Ontogenetic Changes in Daphnia Responsiveness to Fish Kairomone

Hydrobiologia 526: 219–224, 2004. J. Pijanowska, P. Dawidowicz, A. Jachner & K. Szeroczyn´ska (eds), Cladocera. Ó 2004 Kluwer Academic Publishers. Printed in the Netherlands.

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Ontogenetic changes in Daphnia responsiveness to fish kairomone Andrzej Mikulski, Dorota Lipowska & Joanna Pijanowska Department of Hydrobiology, Warsaw University, Banacha 2, 02-097 Warsaw, Poland

Key words: Daphnia, kairomones, life history, ontogenesis

Abstract Exposing Daphnia to the presence of a predator at different stages of ontogenesis leads to different reactions. Predator-induced changes of life history parameters related to the first reproduction schedule, as age and size at first reproduction, take place in the stage preceding that one in which vitellogenesis occurs. Determination of the amount of energy allocated to this first reproduction, including offspring number, occurs in the first 24-h of life. In case of parameters related to reproduction schedule, time since induction until the release of the first clutch of offspring is tens of hours; in case of allocation patterns – more than 100. This suggests that Daphnia do not ‘‘remember’’ the information of a potential threat but, instead, the decisions on future development are undertaken once they have estimated the reigning predation regime. Shortening of the period during which eggs are carried in the brood chamber, thus shortening the time when Daphnia are more easily visible, may be another adaptation to reduce danger from fish predation and so increasing the probability of survival until the first successful reproduction.

Introduction Planktonic animals may change their life parameters in the presence of chemical substances released into the water by predators or prey. For example, threatened individuals may descend deeper (Dawidowicz & Loose, 1992; Dawidowicz, 1993) or may change their body size and shape (Dodson & Havel, 1988; Dodson, 1989), in an attempt to avoid a predator attack. They may also change life history patterns, i.e. depending on the dominating pressures, animals may delay or accelerate maturity, mature at a smaller or larger size, release less but larger, or more but smaller neonates (Macha´cˇek, 1991; Stibor, 1992; Riessen, 1993; Weider & Pijanowska, 1993; Sakwin´ska, 2002). These antipredator defenses are costly and the scale of defense should be adjusted to predation risk, to avoid the unnecessary costs of permanent defense. Therefore, the time needed to display various defensive mechanisms may differ, from seconds to the display of a behavioral reaction following a sudden change in light intensity or water move-

ment, to more than one generation needed to display changes in morphology (Agraval et al., 1999) or life history traits (e.g. producing ephippial eggs, Alekseev & Lampert, 2001). The time between initiation of the defense machinery and the moment when these changes become adaptive is crucial for equating the real costs of defense. When this period is extended, the probability of the disappearance of the factor inducing the defensive mechanism is relatively high and, as a consequence, the probability of bearing costs and taking no advantage from defense is also high. On the other hand, when the adaptive features are determined in different ontogenetic stages, and environmental conditions change during ontogenesis, some components of life strategy may become maladaptive, or an individual may be forced to adjust parameters determined later to these determined earlier in ontogenesis. The aim of our study was to determine how the response of Daphnia females exposed to the

220 presence of fish differs in different stages of their ontogenesis. Timing of adaptive phenotypic changes in the life history of Daphnia exposed to fish presence and the length of reaction time needed to display these changes can thus be determined. Additionally, it will become clear whether females can remember information on predator presence, or the changes occur when the proximal factor is acting directly during physiologically determined moments when undertaking decisions on further development.

