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 Organismos y Sistemas, Universidad de 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, mol- lusts 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 macro- algae (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 sug- gested 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 influ- ence 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 mecha- nisms 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 reproduc- tive habitats (Holdich, 1976). Therefore, it can be safely assumed that animals inhab- iting 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 fae- cal 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 2-1 tanks (16 k 1 “C, with a 14: 10 h 1ight:dark cycle). Animals were kept under continuous submergence. In the laboratory, the ani- mals 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 experi- ment, 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

PREFERENCE EXPERIMENT

Fucus vs Cystoseira

Cystoselra

PREFERENCE EXPERIMENT Trial 1

Fucus 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 digest- ibility 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 con- sidered 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.

J.A.G. Morhz and J. Arrontes /J. Exp. Mar. Biol. Ecol. 182 (1994) 111-121 115

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 ex- periments, 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 0

c F C F C F C FUCUS Cystoseira Fucus 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.

116

Table 1

J A.G. Morcin and J. Arrontes /J. Exp. Mar. Bwl. Ecol. 182 (19941 III-121

Analysis of mean digestive efficiency of specimens of D. bidentata kept in the laboratory on Fucus vesmdosus and Cystoseira baccata when fed with Fucus and Cystoseira

Source df MS b I’

Origm 1 1279.7 3.37 0.083

Food 1 37318 9.82 0.006

OxF 1 246.5 O.h5 0.43 1

Residual 18 380.1

Unbalanced ANOVA, type III sum of squares, SAS procedure (Shaw & Mitchell-Olds, 1993). Variances

were homogeneous.

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 (Ex- periment 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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z 0 0 L-I F C F C F C F C

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B

FF FC CF cc

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.

Table 2

J.A.G. Morcin and J. Arrontes /J. Exp. Mar. Biol. Ecol. 182 (1994) 1 II-121 117

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 1 63.73 3.04 0.090 Second origin 1 125.42 5.98 0.020 FOxSO 1 34.54 1.65 0.218 Residual 36 20.97

ANOVA type III sum of squares, SAS procedure (Shaw & Mitchell-Olds, 1993). Variances were homo-

geneous after square-root transformation.

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 spe- cies 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.

t

C N=35

30

+

-

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.

B

118 J.A.G. Morcin and J. Arrorltes / J. Exp. Mur. &ol. Eml. 182 (1994, 111-121

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 re- sults 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 lati- fblium (Grev.) Thur. et Born. and Cystoseiru. No recruitment of newly released juve- niles 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. bi- dentutu 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. Macro- algae 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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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 avail- able. However, habitat shifts (Holdich, 1968, 1976; Arrontes & Anadon, 1990b) indi- cate 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 re- lation to Fucus. If this is true, then the observed increase in the feeding rate of speci- mens 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 fre- quently 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 in- habiting 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 ques- tion 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 mac- roalgae). A diversified diet might cope with the problems of monophagy on an unbal- anced 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 indi- vidual 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 com- pensatory mechanisms might be expected in widespread species which face heteroge- neous environments, with patches differing in their quality for the consumers. There- fore, 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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