Download Factors affecting food preference in a widespread intertidal isopod

EISEVIER
Journal of Experimental Marine Biology and Ecology
182 (1994) 111-121
JOURNAL OF
EXPERIMENTAL
MARINE BIOLOQY
AND ECOLOGY
Factors affecting food preference in a widespread intertidal
isopod
Jo& A.G.
Morti,
Julio Arrontes*
Lab. de Ecologia, Dept. de Biologia de Organismosy Sistemas, Universidadde Oviedo. 33005Oviedo, Spain
Received 6 January 1994; accepted 3 June 1994
Abstract
Preference for two macroalgae and feeding rate were influenced by previous experience in the
intertidal isopod Dynamene bidentutu (Adams). In preference experiments, animals reared in the
laboratory with either Fucus vesiculosus L. or Cystoseiru baccatu (Gmelin) Silva as sole resources
did not exhibit preference for either of the two algae. Preference for Fucus was exhibited by the
same animals in a subsequent experiment. Specimens reared on Cystoseiru exhibited a greater
feeding rate than those reared on Fucus. Animals collected in the field on Fucus and Cystoseiru
preferred Fucus. Digestive efficiency was consistently higher when the animals ate Fucus than
when the animals ate Cystoseiru. Results suggest that, in D. bidentutu, feeding preferences are set
after the animals sample the environment for food quality. The existence of a compensatory
mechanism in animals kept on suboptimal food resources (Cystoseiru) is also suggested.
Keywords: Digestive efficiency; Dynamene; Food selection; Fucus; Herbivory;
Isopod
1. Introduction
Because marine macroalgae are for many small grazers (including crustaceans, mollusts and polychaetes) both a place to live on and food, the diet of these has been
frequently considered to be subordinated to the selection of habitat (Hay et al., 1990;
Dtiy & Hay, 1991; Brawley, 1992; and many others). Although in some species the
selection of food can be explained in terms of the quality of the algae [e.g. Ampithoe
valida (Smith) in Nicotri, 1980; and Dynamene mugnitoratu Holdich in Arrontes, 19901,
in others, preference for determined algae has a poor correlation with its quality as food.
* Corresponding author.
0022-0981/94/$7.00 0 1994 Elsevier Science B.V. All rights reserved
SSDI 0022-0981(94)00100-6
112
J.A.G.
Momin and J. Arronres 1 J. Exp
Mar. Bwl. Ecol. 182 (1994~ 111-121
Thus, different grazers have been shown to favour algae which provide protection
against the physical environment (e.g. wave stress, dessication) (Nicotri, 1980) or
shelter against predators (Hay et al., 1988a,b). Little more is known about many other
aspects of their feeding ecology; for instance, how the grazers rank the algae in terms
of preference. A possibility is that selection of a given alga as substratum and food might
be made after sampling the environment. If this is correct, then it is obvious that the
past history of the animals should be a key factor in understanding individual feeding
preferences.
An additional interesting aspect appears in species with a broad distribution both in
time and space. Species that can be collected from several species of macroalgae and
over a range of tidal heights are common among intertidal grazers inhabiting macroalgae (hereafter, mesoherbivores) (see Arrontes & Anadbn, 1990a,b and references
therein). Assuming that, on a scale of meters, all the specimens form part of the same
population and can move freely (see Brawley, 1992 for comments on the mobility of
mesoherbivores), the individuals of these broadly distributed species would face a
mosaic of resources of different quality and environmental conditions. The environment
is variable at least for two reasons. Firstly, because macroalgae differ in their quality
as substratum and food (Paine & Vadas, 1969; Himmelman & Carefoot, 1975; Watson
& Norton, 1985a,b) and secondly, because in many species that feed when submersed,
the higher on the shore, the shorter the time available for feeding. if specimens of a given
species are consistently collected at different tidal heights and on macroalgae ditTering
in their value as food then, some compensatory mechanism is expected to exist. In this
regard, increased digestive efBciency in animals collected high on the shore was suggested by Arrontes (1990) as a compensatory mechanism in an intertidal isopod.
