatus Ordway, 1863. We evaluated how infestation is related to host maturity,
molt stage, carapace width and sex. The infestation probability increases
with host carapace width, and infested crabs were more likely to be adults
1
Silva-Inácio et al.
Epibiosis in portunid crabs
in intermolt stage. Infestation prevalence did not differ between sexes, except for C. ornatus, in which females
had higher infestation than males. Infestation intensity was higher for males than females in A. cribrarius and
A. spinimanus, while C. ornatus showed an opposite pattern. Association of O. lowei with portunid seems to
be tightly related to the biological traits of its host. Some of these traits, such as host size, maturity and molt
stage, are likely to affect infestation in a similar way for all host species, while the effect of other traits, such as
sex identity, seems to vary among hosts. We suggest a deeper understanding of the factors driving host use by
generalist epibionts such as O. lowei depends on investigating their occurrence on a variety of potential hosts,
as well as performing manipulative studies to evaluate the factors driving host preferences by this epibiont.
KEY
WORDS
Decapods, epibiosis, infestation patterns, stalked barnacle.
INTRODUCTION
In marine habitats dominated by soft bottoms, some
benthic organisms have an important role in providing
hard substrate for the settlement and growth of
other species such as algae, barnacles and bryozoans
( Jeffries et al., 1992; Wahl and Hay, 1995; Becker
and Wahl, 1996; Key et al., 1999). In this epibionthost interaction, hosts can enhance access to food
sources and optimize epibiont dispersal (review in
Wahl, 1989). However, some hosts can be negatively
affected (e.g. increase in weight and surface friction),
which may cause reduced mobility (Dixon et al., 1981)
depending on the number and species of epibionts.
Among host organisms, marine benthic decapods
have been extensively reported in sheltering epibionts
(Abelló and Macpherson, 1992; Jeffries et al., 1992;
Becker and Wahl, 1996; Key et al., 1999; Santos and
Bueno, 2002; Cordeiro and Costa, 2010). Epibiont
infestation in decapods is often related to the biological
traits of these hosts, such as behavior, size, sex, maturity
and molt stage (Abelló and Macpherson, 1992; Jeffries
et al., 1992; Becker and Wahl, 1996; Key et al., 1999;
Cordeiro and Costa, 2010).
The infraclass Cirripedia is a typical group of
epibionts which occur in decapods (Abelló and
Macpherson, 1992; Jeffries et al., 1992; Key et al.,
1997; Costa et al., 2010). These sessile invertebrates
are found attached to the carapace (Key et al., 1997;
Costa et al., 2010) and branchial chambers of their
hosts (Abelló and Macpherson, 1992; Jeffries et al.,
1992; Santos and Bueno, 2002). Among cirripedians,
the stalked barnacle of the genus Octolasmis Gray,
1825 is an exclusive epibiont, often found adhered
to the gills of decapods such as lobsters ( Jeffries et
Nauplius, 24: e2016022
al., 1984; 1991) and crabs (Dinamani, 1964; Jeffries
et al., 1982; Voris et al., 1994; Cordeiro and Costa,
2010). Usually, the host is not negatively affected by
the epibiont, unless when there is a large number of
the latter, which may cause negative effects in host
gas exchanges (Wahl, 1989). In addition, Octolasmis
species have a planktonic larval stage, followed by
settlement and metamorphosis to adult form in the
branchial chambers of their hosts, completing its life
cycle during host intermolt stage (Walker, 1974; Gili
et al., 1993; Jeffries and Voris, 1996).
Although infestation by the genus Octolasmis in
decapods is well documented (Jeffries and Voris, 1983;
Young, 1990; Shields, 1992; Walker, 2001; Santos and
Bueno, 2002; Yan et al., 2004; Cordeiro and Costa,
2010; Costa et al., 2010; Farrapeira, 2010; Machado et
al., 2013), few studies have attempted to simultaneously
investigate the association of these epibionts in a variety
of sympatric host species (Humes, 1941; Jeffries et al.,
1982; Kumaravel et al., 2009; Machado et al., 2013).
