The dynamics of Ceriodaphnia pulchella (Cladocera) in laboratory

Acta Oecologica 24 (2003) S245–S249 www.elsevier.com/locate/actoec

Original article

The dynamics of Ceriodaphnia pulchella (Cladocera) in laboratory Nelson Abrantes *, Fernando Gonçalves Departamento de Biologia, Universidade de Aveiro, 3810-193 Aveiro, Portugal

Abstract Effects of different food sources on selected life-history traits of Ceriodaphnia pulchella were studied under controlled conditions. Animals were submitted to five treatments: artificial medium (ASTM hard water) supplied with microalgae (Selenastrum capricornutum) as food; lake water filtered through 50 µm mesh size with and without food; lake water filtered through glass fibre filters with and without food. Reproduction and growth parameters of individual animals were assessed at 1 d interval. Organisms tested on 50 µm mesh size filtered treatment with food showed the highest values for all parameters. The presence of competitors, namely rotifers, in lake water, and the water quality did not seem to play a role on the life-history traits of C. pulchella. The survival of organisms cultured on the glass fibre filtered lake water, without microalgae supply, showed that C. pulchella feeds solely on bacteria and small particles. However, in this treatment, the availability of food seems to affect negatively reproduction in favour of growth. Food supply seems to be the main factor affecting C. pulchella dynamics under controlled conditions. © 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Population dynamics; Cladocera; Ceriodaphnia pulchella; Life-history traits

1. Introduction Zooplankton is considered an important compartment of aquatic ecosystems for its role in the trophic chain. It represents the channel of transmission of the energy flux from the primary producers to the top consumers. Therefore, it is of great interest to study mechanisms affecting its size structure, reproduction and survivorship. The most important environmental factors controlling zooplankton growth and reproduction are temperature, food quantity and quality (Vijverberg, 1989) and predation (Gliwicz and Pijanowska, 1989). In natural systems, however, it is difficult to disentangle the role of food and predation, because of the complexities in assessing the effects of these factors separately (Boersma and Vijverberg, 1994). Cladocerans are a key group in the food webs of lakes, mainly due to their ability to filter particles ranging in size from bacteria (Brendelberger, 1991; Hessen and Andersen, 1990) to larger algae (De Bernardi et al., 1990; Infante and Litt, 1985). This implies that these animals are faced with a large spectrum of resources of varying quality. Hence the capacity for food selection is limited; food quality and quantity seems to be an important factor influencing life-history parameters of cladoceran * Corresponding author. E-mail address: [email protected] (N. Abrantes). © 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. DOI: 1 0 . 1 0 1 6 / S 1 1 4 6 - 6 0 9 X ( 0 3 ) 0 0 0 2 0 - 1

populations. It is known that food conditions influence fecundity and some studies have showed that the quantity of food can be directly related to the number of eggs produced per female (Lampert, 1978; Müller-Navarra and Lampert, 1996). In the Vela Lake (Figueira da Foz, Portugal), a variety of cladoceran species usually coexist, ranging from large Daphnia to the smaller Ceriodaphnia and Bosmina (Rodrigues et al., 1993). However, these species showed a spatial or temporal separation of abundance peaks (Barros, 1994), supporting the argument that competition is another important factor in structuring zooplanktonic communities (Makarewicz and Likens, 1975). The effects of food on the dynamics of herbivorous zooplankton species have been a well-researched field. However, most studies have focused on Daphnia species, and few studies have appeared on dynamics of smaller Cladocera [e.g. (Balseiro et al., 1992; Boersma and Vijverberg, 1996; Vijverberg and Boersma, 1997)]. Little is known about dynamics and life-history of Ceriodaphnia pulchella (Boersma and Vijverberg, 1996), which represents an important element of zooplankton community in temperate lakes. Therefore, we evaluate the life-history traits responses of C. pulchella in laboratory at different conditions of food, using longevity, age and size at first reproduction, clutch size and body length as endpoints.

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2. Materials and methods C. pulchella individuals were collected in the Vela Lake and were submitted to five different treatments: ASTM hard water (ASTM, 1980) with Selenastrum capricornutum (ASEL); lake water filtered on GF/C glass fibre filters (Whatman) with and without S. capricornutum (GFFSEL and GFF, respectively) and 50 µm mesh filtered lake water with and without S. capricornutum (N50SEL and N50, respectively). Ten replicates were used for each treatment, and animals were placed individually in 50-ml test vials at a temperature of 20 ± 1 °C, with a light:dark regime of 16:8 h. S. capricornutum cells were supplied daily to attain a final concentration of 15×104 cells ml–1. The animals were transferred daily to clean vials with fresh medium. As soon as the field-caught animals produced newborn, the mothers were removed and this first generation was used for our study that was completed when these individuals died. Body length (mm; measured from just above the eye to the base of the tail spine), age (d) and length (mm) at first reproduction and clutch size (eggs number) were daily recorded, during the time of experience. Newborns were removed from the vials. The population growth rate was determined by the first three clutches (Porter et al., 1983; Vanni and Lampert, 1992) and the rate of increase (r) was estimated using the Euler equation: n

兺e

x=0

− rx

lx.mx = 1,

where r is the intrinsic rate of increase (d–1), x is the age class (0... n ), lx is the probability of surviving to age x, and mx is the fecundity at age x. Standard errors for r were computed using a jackknifing method (Meyer et al., 1986). The differences among five treatments were analysed with one way ANOVA followed by the Tukey multiple comparison test (Zar, 1984).