In this work, we investigate how preference for different macroalgae is determined
in a widely distributed intertidal isopod, D. bidentutu (Adams). We focus on the influence of the past history of the animals on the preference for two macroalgae, Mucus
vesiculosus L. and Cystoseiru baccatu (Gmelin) Silva, and look for compensatory mechanisms in those animals kept in the laboratory with a low quality food resource. We test
the hypotheses that (1) animals kept in the laboratory with different algae as food should
exhibit different preferences and (2) animals kept with a resource of lower quality should
exhibit some compensatory mechanism, in terms of increased feeding rate or digestive
efficiency.
2. Mate&l
and rn&ods
2.1. The species
Dynamene bidentata has a broad distribution on European shores (see Holdich,
1970). In northern Spain, it has been collected on macroalgae (mainly fucaceans) over
almost the entire intertidal range (Arrontes & Anadbn, 199Oa). It is abundant during
most of the year, though conspicuous seasonal variations in abundance exist (Arrontes
& Anadon, 1990b). Juveniles swim in the water column for several hours after releasing
from the maternal pouch (Holdich, 1968, 1976). The juveniles recruit on macroalgae
J.A.G.
Momin and J. Awontes / J. Exp. Mar. Biol. Ecol. 182 (1994) 111-121
113
low in the intertidal zone and subsequently they migrate and reach macroalgae high on
the shore (e.g. Fucus spp.) (Arrontes & Anadon, 1990b). An additional habitat shift
occurs when individuals reach maturity and migrate from the juvenile to the reproductive habitats (Holdich, 1976). Therefore, it can be safely assumed that animals inhabiting a given locality come from the same population. The feeding habits of D. bidentuta
are described in Arrontes (1990). Briefly, the species predominantly ate perennial
macroalgae (on which the isopod lives) instead of delicate filamentous algae, both in
the field and in laboratory experiments. Analysis of gut contents only revealed the algae
on which the isopods were collected. This suggests that feeding forays are unlikely.
2.2. Experimental procedures
Three preference experiments were done: Experiment 1 used specimens reared in the
laboratory; Experiment 2 used specimens collected in the field on Fucus vesiculosus; and
Experiment 3 used specimens collected in the field on Fucus and Cystoseira baccatu. The
animals were collected at Btiugues, a sheltered locality in central northern Spain
(43” 38’ N, 5” 48’ W). The preference experiments were carried out in 0.5 1 tanks in
which single specimens were simultaneously offered pieces of Fucus and Cystoseira of
approximately 4 g (fresh weight). Food was offered in excess. The experiments ran for
24 h. At the end of the experiment, the position of the isopod and the number of faecal pellets under each piece of alga was recorded. Gut passage time is short in this
species (as short as 20 min in starved animals, Moran & Arrontes, pers. obs.). The
animals do not shuttle between the food plants very often. Instead, they stay for periods
of several hours. Therefore, a fine correlation between where the animals fed and where
they deposited the pellets is expected. The number of faecal pellets produced during
24 h was considered as an estimator of the feeding rate of the isopods. Preference was
assessed by comparison of individual feeding rates on each macroalga. When variances
were homogeneous, t-test, paired-sample t-tests and ANOVA were used; otherwise,
Wilcoxon matched-pairs signed-ranks test was used as alternative for the t-test (see
Siegel, 1956; Winer, 1971). Two-tailed tests were considered. Unbalanced ANOVA
followed recomendations from Shaw & Mitchell-Olds (1993). For experiments done
with animals collected in the field, specimens were used once and discarded. In order
to avoid unnatural feeding habits, the experimental animals were not starved before the
experiment (see comments by Brawley, 1992).
