Journal of Plankton Research Vol.23 no.9 pp.945-951, 2001
© Oxford University Press 2001
Fish-induced life-history shifts in the cladocerans Daphnia and Simocephalus: are they positive or negative responses?
Research And Education Centre For Inland Water Environment, Shinshu University, 5-2-4 Kogandori, Suwa 392-0027, Japan
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Abstract |
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The cladocerans Daphnia and Simocephalus were exposed to fish smells under different food conditions, and their life-history parameters were analysed. They showed similar responses to fish smells and food shortage: lowered juvenile growth rate, reduced mature size, elongated maturation time, reduced brood size and increased offspring size. The life-history changes induced by the fish smell might be a result of deleterious effects of the factor. Although it has been considered that fish-induced life-history shifts in Daphnia are positive responses to predators, our results suggest that they are negative responses of animals that show some other positive responses to fish, such as behavioural and morphological changes to reduce mortality due to predation. Synergism was detected in the effects of the fish smell and food deficiency, which suggests that fish smell reduces the tolerance of Daphnia to an environmental stress, food shortage.
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INTRODUCTION |
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TOPAbstractINTRODUCTIONMETHODRESULTSDISCUSSIONREFERENCES |
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It has been found that the cladoceran Daphnia pulex changes its morphology (developing protuberant structures) in response to chemicals released from a predator, the phantom midge Chaoborus (Krueger and Dodson, 1981
). Similar findings were obtained in many Daphnia species, including D. ambigua, D. galeata mendotae, D. cucullata, D. retrocurva and D. carinata (Grant and Bailey, 1981; Hebert and Grewe, 1985; Dodson, 1988a; Tollrian, 1990). The morphological responses of Daphnia have been considered to be adaptive, because the protuberant structures reduce predation risk by potential predators (Havel and Dodson, 1984; Parejko, 1990; Tollrian, 1995). The chemicals released from predators have thus been called kairomones, defined as chemicals giving benefit to receivers rather than releasers (Brown et al., 1970).
The morphological changes are, however, associated with a cost, which appears in some life-history parameters in Daphnia exposed to predator kairomones, probably because the Daphnia use energy in their morphological responses to the kairomones. The kairomones lower growth rate, reduce mature size, lengthen maturation time and reduce brood size (Havel and Dodson, 1987; Riessen and Sprules, 1990; Black and Dodson, 1990; Spitze, 1991, Hanazato and Dodson, 1992). Thus, such changes in life-history characteristics are considered to be negative responses by Daphnia to the kairomone.
Dodson (Dodson, 1988b) found that Daphnia showed an adaptive response in behaviour to chemicals released from fish; Daphnia increased their depth of occupation in an aquarium when exposed to the chemicals. The behaviour was considered to be a mechanism to avoid fish predation. It was shown experimentally that Daphnia hyalinexgaleata migrated vertically by day, a behaviour to avoid fish, in a Plankton Tower in the presence of fish smell (chemicals) but not in its absence (Lampert and Loose, 1992). Therefore, these chemicals are also kairomones.
In response to fish kairomones, Daphnia also changes its life-history parameters. The animals' mature size, maturation time and egg and offspring size are reduced, and their clutch size is increased (Dodson, 1989; Machacek, 1991, 1993; Stibor, 1992; Weider and Pijanowska, 1993; Hanazato, 1995). These changes may increase the chance of survival of individual Daphnia and the population growth rate in the presence of fish that prefer larger prey. The responses are therefore likely to increase the population fitness in the presence of predators.
The life-history responses of Daphnia to kairomones from invertebrate predators have been considered to be negative responses (costs associated with morphological responses), and those to fish kairomones to be positive responses. Thus, a question arises (Hanazato, 1998): what is the cost associated with the life-history responses to the fish kairomones by Daphnia? In other words, what are the negative effects of the kairomone?
It has been hypothesized that Daphnia that change life history parameters in response to fish kairomones reduce their tolerance to environmental stress, and that this is the cost (Hanazato, 1998).
In this study, we tried to identify the negative effects of fish kairomones on daphnids by analysing their life-history responses to the kairomones under an environmental stress, food shortage. We used Daphnia pulex and Simocephalus vetulus, the latter is a large daphniid Cladocera inhabiting the vegetation area of lakes. We assumed that Simocephalus shows a life-history response to fish kairomones similar to that of Daphnia, because it is also vulnerable to fish predation.