Such approach is important for understanding host
usage range in epibionts, as well as to evaluate the
effect of biological traits (e.g. maturity, size and sex)
on infestation, which could improve our knowledge
of the factors influencing epibiont-host interaction. In
Brazil, the occurrence of Octolasmis lowei Darwin, 1851
has been reported in the branchial chambers of crabs
from the families Aethridae, Epialtidae, Leucosiidae
and Portunidae (Young, 1990; Santos and Bueno,
2002; Cordeiro and Costa, 2010; Costa et al., 2010;
Machado et al., 2013). However, these findings are
reported in different areas and for few host species
per study. Herein, we evaluated the infestation of the
stalked barnacle O. lowei in branchial chambers of
four portunid species, investigating how infestation
2
Silva-Inácio et al.
Epibiosis in portunid crabs
by this epibiont is related to host maturity, size, sex
and molt stage.
MATERIAL
AND
METHODS
Portunid crabs were collected monthly in the Ubatuba
bay, on the northern coast of the state of São Paulo,
Brazil (23º30’ to 23º23’S; 45º05’ to 44º47’W) from
November 2001 to April 2002 (except December
2001). Sampling was carried out using an otter trawl
towed by a commercial fishing boat, along transects
parallel to the coastline, covering depths from 5 to 25
m. We trawled 6 to 10 transects monthly, totalizing 43
transects. Samples were bagged and maintained frozen
until analysis. Crabs were identified in accordance
to Melo (1996). For each individual, maximum
carapace width (CW in mm) was measured, excluding
lateral spines. Crabs were sexed based on abdomen
shape (Williams, 1974) and the number of pleopods
(Melo, 1996). Molt stage (intermolt or molt activity)
was determined according to carapace consistency
(Skinner, 1985). After removing the dorsal carapace,
we inspected the branchial chambers in O. lowei using
a stereo-microscope and determined maturity stage
(adult or juvenile) based on gonad state (Costa and
Negreiros-Fransozo, 1998).
For all host species, data analyses were restricted to
adult crabs, since juveniles are unlikely to be infested
(Machado et al., 2013). Only one juvenile (a female
of Callinectes ornatus Ordway, 1863) was found to be
infested, but it was excluded from the analysis. For
each host species, we compared carapace width and
proportion of individuals in intermolt stage between
males and females applying Student’s t test (assuming
equal or unequal variances) and a Chi-squared test,
respectively. Homogeneity of variance was verified by a
Cochran test. Infestation (considering crab condition:
infested or non-infested) was analyzed using logistic
regression, with CW and sex as explanatory variables.
Also, for each host, the effect of CW on infestation
was tested in both sexes with a logistic regression
and, from the resulting models, we estimated odd
ratios of infestation (the ratio of the probability of
being infested to the probability of not being infested)
according to CW. Prevalence (%) and intensity of
infestation (number of epibionts per infested host)
were compared between males and females using a Chisquared test and a generalized linear model (GLM),
Nauplius, 24: e2016022
respectively. All GLM applied to the intensity of
infestation comparisons among sexes were tested using
Negative Binomial distribution. Statistical difference
was considered when p < 0.05.
RESULTS
A total of 1840 adult portunid crabs were sampled,
represented by the following species: Achelous spinimanus
(Latreille, 1819) (N = 246), Arenaeus cribrarius (Lamarck,
1818) (N = 112), Callinectes danae Smith, 1869 (N = 164),
and Callinectes ornatus (N = 1318). Highest infestation
prevalence by O. lowei was observed in C. danae (22.56%)
followed by A. cribrarius (13.39%), C. ornatus (10.85%)
and A. spinimanus (8.13%). Among infested host species,
A. spinimanus showed higher infestation intensity values
(11.1 ± 16.4 epibionts/ind.) than those observed in C.
ornatus (7.4 ± 8.4), C. danae (3.3 ± 3.2) and A. cribrarius
(3.1 ± 3.4). Males had larger CW than females in all host
species (A. cribrarius: t = 3.204, df = 83.41, P = 0.002; C.
danae: t = 3.745, df = 26.06, P = 0.001; C. ornatus: t =
15.523, df = 1092.8, P < 0.0001), except in A. spinimanus
(t = 1.877, df = 244, P = 0.062). Proportion of individuals
in intermolt stage did not differ between sexes, in any of
the host species (A. cribrarius: χ2 = 0.620, P = 0.431; C.
danae: χ2 = 2.601, P = 0.107; C. ornatus: χ2 = 2.019, P =
0.155 and A. spinimanus: χ2 = 3.601, P = 0.058) (Tab. 1).