A summary of the experimental design of Experiment 1 appears in Fig. 1. Juvenile
specimens of D. bidentatu inhabiting Fucus were collected in March and kept in the
laboratory under controlled conditions in 2-1tanks (16 k 1 “C, with a 14: 10 h 1ight:dark
cycle). Animals were kept under continuous submergence. In the laboratory, the animals reached sexual maturity and reproduced. After the juveniles were released from
the maternal pouch, the field collected animals were discarded. The laboratory born
juveniles were distributed at random in two batches and kept in separate tanks. One
batch was fed with Fucus, while the other was fed with Cystoseira. After 40 days, the
animals of each batch were used for preference experiments (Trial 1). After the experiment, the animals of each batch were divided into two new groups, one fed with Fucus
and the other with Cystoseira. After 14 days, the specimens were used again for pref-
114
J.A.G. Morcin and J Arrontes 1 J. Exp Mar. &ol. Ecol. 182 (19941 II I-121
JUVENILES
BORN
IN THE
LABORATORY
Fucus
Cystoselra
PREFERENCE
EXPERIMENT
Fucus
PREFERENCE
EXPERIMENT
vs Cystoseira
Fucus
Trial
1
vs C.I-stoselra
EXPERIMENT
Fucus
vs Cysloseira
Fig. 1. Experimental design for Experiment
1.
erence experiments (Trial 2). At this time, the experimental isopods had four different
origins: (1) isopods kept continuously with Fucus, (2) isopods kept continuously with
Cyszoseiru, (3) isopods kept firstly with Fucus and then with Cystoseira and, (4) isopods
kept firstly with Cystoseira and then with MUCUS.
Those animals with fully developed
secondary sexual characters were discarded as the feeding habits of these specimens
in D. bidentuta are deeply altered (see Holdich, 1968).
Experiments 2 and 3 started within 3 days of collection of the isopods in the field.
2.3. Digestive eficienq
Digestive efficiency was estimated by using an indicator method which compares the
ratio of soluble sugars to structural polysaccharides in the food with the same ratio in
the faecal pellets (for full details see Arrontes, 1989). The method assumes low digestibility of structural polysaccharides whereas the soluble sugars are readily assimilated
by the isopods (Kristensen, 1972; Dal1 & Moriarty, 1982). Of course, since the method
ignores the assimilation of other materials such as protein, the results should be considered as rough estimates of true digestive efficiency. In addition, in this work, the ratio
of soluble sugars to insoluble polysaccharides in the algae is considered an estimator
of the quality of the macroalgae as food for the isopods (see also Viejo & Arrontes,
1992). The lower the ratio, the lower the quality as food (i.e. the food has a higher
proportion of undigestible components).
Digestive efficiency was estimated in the animals used in Experiment 1 after the
preference experiment. The animals were offered a piece of either Fucus or Cystoseira.
The faecal pellets produced and the piece of alga offered as food were frozen until sugar
analysis. Conditions of experimentation were the same as in preference experiments.
115
J.A.G. Morhz and J. Arrontes /J. Exp. Mar. Biol. Ecol. 182 (1994) 111-121
Digestive efficiency of animals in Experiment 2 and 3 was estimated using the faecal
pellets produced and algae offered in each preference experiment and thus, paired data
existed for those animals which ate both algae.
3. Results
In Experiment 1, after 40 days (Trial l), isopods reared under laboratory conditions,
either on MUCUS
or Cystoseiru, showed no preference for either of the two algae offered
as food (t-test, for animals kept on MUCUS,
r = 0.33, 18 df, p>O.O5; animals kept on
Cystoseiru, t = 0.79, 19 df, p> 0.05) (Fig. 2a). Because in some of the preference experiments, variances were not homogeneous (F ratio), square root transformation was
done for all data sets. Significant differences existed, however, in the feeding rate of the
isopods in relation to their origin. When the total production of faecal pellets per animal
was considered, animals kept on Cystoseiru fed more actively than those kept on FUCU.S
(t-test, t = 2.69, 37 df, p < 0.05). Digestive efficiency was significantly higher when the
animals ate MUCUS
than when the animals ate Cystoseiru (Fig. 2B, Table 1). Animals
reared on Cystoseiru were not less efficient than those kept on MUCUS.
In terms of the
S/I ratio, the quality of Fucus as a food resource proved to be higher than Cystoseiru.
For instance, for Trial 1 of Experiment 1, the mean S/I ratio for Fucus was 70.52%
(SE = 2.76, n = 14) and the mean ratio of Cystoseiru was 31.11% (SE = 1.95, n = 10).
