Cannibalistic behaviour of rock-pool copepods: An experimental approach for space, food and kinship

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Abstract

Studies on cannibalism in harpacticoid copepods are restricted to predation on naupliar larvae in rock-pool harpacticoids of the genus Tigriopus. An earlier experimental study on the Mediterranean copepod Tigriopus fulvus indicated that females recognized their own larvae and preferentially preyed on nauplii other than their own. In a series of laboratory experiments, we tested if there were differences in naupliar predation as a function of crowding, food level and sex in Tigriopus brevicornis and T. fulvus. Results show that cannibalism was restricted to the first larval stages (N1 and N2). Both food availability and adult density significantly affected the predation rate. Contrary to earlier suggestions, adult males also preyed on the nauplii. We found no evidence that adults spare their own offspring, for neither T. fulvus nor T. brevicornis.This is in accordance with what one would expect for species having the life history characteristics of Tigriopus, i.e.: multiple broods and large number of offspring. Earlier results indicating parental care in Tigriopus must be taken with caution.

Introduction

Cannibalism, defined as intraspecific predation, is a behaviour trait found in a variety of animals, from protozoa to birds and mammals (e.g. Fox, 1975, Polis, 1981, Elgar and Crespi, 1992a). This behaviour is a major strategy in the biology of many species and may influence population structure, life history, competition for mates and resources, and other behaviours (Polis, 1981). Often it develops at ecological time scales as a reaction to food scarcity (Fox, 1975) but other factors such as population density (Fox, 1975, Polis, 1981), predator size and sex, and size or moult stage of the prey (Luppi et al., 2001) may affect this behaviour.

Cannibalism of newborn animals is widespread and common in nature (Polis, 1981). Seizing a similarly sized victim may be a highly energy consuming and rather risky way of acquiring nutrients. To minimize the risk, individuals from many cannibalistic taxa preferentially cannibalize on small and vulnerable stages (Schausberger, 2003). Intraspecific predation on smaller immature life stages has been observed in several marine and estuarine crustacean species and can be the main cause of juvenile mortality in size-structured populations (Sparrevik and Leonardsson, 1995, Luppi et al., 2001, Moksnes, 2002). It can also result in age-specific habitat segregation as already reported for isopods (Leonardsson, 1991, Sparrevik and Leonardsson, 1995), crabs (Kurihara et al., 1989), fishes (Foster et al., 1988) and aquatic insects (Robinson et al., 1991, Sih and Krupa, 1992). In the terrestrial environment, preferential cannibalism on larvae has been well reported for adult phytoseiid mites (Croft et al., 1996, Schausberger, 1997, Walzer and Schausberger, 1999, Schausberger and Croft, 2001).

The most intriguing costs of cannibalism are the potential loss of inclusive fitness when a cannibal kills and consumes a genetically related individual (Elgar and Crespi, 1992b). Negative fitness, consequences of consuming one's own young, has resulted in the evolution of prey discrimination in a number of cannibalistic taxa (Anthony, 2003). Animals from various groups appear to be able to recognize their kin and display favouritism to relatives (Komdeur and Hatchwell, 1999, Schausberger and Croft, 2001, Anthony, 2003). For many species, this nepotism is expressed as differential cannibalism of kin and non-kin (Elgar and Crespi, 1992a, Pfennig, 1997). Nevertheless, although kinship has been considered a fundamental factor in the evolution of cannibalism (Fox, 1975, Polis, 1981, Elgar and Crespi, 1992b), the indirect inclusive benefits of kin recognition must be substantial for this behaviour to be maintained by natural selection.

Intraspecific predation of nauplii by adults has been reported for several calanoid copepods (Landry, 1981, Conley and Turner, 1985, Daan et al., 1988). So far, no evidence exists of nauplii recognition by mothers or/and preferential cannibalism. When it comes to harpacticoids, this subject is restricted to only two studies, which reported a cannibalistic behaviour in the rock-pool genus Tigriopus (Lazzaretto and Salvato, 1992, Lewis et al., 1998). The species of this genus are found in the supralittoral fringe of almost every ocean (Damgaard and Davenport, 1994, Davenport et al., 1997) and since its earliest descriptions, its congeners have become familiar subjects in a variety of mensurative and manipulative studies of harpacticoid copepod biology (Powlik, 1999). Lewis et al. (1998) described T. californicus as cannibalistic, often ingesting their own nauplii or even younger copepodite stages. Lazzaretto and Salvato (1992) also reported the existence of cannibalistic behaviour in laboratory-reared T. fulvus. However, this cannibalism was restricted to females and non-related nauplii since mothers were found to spare their own offspring. Lazzaretto and Salvato (1992) also suggested that males do not exhibit this cannibalistic behaviour and that predation is limited to the first larval stages.

In this study, a series of experiments was carried out using the Mediterranean Tigriopus fulvusand the Atlantic Tigriopus brevicornis to see if there is a cannibalistic behaviour of these harpacticoid copepods on their own nauplii and what the major regulating factors are. We tested specifically the following hypothesis: H1: Adult females of T. brevicornis and T. fulvus prey on their own nauplii and hence do not exhibit kinship recognition; H2: Naupliar predation is both food and density dependent H3: Adult males cannibalize on nauplii larvae to the same extent as females; H4: Predation on naupliar larvae by adults is restricted to the first larval stages.

Section snippets

Materials and methods

All animals used in the experiments came from cultures reared from T. brevicornis and T. fulvus individuals collected in the west coast of Sweden (Atlantic Ocean) and Mallorca, Spain (Mediterranean Sea), respectively. The diatom Phaeodactylum tricornutum was cultured in f2 medium (Guillard, 1975) and used as food in the experiments. At the onset of each experiment density estimates of the microalgae were calculated by counting cells from a known volume of culture medium under high power

Food effect

There was a significant decrease in predation rates with increasing amount of food (p < 0.01, HSD: 16 × 102 > 8 × 102 > 2 × 102, 0; Fig. 1a). The results from the two-way ANOVA showed no significant interaction between the factors ‘species’ and ‘food level’ (p > 0.05). Still, at each resource level and for both copepod species, numbers of nauplii were significantly higher (p < 0.05) in the control plates without females than in plates with females. Results from a 2-way ANOVA performed only for control plates

Discussion

The results of the present study clearly show that adult T. brevicornis and T. fulvus feed on their own nauplii. Besides, when comparing the food effect (with mothers) and the sex effect (with non-related females) experiments at equivalent food levels, we saw no significant differences (p > 0.05) in predation rates indicating that females ate their own larvae to the same extent as they ate non-kin. These observations are in sharp contrast to what was described by Lazzaretto and Salvato (1992) who

Acknowledgements

We thank G. Fonseca and L. Arroyo for valuable comments and suggestions on earlier versions of the manuscript. [RH]

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