In A. cribrarius, C. ornatus and A. spinimanus,
infestation (infested or non-infested) was affected
by host CW and sex (Tab. 2); in A. cribrarius and A.
spinimanus, the effect of sex was marginally significant;
in C. danae, CW affected infestation in males only (Tab.
3). In all cases in which CW affected infestation, it was
observed that infestation probability increased with size
(Fig. 1, Tab. 3). For example, for one-unit increase in
size, males of A. cribrarius were 1.265 times (26.5%)
more likely to be infested.
Infestation prevalence did not differ between males
and females in A. cribrarius (χ2 = 0.002, P = 0.968),
C. danae (χ2 = 0.329, P = 0.566) and A. spinimanus
(χ2 = 0.791, P = 0.374). In contrast, prevalence was
higher for females than males in C. ornatus (χ2 =
5.281, P = 0.022). Infestation intensity was higher in
males than females in A. cribrarius (GLM, Deviance =
6.441, d.f. = 1, Residual deviance = 12.393, P = 0.011)
and A. spinimanus (GLM, Deviance = 9.042, d.f. = 1,
Residual deviance = 20.910, P = 0.003). In C. ornatus,
the pattern was opposite (GLM, Deviance = 3.975, d.f.
= 1, Residual deviance = 149.48, P = 0.046), while in C.
3
Silva-Inácio et al.
Epibiosis in portunid crabs
Table 1. Descriptive variables of portunid crabs and Octolasmis lowei infestation by host species and sex (M = male; F = female):
Number of individuals (N), Carapace width (mean ± standard deviation in mm), Individuals in intermolt stage (%), Prevalence
of infestation (%) and Intensity of infestation (mean ± standard deviation). * Indicates a significant difference between males and
females (P < 0.05).
N
Host species
Carapace width
Intermolt (%)
Prevalence (%)
Intensity
M
F
M
F
M
F
M
F
M
F
48
64
*77.5±12.0
70.9±8.9
91.7
96.9
14.6
12.5
*4.7±4.4
1.6±1.1
C. danae
24
140
*77.5±12.4
67.7±7.6
87.5
97.1
29.2
21.4
2.9±2.9
3.4±3.3
C. ornatus
631
687
*56.6±10.0
49.4±6.2
87.2
89.8
*8.7
12.8
*5.9±7.4
8.3±8.9
A. spinimanus
71
175
59.0±14.1
63.2±16.1
77.5
88.0
11.3
6.9
*20.1±23.2
5.0±5.0
A. cribrarius
Table 2. Analysis of deviance for logistic regression fitted to condition of infestation by Octolasmis lowei in each host species. Size
and sex of crabs were used as explanatory variables.
Source of variation
Df
Deviance
Residual df
Residual deviance
P(>|χ2|)
A. cribrarius
NULL
-
-
111
88.208
-
Size
1
16.596
110
71.613
<0.001
Sex
1
3.887
109
67.725
0.049
Size X Sex
1
0.428
108
67.298
0.513
C. danae
NULL
-
-
163
175.12
-
Size
1
0.350
162
174.78
0.554
Sex
1
0.403
161
174.37
0.526
Size X Sex
1
7.349
160
167.02
0.007
C. ornatus
NULL
-
-
1317
905.10
-
Size
1
18.169
1316
886.94
<0.001
Sex
1
27.115
1315
859.82
<0.001
Size X Sex
1
0.882
1314
858.94
0.348
A. spinimanus
NULL
-
-
245
138.71
-
Size
1
24.428
244
114.28
<0.001
Sex
1
4.266
243
110.02
0.039
Size X Sex
1
2.605
242
107.41
0.107
Table 3. Analysis of deviance for logistic regression fitted to condition of infestation by Octolasmis lowei. Odds ratio (OR) and 95%
confidence interval (CI) for males and females of host species.
Species
OR
95% CI
Female
1.171
1.04 - 1.39
7.045
0.008
Male
1.265
1.09 - 1.60
13.763
<0.001
C. danae
Female
0.969
0.92 - 1.02
1.421
0.233
Male
1.142
1.02 - 1.37
6.012
0.014
C. ornatus
Female
1.069
1.03 - 1.11
11.316
<0.001
Male
1.098
1.06 - 1.14
29.094
<0.001
Female
1.089
1.03 - 1.16
10.853
0.001
Male
1.211
1.09 - 1.44
19.203
<0.001
A. cribrarius
A. spinimanus
Nauplius, 24: e2016022
Deviance
P(>|χ2|)
Sex
4
Silva-Inácio et al.