Differences were significant (t-test, t = 11.65, 2 1 df, p c 0.00 1; variances were not equal
and number of degrees of freedom was estimated as suggested by Winer (1971)).
The second trial of Experiment 1, also done with laboratory reared isopods, showed
that within groups of animals with identical origin no preference for either of the two
algae existed (Wilcoxon tests, p> 0.05, Fig. 3a). However, when pooled data from all
specimens used in Trial 2 were considered, a preference for Fucus existed (Wilcoxon
test, n = 40, z = 2.10, p = 0.018). The past history of the animals in the laboratory sig-
F
FUCUS
c
F
C
Cystoseira
0
F
C
Fucus
F
C
Cystoseira
Fig. 2. Experiment 1, Trial 1. (A) Consumption
of Fucus vesiculosus and Cystoseira baccata by specimens of
D. bidentata kept in the laboratory with either Fucus or Cystoseira. (B) Digestive efficiency of the same
specimens. Food: F = Fucus; C = Cystoseira. Figures are numbers of animals. Data are untransformed.
J A.G. Morcin and J. Arrontes /J. Exp. Mar. Bwl. Ecol. 182 (19941 III-121
116
Table 1
Analysis of mean digestive efficiency of specimens of D. bidentata kept in the laboratory
and Cystoseira baccata when fed with Fucus and Cystoseira
df
Source
1
1
Origm
Food
OxF
Residual
1
18
Unbalanced
ANOVA,
were homogeneous.
type III sum of squares,
on Fucus vesmdosus
MS
b
I’
1279.7
37318
246.5
380.1
3.37
9.82
O.h5
0.083
0.006
0.43 1
SAS procedure
(Shaw & Mitchell-Olds,
1993). Variances
nificantly influenced the feeding rate (Fig. 3a, Table 2). Specifically, the effect of the
immediate origin was significant. The feeding rate of animals kept with Cystoseira in
the second part of the maintenance period was greater than that of animals which were
kept with Fucus. As in the previous trial, animals were more eflicient when they were
offered Fucus as food than when they consumed Cystoseira (t-test, t = 3.44, 29 df,
p < 0.05; Fig. 3b).
Results of the preference experiments done with animals collected in the field (Experiment 2 and 3) were clearly different. A marked preference for Fucu.s existed in both
experiments, Cystoseira being little consumed (Figs. 4, 5; Experiment 2: t-test, t = 4.56,
34 df, p< 0.01; Experiment 3: origin MUCUS,
r-test, t = 6.77, 17 df, p< 0.01, origin
Cystoseira, t-test, t = 5.17, 13 df, p-c 0.01). In addition, in Experiment 3, no differences
in the feeding rate existed between animals of di&rent origin (t-test, t= 0.29, 30 df,
p> 0.05). In expts. 2 and 3, digestive efficiency was estimated in the same experiment
than preference, therefore for some experimental animals efficiency with Fucus and
Cystoseira was obtained, while in others estimations were made only with either Fucus
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F
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Fig. 3. Expenment 1, Trial 2. (A) Consumption
of Fucus vesiculosus and Cystoseira baccata by specimens of
D. bidentata kept in the laboratory on Fucus (FF); first on Fucus and then on Cystoseira (FC); first on
Cysroseira and then on Fucus (CF) and on Cysroseira (CC). (B) Digestive eBieiency of the same specimens
(origins pooled). C, F and figures as in Fig. 2.
J.A.G. Morcin and J. Arrontes /J. Exp. Mar. Biol. Ecol. 182 (1994) 1 II-121
117
Table 2
Analysis of mean feeding rate of specimens of D. bidentata kept in the laboratory under different conditions:
initially on Fucus or Cystoseira (first origin), then each group was divided in two new groups which were kept
on Fucus or Cystoseira (second origin)
Source
df
MS
F
P
First origin
Second origin
FOxSO
Residual
1
1
1
36
63.73
125.42
34.54
20.97
3.04
5.98
1.65
0.090
0.020
0.218
ANOVA type III sum of squares, SAS procedure
geneous after square-root transformation.