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METHOD |
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The D. pulex used in the experiments were offspring of an individual hatched from a resting egg in the bottom sediment from Lake Kasumigaura more than 5 years previously. The lake is inhabited by pond smelt, carp, crucian carp, topmouth gudgeon and other fish (Sakai et al., 1984
). We also used a clone of Simocephalus vetulus collected from Akanoi Bay, Lake Biwa, Shiga Prefecture (the largest lake in Japan), which is inhabited by abundant fish of various species, including topmouth gudgeon and bluegill sunfish. All cladocerans had been reared in stock cultures with the green alga Selenastrum capricornutum (2 x 105 cells ml–1, i.e. 2 µg dry wt ml–1) at a temperature (20 ± 2°C) and in aphotocycle-controlled room (16 h light/8 h dark). Two species of fish (topmouth gudgeon, Pseudorasbora parva and bluegill sunfish, Lepomis macrochirus) were used to make fish-conditioned water containing kairomones. Topmouth gudgeon (body length ca. 80 mm) were donated by Nagano Prefectural Fisheries Experimental Station, Suwa, which collected them from Lake Suwa. Bluegill sunfish (body length ca. 50 mm) were caught from Tamizo-ike pond, Nagano Prefecture, by Mr M. Yamamoto of Shinshu University. The fish were reared individually in aquaria, each containing 15 l of aged tap water with D. pulex, D. magna, S. vetulus as food. Some of the aquarium water (1.2–1.5 l) was withdrawn and filtered through Whatman GF/C filters every day to remove any particles larger than about 1 µm in size, and was used as the fish-conditioned water in the experiments. The same amount of aged tap water was added to the aquaria to compensate. Filtered aged tap water in which fish had never been reared was used as a control.
Four experiments were performed with different species of cladocerans in water conditioned by different fish species or in control water containing Selenastrum at different concentrations. The conditions for each experiment are shown in Table I. The cladocerans were transferred to culture waters (control water, or water conditioned by topmouth gudgeon or bluegill) with different concentrations of Selenastrum (Table I) when they had eggs in their brood chambers. Young born within 10 h were reared individually in 50 ml beakers containing 50 ml of the same culture water as used for the egg hatching at 20 ± 2°C under a 16 h light/ 8 h dark photocycle.
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The rearing medium was renewed every day, at which time the body length of the animals (from the top of the head to the posterior of the carapace) was measured to the nearest 0.003 mm under a binocular dissecting microscope. The number of eggs (if any) in the brood chamber was also determined. When neonates were born to the individuals examined, their body length was measured under the microscope. Culture was terminated when an animal produced its fourth brood, except in Experiment 3, which was continued until all individuals died, and the life span and total number of offspring produced were determined. The growth rate during juvenile stages (GR) was calculated as:
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Differences in life-history parameters among treatments (different concentrations of fish kairomones x different food concentrations) were tested by two-way ANOVA for each cladoceran species.
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RESULTS |
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In Experiment 1, Daphnia lengthened their maturation time when exposed to the smell of topmouth gudgeon at both high and low food levels (Hfood and Lfood, respectively), and at Lfood in both the presence (K+) and absence (K–) of the fish smell (kairomone) (Table II
). These results indicate that both fish smell and lower food concentration affected the maturation time. The effects of both factors and their interaction were highly significant (P <0.001). The fish smell and lowered food concentration increased the instar at maturation of Daphnia, which means that Daphnia molted more times before reaching maturity when exposed to fish smell and to food deficiency.
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Fish smell significantly reduced size at maturation. Reduced food density also decreased the size, but the effect was not significant. The increased maturation time and decreased size at maturation under the conditions of K+ and Lfood reduced the growth rate during juvenile stages. Fish smell and food deficiency had a significant effect (P <0.001) on the growth rate. Both fish smell and low food concentration reduced brood sizes significantly, although the effect was stronger for the latter factor. There was no significant interaction of the two factors on brood size. Offspring size increased significantly when mothers were exposed to both factors, but there was no significant interaction between the factors.
In Experiment 2, effects of fish smell on Daphnia were analysed at three different food levels [high food (Hfood), medium food (Mfood), and low food (Lfood) levels]. Fish smell significantly increased maturation time, instar at maturation and offspring size, and decreased juvenile growth rate and brood sizes; the reduced food density significantly induced the same life-history responses (Table III). Interaction of the two factors was highly significant in most parameters examined.
The same tendencies were also observed for Simocephalus from Lake Biwa in Experiment 3, where the animals were exposed to topmouth gudgeon at different food levels (Table IV). The effects of fish smell, food deficiency or both on some parameters (maturation time, maturation size, juvenile growth rate, brood size, offspring size) were statistically significant. Significant interaction between the two factors was found only for juvenile growth rate.
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In Experiment 4, Simocephalus were exposed to the smell of bluegill at two food levels. Fish smell increased maturation time but reduced maturation size, juvenile growth rate and brood size (Table V
). No effect on offspring size was detected. Food deficiency increased the maturation time and offspring size, and decreased maturation size, juvenile growth rate and brood size. Significant interactions between fish smell and food density were found for some parameters.