Epibiosis in portunid crabs
Figure 1. Relationship between probability of being infested by Octolasmis lowei and host size by sex. Gray solid circles = Female;
Black solid circles = Male. For each species, solid circles on the top and bottom of graph represent the size of infested and no infested
individuals, respectively. Solid and dashed lines represent the fitted model for males and females, respectively.
danae infestation intensity did not differ between sexes
(GLM, Deviance = 0.219, d.f. = 1, Residual deviance
= 34.837, P = 0.640) (Tab. 1). Overall, infested crabs
were in intermolt stage, except for two A. spinimanus
individuals that were in pre-molt stage.
DISCUSSION
Portunid crabs have an important role as hosts for O.
lowei. Infestation by O. lowei in portunid crabs was
affected by the biological traits of these hosts. We found
the probability of infestation by O. lowei increased with
host carapace width, regardless of host species, as well
as that infested crabs were more likely to be adults in
intermolt stage. Furthermore, although the prevalence
of infestation was similar between females and males
(except for C. ornatus), the intensity of infestation
was influenced by sex for most host species. Overall,
infestation by O. lowei seems to be restricted to a
fraction of the host populations (i.e. adults in intermolt
stage), which is in an agreement with other studies that
reported epibiont infestation in decapods (Santos and
Bueno, 2002; Costa et al., 2010; Machado et al., 2013).
Nauplius, 24: e2016022
Spatial availability can be a limiting factor for the
success of sessile organisms (Connell, 1972). However,
the interval during which such space is available is
also vital for epibionts on living substrates (Gili et
al., 1993). Since molting eliminates epibionts on the
carapace surface and within the branchial chambers of
crabs and other crustaceans (Walker, 1974; Jeffries and
Voris, 1996), the interval between consecutive molting
processes, or intermolt period, is often a constraint
for epibiont success (Kuris, 1978; Jeffries and Voris,
1996). We found the probability of infestation by O.
lowei in portunids crabs increases with host carapace
width. Also, almost all infested crabs were adults in
intermolt stage. These findings support the importance
of temporal substrate availability for epibionts, since
older and larger crabs molt less frequently than smaller
individuals, and are thus more likely to be infested (Li
et al., 2014). Similar results have been reported for
other decapods infested by Octolasmis spp. ( Jeffries et
al., 1992; Shields, 1992; Machado et al., 2013).
Molt frequency and spatial distribution have
been suggested as to promote differences in epibiont
5
Silva-Inácio et al.
infestation between sexes of decapods (Abelló and
Macpherson, 1992; Key et al., 1997). For all host
species, the proportion of individuals in intermolt stage
did not differ between males and females. Since molt
activity is related to infestation, such results support
the lack of difference in infestation prevalence between
sexes for all portunid crabs in the present study, except
for C. ornatus, in which females had higher infestation
prevalence than males. Also, for all host species, males
had a larger carapace width than females. However,
although a positive relationship was found between
host size and probability of infestation for males and
females of most host species, the differences in size
between sexes alone are unlikely to explain the patterns
of infestation prevalence observed for these species.
The differences in infestation prevalence between
males and females of C. ornatus contrast with previous
studies that reported higher infestation prevalence by
O. lowei in males (Santos and Bueno, 2002; Machado
et al., 2013). This may be explained by the differential
spatial distribution between sexes of this portunid
in the Ubatuba bay. Andrade et al. (2013) observed
that males inhabit shallower waters, while females
are more often found in depths between 15 and 20
m. Our sampling was carried out in a wide range that
included both male and female habitats (from 5 to 25
m). It may be that the vulnerability of C. ornatus to the
infestation by O. lowei is higher in deeper waters, where
females occur more often. However, our sampling was
not properly designed to address robust comparisons
among depths and, thus, further studies are required
to test if the infestation by O. lowei varies throughout
a range of depths. In addition, Machado et al. (2013)
observed higher infestation prevalence by O. lowei in
females of C. danae than males, contrary to our results.