(Shaw
& Mitchell-Olds,
1993). Variances
were homo-
or C~~~toseira. Statistical tests (paired-sample
t-tests) were performed only on animals
which fed on both algae. No significant difference existed in digestive efficiency in the
Experiment 2, done with animals exclusively collected on Fucus (t-test, t = 0.50, 11 df,
p> 0.5). In Experiment 3, animals were more efficient when they ate Fucus than when
they ate Cystoseiru (origin ignored, t-test, t = 11.5 1, 10 df, p < 0.01).
4. Discussion
Results suggest that feeding preferences in D. bidentata are strongly influenced by the
previous experience of the animals. When the isopods were reared with a single species of macroalga as food (Fucus or Cystoseira), no preference was observed in the
experiments. When the experiment was repeated with the same isopods 2 wk later, these
exhibited preference for Fucus (pooled data). A similar result, marked preference for
Fucus. was obtained with isopods collected in the field, either on Fucus or Cystoseira.
B
t
30
+
-
N=35
C
F
Fig. 4. Experiment 2. Preference (A) and digestive efficiency (B) of specimens of D. bidentata collected in
the field on Fucus vesiculosus when they were offered Fucus and Cystoseira baccata as food. C, F and figures
as in Fig. 2. Figures differ m A and B because not all the animals ate both algae.
J.A.G. Morcin and J. Arrorltes / J. Exp. Mur. &ol. Eml. 182 (1994, 111-121
118
Cystoseira presumably is a resource of lower quality as food than Fucus (it has a lower
ratio of soluble to insoluble sugars). In most cases, digestive efIiciency of D. bidentatu
is higher with Fucus than with Cystoseira, which suggests that the isopods might be
choosing the most rewarding food item (see also Arrontes, 1990; Viejo & Arrontes,
1992). Considering that the experimental animals collected in the field might have been
in contact with a wide range of macroalgae, including Fucus and Cystoseiru, these results suggest that feeding preferences in D. bidentata may be set after the animals have
sampled the environment
for food quality. When the experimental
animals were not
given the opportunity
to sample different algae (as in Trial 1 of Experiment
1) no
preference existed.
This conclusion is consistent with, and helps us to understand,
previous information
on the life history of D. bidentata in Spain (Arrontes & Anadon,
1990b). Juveniles
recruit on macroalgae low on the shore, predominantly
on the red alga Gelidium latifblium (Grev.) Thur. et Born. and Cystoseiru. No recruitment of newly released juveniles has been observed on Fucus, which is found higher on the shore. After a short
period, the abundance
of juvenile isopods on low-shore macroalgae decreases. D. bidentutu first appears on Fucus as 2nd or 3rd stage juveniles, reaching high densities.
Thus, apart from periods of massive recruitment, the density of D. bidentuta on Fucus
is considerably
higher than on Cystoseira.
A contradictory
result appears in Experiment 2. The isopods favoured Fucus though
no difference in digestive efficiency was observed between Fucus and Cystoseira. Macroalgae are not homogeneous
resources and parts of different quality are likely to exist
on a single plant. On a whole, however, Dynamene should be more efficient when feeding
Fucus than when feeding Cystoseiru (as it was obtained in 3 out 4 experiments).
Our
interpretation
is that experimental isopods had their feeding preferences established
when the experiment was carried out. Alternate explanations
should include other
differences between the two algae such as different quality as refuge against physical
factors (Nicotri, 1980) or predation (Hay et al., 1988a). For some mesoherbivores,
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t
C
Fucus
F
C
Cystoseira
F
C
Fucus
F
C
Cystoseira
Fig. 5. Experiment 3. (A) Consumption
of Fucus wsiculosus and Cptoseira baccata by specimens of D.
bidentaca collected in the field on Fucus and Cysroseiru. (B) Digestive efficiency of the same specimens. C,
F and figures as in Fig. 2.