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Life span and total number of offspring produced were determined for Simocephalus in Experiment 3. The total number of offspring was reduced by fish smell and food shortage (P <0.001), and reduced more by both together (P <0.001) (Table IV
). Fish smell also reduced life span. In contrast, low food concentration increased life span by up to 36%. The effects of fish smell and food shortage on life span were statistically significant, but the interaction was not. |
DISCUSSION |
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TOPAbstractINTRODUCTIONMETHODRESULTSDISCUSSIONREFERENCES |
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Daphnia pulex and S. vetulus showed similar responses in life history parameters to food deficiency and fish kairomones: reduced juvenile growth rate, reduced mature size, delayed maturation time, increased instar number at maturation, reduced brood size and increased offspring size. Significant interactions were obtained in some of the effects of the two factors, indicating synergism.
The life-history responses to food deficiency that we observed agree with those reported in Daphnia (Gliwicz and Guisande, 1992; Guisande and Gliwicz, 1992; Hanazato, 1996). The increased size of offspring where food is limited is a result of a change in energy allocation by mothers from somatic growth to reproduction, and the responses in the other parameters are due to a reduced amount of energy available (Tessier and Consolatti, 1989; Gliwicz and Guisande, 1992; Guisande and Gliwicz, 1992).
In contrast, the life-history responses to fish smell (kairomone) reported here do not agree with those in other papers except for mature size. Other papers reported that Daphnia exposed to fish kairomones had reduced mature size, maturation time and offspring size, and increased brood size (Machacek, 1991, 1993; Stibor, 1992; Weider and Pijanowska, 1993; Hanazato, 1995). These papers explained the life-history shifts as positive responses of Daphnia, because reduced mature size and offspring size produce small adults, which are less vulnerable to the visually oriented predator fish, and reduced maturation time and increased brood size increase the population growth rate to compensate for population reduction by predation. However, our experiments show that the responses of Daphnia and Simocephalus to fish kairomones are similar to responses to food deficiency. This suggests that they are negative responses to the kairomones. The fish kairomones might alter cladoceran behaviour, morphology, or some other characteristics, and force the animals to lose more energy or gain less energy, resulting in negative responses. The decreased energy gain may be a probable factor in inducing the responses, because the increased offspring size is similar to the response to food-limitation, where energy gain was reduced, and dissimilar to the response to pesticide contamination (Hanazato and Dodson, 1995), where energy loss might be large. The mechanism by which kairomones altered the energetics of the animals in our experiments should be analysed in future studies.
The reduction in mature size is a phenomenon commonly observed in this study and others of Daphnia and Simocephalus (Dodson, 1989; Machacek, 1991, 1993; Stibor, 1992; Weider and Pijanowska, 1993; Hanazato, 1995). Although most authors considered it a positive response, it could be a negative response accompanying other positive responses to the fish kairomone, because a reduced mature size also occurred in Daphnia exposed to food shortage [this study and also (Guisande and Gliwicz, 1992; Hanazato, 1996)], pesticide contamination (Hanazato and Dodson, 1992, 1995), and oxygen deficiency (Hanazato and Dodson, 1995).
The purpose of this study was to identify the costs associated with the life-history responses to fish kairomones. However, our results suggest that the changes in life-history parameters are themselves induced by costs.
Some of the life-history changes induced by fish kairomones differ between this study and others. The differences may be due partly to differences in species and clones used and in kairomone concentration. However, whether each life-history response to the kairomones is positive or negative should be reconsidered.
The fish kairomones and food deficiency caused deterioration in some life-history parameters of Daphnia and Simocephalus, and the two factors were synergistic. The synergism may actually occur in lakes, where cladocerans are exposed both to fish kairomones and food deficiency when they take daytime refuge from fish in the hypolimnion and areas of vegetation, where food concentrations are lower than in the pelagic epilimnion (Davies, 1985; Lampert, 1989). The result suggests that fish kairomones are stressors on the cladocerans, and that the kairomones make the animals more vulnerable to food deficiency and vice versa. This supports the hypothesis that predators control zooplankton populations by releasing kairomones, which reduce the tolerance of the prey to various environmental stress (Hanazoto, 1998).
The fact that fish kairomone and food deficiency have a similar effect on the life-history parameters of cladocerans was also found in the total number of offspring produced by Simocephalus in Experiment 3. However, the two factors had different effects on life span: kairomones reduced life span whereas low food concentration increased it. Under food shortage, the animals might have a strategy in which they elongate life span to increase the total number of offspring produced. Such a strategy does not apply for the kairomones.
This study has shown that Daphnia and Simocephalus show similar responses to fish kairomones. Although the habitats of the two cladoceran species differ (Daphnia are plankton in the pelagic zone, whereas Simocephalus are often attached to aquatic macrophytes in the littoral zone), Simocephalus may use chemicals from fish as a cue to initiate strategies against predator fish, as does Daphnia.
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Acknowledgments |
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We thank Mr M. Yamamoto and Nagano Prefectural Fisheries Experimental Station, Suwa, who kindly offered us bluegill sunfish and topmouth gudgeon. This study was partly supported by a Grant-in-Aid (No. 10480144) toT. Hanazato from the Ministry of Education, Science and Culture, Japan.
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Received on December 14, 2000
; accepted on April 5, 2001
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