A shorter sampling period (5 months) in comparison
with other studies may be responsible for such singular
results, since infestation can vary temporally. Costa et
al. (2010) found that A. cribrarius presented a lower
prevalence of infestation by O. lowei and other epibionts
during winter. Since the relative contribution of each
demographic category (males, non-ovigerous females,
ovigerous females and juveniles) to the population of a
crab species often varies temporally (Santos et al., 1995;
Johnson and Perry, 1999; Carvalho and Couto, 2011;
Andrade et al., 2013), these categories might have been
represented differently in our sample when compared
to those of previous studies, which may explain some
Nauplius, 24: e2016022
Epibiosis in portunid crabs
divergences in results (e.g. infestation on ovigerous
females tend to be higher than non-ovigerous females
and males, probably because these females has longer
intermolt periods; Costa et al., 2010).
The infestation intensity by O. lowei in our study
differed between sexes for most host species, but
in distinct ways. Males of Achelous spinimanus and
Arenaeus cribrarius presented higher infestation
intensity than females. In contrast, females of C.
ornatus presented higher infestation intensity than
males, while no difference was observed between
sexes in C. danae. Such results suggest the mechanisms
involved in avoiding and/or reducing infestation may
vary between host sexes and species. For example,
Cordeiro and Costa (2010) suggest that an efficient
branchial cleaning by females of Libinia spinosa H.
Milne Edwards, 1834 may result in a lower intensity
of infestation than that observed for males. However,
this question remains unclear and, thus, further studies
are required to explore the causes of inter-specific and
sex differences in epibiont infestation. Furthermore,
except for C. danae, the obtained results contrast with
studies that reported a lack of difference in infestation
intensity between sexes in portunid crabs (Santos and
Bueno, 2002; Costa et al., 2010; Machado et al., 2013).
Some divergences in results may be explained by many
factors, such as: differences in sampling sites, depth and
length among studies. Further studies considering a
variety of spatial and temporal scales could contribute
to elucidate such divergences.
Octolasmis species have been reported to have low
specificity regarding the host use, occurring in a variety
of host species ( Jeffries et al., 1982; Jeffries and Voris,
1983; Shields, 1992; Walker, 2001; Yan et al., 2004;
Kumaravel et al., 2009; Machado et al., 2013), which
should be advantageous, since the availability of hard
substrate is often a constraint for sessile organisms.
In the present study, although O. lowei occurred
in all portunid species sampled, the infestation by
this epibiont seems to vary among their hosts. Both
males and females of A. spinimanus had much higher
intensity of infestation than any other host species,
but an infestation prevalence that was comparable to
those of other hosts (except C. danae). In this case,
the abundance of A. spinimanus is unlikely to explain
the higher infestation intensity, since this portunid
species occurred in lower abundance than C. ornatus,
6
Silva-Inácio et al.
which had lower infestation intensity. Such result may
suggest certain degree of host preference by O. lowei
towards A. spinimanus. In contrast, C. danae had the
highest infestation prevalence, but lower infestation
intensity, which indicates that although a higher
proportion of individuals was infested, the average
number of O. lowei per individual was low. The extent
to which the occurrence of O. lowei in a variety of host
species is related to the preference of this epibiont
and/or is a constraint to other factors (e.g. availability
of host) requires further investigation. Manipulative
experiments with robust designs could improve our
understanding about the factors driving the host
species and sex preferences by O. lowei.
We found that biological traits of portunid crabs,
such as carapace width and sex, influence infestation
by O. lowei, which is in agreement with previous studies
(Abelló and Macpherson, 1992; Jeffries et al., 1992;
Shields, 1992; Key et al., 1997; Santos and Bueno, 2002;
Machado et al., 2013). Some of these traits, such as
carapace width, maturity and molt stage, seem to affect
O. lowei infestation in a similar way for all host species.
On the other hand, the effect of sex on infestation
varied among host species. In this sense, we suggest a
deeper understanding of the factors driving host use
by generalist epibionts such as O. lowei depends on
investigating their occurrence on a variety of potential
hosts.
ACKNOWLEDGEMENTS
We would like to thank the personnel from Núcleo
de Estudos em Biologia, Ecologia e Cultivo de
Crustáceos(NEBECC - Unesp Botucatu) and Grupo
de Pesquisa em Biologia de Crustáceos (CRUSTA
- Unesp São Vicente) for helping with field and
laboratory analyses. Also, we appreciate the valuable
comments of two anonymous reviewers. This work
was financially supported by São Paulo Research
Foundation (FAPESP) (# 98/07090-3 BIOTA Project,
# 02/09217-8 fellowship undergraduate Silva-Inácio
ML and # 01/00886-1 post-doctorate grant Costa
TM).
Epibiosis in portunid crabs
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