J.A.G. Morh
and J. Arrontes / J. Exp. Mar. Biol. Ecol. 182 (1994) 111-121
119
selection of substratum has been related to the physical structure of the habitat (Dean
& Connell, 1987a,b,c; Hacker & Steneck, 1990) though predation is the factor more
frequently invoked to explain the distribution of mesoherbivores (Edgar, 1983; Dean
& Connell, 1987~; Hohnlund et al., 1990; but see Edgar, 1990, for food limitation in
mesoherbivores and Schneider & Mann, 1991, for species-specific responses).
Sampling of the environment as a mechanism to set feeding preferences is only
feasible when the consumers are mobile enough to visit patches of habitat of different
quality. Direct measurements on the short term mobility of D. bidentata are not available. However, habitat shifts (Holdich, 1968, 1976; Arrontes & Anadon, 1990b) indicate that the specimens can readily travel from one patch of macroalgae to another.
High mobility is a widespread feature among mesoherbivores inhabiting macroalgae
(see Brawley, 1992, for a review) though nocturnal habits and the inherent difIlculty of
direct observations in the field have led to some generalizations on the low mobility of
mesoherbivores (e.g. Hay et al., 1987).
It has been assumed that Cystoseira is a low quality resource for D. bidentata in relation to Fucus. If this is true, then the observed increase in the feeding rate of specimens kept in the laboratory with Cystoseira as sole resource can be considered as a
compensatory mechanism. D. bidentata is a very widespread isopod and despite the
general pattern of abundance of the isopods in the field outlined above, it is also frequently collected on many other macroalgae (Arrontes & Anadon, 1990a,b). It can be
safely assumed that different macroalgae have different values as food (Paine & Vadas,
1969; Carefoot, 1973; Himmelman & Carefoot, 1975; Watson & Norton, 1985a,b). If
the specimens of D. bidentata could match the feeding rate to the quality of the algae
on which live, this would help to understand the broad distribution of D. bidentata. A
different compensatory mechanism has been already suggested in D. bidentata (Arrontes,
1990). Specimens living high on the shore were found to exhibit an increased digestive
efficiency in relation to specimens collected lower on the shore. Increased digestive
efficiency would compensate for reduced time available for grazing in specimens inhabiting high tidal levels (D. bidentata only feeds when submersed, Holdich, 1976;
Moran & Arrontes, pers. obs.).
The compensatory mechanism was found in the laboratory, but the important question is whether it exists in the field. Higher feeding rate was not observed in isopods
collected in the field on Cystoseira (Experiment 3). At least, two explanations are
possible. First, the presence of isopods on Cystoseira may be purely circumstantial.
Second, the isopods may, in fact, live permanently on Cystoseira but their diet might
include other food items apart from Cystoseira (epiphytes, other accompanying macroalgae). A diversified diet might cope with the problems of monophagy on an unbalanced resource, rendering unnecessary any compensatory mechanism.
A practical consideration for future experimentation with mesoherbivores emerges
from the results. Most of the preference experiments using mesoherbivores have been
done with species which were selected because they were abundant and widespread
[e.g. Littorina spp. in Lubchenco (1978) and Barker & Chapman (1990); Idotea spp.
in Nicotri (1980) and Salemaa (1987); and Hyale spp. in Buschmann (1990)]. If individual preferences and feeding rates can be influenced by the species that the isopods
have encountered or fed upon in the field, it is clear that feeding preferences assessed
1’0
J.A.G
Morrin and J. Arrontes 1 J. Exp. Mar. B~ol. Ecol. 182 (19941 111-121
from the results of multiple choice experiments in the laboratory can be biased by the
past experience of the animals in the field. Sampling of the environment and/or compensatory mechanisms might be expected in widespread species which face heterogeneous environments, with patches differing in their quality for the consumers. Therefore, special attention should be paid in offering plant species that the animals have in
their natural environment, specially when experiments compare different populations
with different origin.
Acknowkdgements
We thank R.M. Viejo for help during the experimental part of the work and for
comments on the manuscript. Comments and corrections from two anonymous referees
considerably improved the paper. The work was partially supported by Grant TA 92/43
of the University of Oviedo.
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