3. Results Growth and reproduction of C. pulchella were significantly affected by different treatment conditions (Table 1). Estimated growth rate (r) was higher for animals raised in N50Sel and N50 treatments. (Fig. 1), in contrast to animals kept in the ASEL medium, which showed the lowest r-value (0.191 d–1). In all treatments, mean clutch size increases at the beginning, but decreases with time. The highest value of mean clutch size was found in N50 (8.8 eggs per female)

Fig. 1. Population growth rates (r, d–1) of Ceriodaphnia pulchella reared on five treatments: ASEL, GFFSEL, GFF, N50SEL, and N50. The error bars give the S.E.

(Fig. 2). Animals reared on ASEL grew more slowly and were smaller than those reared in other treatments (Fig. 3). The maximum body length recorded was found in N50Sel and N50 (0.85 mm). After 5 d, C. pulchella in N50SEL and N50 treatment produced the first neonates (Fig. 4). In GFFSEL and GFF, on average, the first reproduction occurred 2 d later. In the ASEL treatment, animals delayed to reach the first reproduction and showed the smallest size at first reproduction (Fig. 5). The highest mean longevity (44.56 d) was recorded in N50SEL (Fig. 4). There was a good correlation between clutch size and body length (r2 = 0.9964) of C. pulchella reared in N50SEL (Fig. 6). During the study, the presence of males was not registered.

4. Discussion Our results show that both growth and reproduction of C. pulchella were influenced by the quantity and the quality of food available. The organisms differed in their growth and reproductive performance on ASEL and other treatments. N50SEL and N50 treatments proved to be a good medium with r-values ranging between 0.411 and 0.426 d–1, respectively. These organisms with higher r also grew faster during the experimental period and were thus characterised by their large size at first reproduction. Size at first reproduction may be adjusted by daphnids phenotypically either in response to chemical kairomones released by fish (Machácek, 1991; Sakwinska, 1998; Stibor, 1992), or as a demographic effect combined with shifts in relative abundance of small firstbrood eggs, which hatch to smaller neonates, maturing at a smaller size (Lampert, 1993). In our experience, animals in

Table 1 One way ANOVA followed by Tukey’s test to compare treatments Parameter

P

Body length Clutch size Longevity Age at first reproduction Size at first reproduction

≤0.001 ≤0.001 0.016 ≤0.001 ≤0.001

Treatment (Tukey’s test) ASEL GFFSEL a a a b a a a a a b

GFF b c a a b

N50SEL b c a b b

N50 b c b b b

N. Abrantes, F. Gonçalves / Acta Oecologica 24 (2003) S245–S249

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Fig. 2. Mean clutch size (number of eggs) of 10 Ceriodaphnia pulchella replicates from five treatments: ASEL, GFFSEL, GFF, N50SEL, and N50. The error bars give the S.E.

Fig. 3. Mean body length (mm) of 10 Ceriodaphnia pulchella replicates from five treatments: ASEL, GFFSEL, GFF, N50SEL, and N50. The error bars give the S.E.

Fig. 4. Mean age at maturity (d) and longevity (d) Ceriodaphnia pulchella replicates from five treatments: ASEL, GFFSEL, GFF, N50SEL and N50. The error bars give the S.E.

Fig. 5. Mean size at maturity of 10 Ceriodaphnia pulchella replicates from five treatments: ASEL, GFFSEL, GFF, N50SEL and N50. The error bars give the S.E.

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Fig. 6. Relation between body length (mm) and clutch size (number of eggs) of Ceriodaphnia pulchella at the first three clutches for the five tested mediums: ASEL (r2 = 0.6266); GFFSEL (r2 = 0.793); GFF ( r2 = 0.9544); N50SEL (r2 = 0.9964) and N50 (r2 = 0.9845).

ASEL showed the lowest size at first reproduction, which were controlled by food quality and not by predation, as predators were non-existent. On the other hand, the brood chamber of large individuals is also larger, enabling the production of large numbers of eggs. Animals in ASEL medium matured more slowly and at a smaller size. Smaller size at first reproduction may be advantageous for C. pulchella when fish predation prevails, but disadvantageous when invertebrate predators are dominant (Zaret, 1980). The presence of competitors, namely rotifers, and the chemical quality of lake water, in N50SEL and N50, did not affect the dynamics of C. pulchella. Thus, the diversity of food types present in these treatments may be the main factor responsible for the significant differences observed in all the treatments (Table 1). The organism’s survival in the GFF treatment confirms that C. pulchella feeds solely on bacteria and small particles. According to Threlkeld (1987), when food is limited, the allocation of energy (e.g. reproduction, growth, maintenance) changes with time. Initially, C. pulchella allocated higher percentage of energy for growth in N50 and N50SEL than in other treatments. Thus, in GFF, the quantity of food affects negatively reproduction in favour of growth. This study indicates that under the culture conditions used in our experiments, S. capricornutum is a poor quality food for C. pulchella. However, the chemical composition of the standard medium, ASEL, also seems to be inadequate for cultivating this cladocera. The absence of males during the period of experience, suggests that food is not the main factor inducing those changes, that might arise from other factors (e.g. temperature, predation or competition). Growth rate values of C. pulchella in N50SEL and N50 were very high when compared with field studies (Boersma and Vijverberg, 1996), where r does not exceed 0.2 d–1. This suggests that r can be biomanipulated by the control of factors, namely predation. In conclusion, food quantity and

quality were the main factors affecting C. pulchella dynamics at controlled temperature and absence of predators.

Acknowledgements We are grateful to Abel Ferreira, Catarina Marques and other colleagues for laboratory assistance. Nelson Abrantes was supported by a grant from the Aveiro University.

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