Materials and methods A clone of Daphnia magna Straus originating from Lake Binnensee (where Daphnia coexist with fish) was used. Females were cultured individually in glass jars in synthetic medium ADAM (Klu¨ttgen et al., 1994) and fed the green algae Scenedesmus acutus in a concentration equal to 1 mg Corg Æ l)1. Medium with algae was changed daily. Presence of fish was simulated by exposing Daphnia to water containing fish kairomone from crucian carp (Carassius carassius – one fish/7 l/24 h), fed 50 Daphnia per day. Neonates from the third clutch of third generation (great-grand daughters of the single founder female) were split into six groups (10 individuals in each). Females from the first group were cultured in ‘fish water’ from birth to 1st post-embryonic exuvium (for the duration of the first instar), then transferred to control water. Females from second group were exposed to fish kairomone for second instar, from third group – in third instar, etc. Females from the sixth group (control) were not exposed to fish kairomone. Age at release of eggs from the ovaries to the brood chamber (AFO) and age at first reproduction (AFR, i.e. age at releasing the first-clutch of offspring) were recorded with 10 min. accuracy. Size at first reproduction (SFR, i.e. size after releasing the first clutch eggs to the brood chamber) and the size of neonates were measured with 10 lm accuracy. Neonates from the first clutch were counted, dried and weighted; second clutch eggs were counted. The weight of adult females was calculated using model obtained for the same clone of Daphnia: W ¼ expð
4:1291 þ ð1:8963  lnðLÞÞÞ;

where W is weight (lg) and L is length of an animal (mm). The influence of fish kairomone on the life-history traits of Daphnia was tested using a Kruskal– Wallis non-parametrical ANOVA. The differences between means were tested using a t-test for ranks. Reproductive effort (RE) was calculated as a proportion of weight of the first clutch to the total weight of female at first reproduction and the first clutch eggs: RE ¼ ðWc =Wc þ Wf Þ  100%; where RE is reproductive effort, Wc – dry weight of whole 1st clutch, Wf – dry weight of female at first reproduction. Correlation of certain life-history traits was tested using the product-moment (Pearson’s) correlation coefficient (Sokal & Rolf, 1981).

Results Daphnia exposed to fish kairomone during the third instar released their first clutch of eggs from the ovaries to the brood chamber (Fig. 1A, Table 1), and released their first offspring (Fig. 1B, Table 1) earlier than their sisters that had not been exposed to this factor, or exposed to this factor in other instars. Time of carrying their first eggs was significantly shorter (Fig. 1C, Table1), and they were smaller at first reproduction than other females (Fig. 1D, Table 1). All females exposed to fish kairomone in the third instar had four juvenile instars (Fig. 1E), whereas control females as well as those exposed to the kairomone in the first instar had five juvenile instars. Females from other treatments had either four or five juvenile instars. Daphnia in fish treatments released, on average, significantly fewer first-clutch offspring (Fig. 1F, Table 1) and, as a consequence, the total mass of their first clutch was lower (Fig. 1G, Table 1), despite the fact that the mass of a single neonate did not differ from that in the control treatment (Fig. 1H, Table 1). Daphnia exposed to fish kairomone in first and second instar exhibited a significantly lower reproductive effort than control females (Fig. 1I, Table 1). The number of secondclutch eggs of females exposed to fish kairomone at the third instar was smaller than in Daphnia

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Figure 1. Age at maturity – AFO (A), age at first reproduction – AFR (B), time of carrying eggs in brood chamber – THE (C), size at first reproduction – SFR (D), number of juvenile instars (E), number of first-clutch offspring (F) dry mass of 1st clutch offspring (G), dry mass of single neonate (H), reproductive effort RE – ratio of first clutch weight to total weight of egg-carrying female together with first clutch eggs in brood chamber (I) and number of second-clutch offspring (J) of Daphnia exposed to fish kairomone in first, second, third, fourth and fifth instars (dark bars), and not exposed to this factor (light bar); means ± 1 SD; ‘‘’’ – significant differences from control treatment (test t for ranks, p < 0.05).

cultured in other fish treatments and in fish-free environment (Fig. 1J). Variability of life history traits (measured as coefficients of variation CV ¼ s/x, where s is and x is mean) in females

exposed to fish kairomone in first and third instars, especially age and size at first reproduction and the number of juvenile stages, was significantly lower than in remaining treatments (Fig. 2).

222 Table 1. Kruskal–Wallis test for differences in life history parameters between Daphnia not exposed and exposed to fish kairomones in various instars; significant differences shown with bold font Df

N

H

AFO

5

55

24.1824

0.0002

AFR Time of holding eggs in brood chamber

5 5

55 55

22.5085 12.0583

0.0004 0.0340

p

SFR

5

55

24.9188

0.0001

Number of juvenile instars

5

55

29.7468