Journal of Plankton Research Vol.15 no.4 pp.403-412, 1993

Resource quality effects on Daphnia longispina offspring fitness

Michael T.Brett Division of Environmental Studies, University of California, Davis, CA 95616, USA Downloaded from https://academic.oup.com/plankt/article/15/4/403/1442975 by guest on 29 September 2021

Abstract. The present study addressed the question: is the fitness of Daphnia longispina neonates related to the quality (species) of the resource their mothers consumed? A 2 x 2 factorial design with two maternal and neonate resource types was employed, with Rhodomonas and Microcystis used as high- and low-quality resources, respectively. Neonate fitness was assessed using demo- graphic parameters obtained from a life-table study. The resource type neonates consumed always had a stronger effect on the neonates than did the maternal type. Neonate consumption of Rhodomonas, relative to Microcystis, increased fitness, as estimated by the instantaneous population growth rate, by 25-28%, while maternal consumption of Rhodomonas increased fitness by 6—8%. Neonate Rhodomonas consumption also reduced the age at reaching the primiparous instar; increased brood size at the primiparous instar and body length immediately after the primiparous instar; increases average clutch size, number of clutches produced, total egg production, and mean body length up to and on age 30 days. Regardless of resource type, maternal Rhodomonas consumption resulted in neonates which reached maturity at an earlier age and had a larger individual size immediately after reaching maturity. The mean clutch size, total egg production, and length up to and at age 30 days were all significantly affected by maternal diet when neonates consumed Microcystis; however, these variables were not influenced by maternal type when neonates consumed Rhodomonas. This is the first study to document maternally mediated effects of resource quality on the fitness of crustacean zooplankton neonates.

Introduction The term pre-natal maternal effects is generally used to describe non-genetic influences on neonate fitness. These effects are often environmental in origin and are physiologically mediated. For freshwater crustacean zooplankters, the quantity and quality (algal species and culturing media) of resources consumed by the mother have been shown to affect neonate tolerance to starvation (Tessier et al., 1983; Cowgill et al., 1984). The quantity of resources consumed by the mother has been shown to be positively related to daphnid neonate mass in some studies (Lynch and Ennis, 1983; Tessier and Consolatti, 1991) and negatively related to copepod egg mass in other studies (Cooney and Gehrs, 1980; Jamieson and Burns, 1988). A potential mechanism for these maternal effects is thought to be maternal investment in egg lipid content (Tessier et al., 1983; Cowgill et al., 1984; Goulden et al., 1987). Although the species composition of the phytoplankton is known to be as dynamic as is the biomass, and different algal species are known to promote vastly different population growth rates for crustacean zooplankton (Infante and Litt, 1985; Lundstedt and Brett, 1991), resource quality influences, mediated through maternal con- sumption, on neonate growth and reproductive success have not been previously documented. The present study tested the hypothesis that resource quality affects the reproductive success of a female. This was done using a life-table design, which © Oxford University Press 403 M.T.Brett made it possible to assess the responses of a wide range of demographic parameters to the treatments. This study also tested the hypothesis that neonates produced by females consuming high-quality resources are of higher fitness than those produced by females consuming low-quality resources. Past research on maternal effects on neonate characteristics has focused primarily on neonate starvation tolerance in response to the quantity of food consumed by the

mother. Since the quality of food in takes is often as dynamic as is the quantity of Downloaded from https://academic.oup.com/plankt/article/15/4/403/1442975 by guest on 29 September 2021 food, I chose to test what effects maternal food quality might have on neonate fitness. It is suggested that maternal resource consumption may help ameliorate neonate resource stress caused by exclusive consumption of low-quality resources. To test these hypotheses, the cladoceran Daphnia longispina was used. Daphnia represent a key group within limnetic environments in that they are known to be dominant herbivores, but are at the same time very sensitive to predation from vertebrate planktivores. A 2 x 2 factorial with two maternal and neonate resource types and a life-table experimental design was employed. The variable used to assess individual fitness was the Malthusian parameter (r), also known as the instantaneous rate of population growth. In addition, age at reaching the primiparous instar, egg production during the primiparous instar, and body length immediately after the primiparous instar; and average clutch size, number of clutches produced, total egg production, mean body length, and survival rate up to and on age 30 days were assessed. Previous studies have used starvation tolerance and size as measures of neonate quality. Tolerance of starvation is a very relevant ecological parameter (Gliwicz, 1990), but I chose to examine the fitness of the neonates independent of resource limitation because in natural ecosystems shifts in resource type are often as pronounced and occur as rapidly as do shifts in total resource availability (Sommer et al., 1986). Furthermore, dramatic shifts in individual fecundity are commonly noted in the absence of major shifts in total algal biomass, suggesting the importance of qualitative shifts in the algal community (Threlkeld, 1985). The algae used in this experiment (Rhodomonas and Microcystis) represent common species in meso- to eutrophic temperate lakes. These algae were found to be the best and the worst, respectively, of six common algae tested in bioassays, in terms of promoting population growth of the common cladocerans D.longispina, Eubosmina longispina and Chydorus sphaericus (Lundstedt and Brett, 1991). These algae also represent extremes of common algae in terms of total lipid and fatty acid content, with Rhodomonas having much higher concentrations (Ahlgren etal., 1990; G.Ahlgren, unpublished data). Arts et al. (1992) suggested that shifts between cryptophyta and cyanobacteria were in large part responsible for seasonal patterns in nutrition, lipid deposition and reproduction for crustacean zooplankton. Although cyanobacteria are known to resist grazing by forming large colonies, clogging the filtering apparatus of zooplankton with filaments, or secreting toxins (Lampert, 1987), the strain of Microcystis used in the present experiment was single celled and apparently non- toxic. The presumption of non-toxicity is supported by previous bioassays in which both D.longispina and C.sphaericus achieved positive growth in this strain of Microcystis (Lundstedt and Brett, 1991). 404 Resource quality effects on D.longispina offspring

Method

The 2x2 factorial design of this life table resulted in the following treatments: (1) maternal and neonate Microcystis; (2) maternal Rhodomonas and neonate Microcystis; (3) maternal Microcystis and neonate Rhodomonas; (4) maternal and neonate Rhodomonas. Comparisons of treatment 1 with 3, and of treatment

2 with 4, were used to measure the influence of resource consumption by Downloaded from https://academic.oup.com/plankt/article/15/4/403/1442975 by guest on 29 September 2021 neonates on the results obtained and will hereafter be referred to as resource effects. Comparisons of treatments 1 with 2, and of 3 with 4, were used to measure maternal influences due to resource consumption on the quality of the neonates. These comparisions will hereafter be referred to as maternal effects in neonate Microcystis and maternal effects in neonate Rhodomonas, respectively. The clone of D.longispina used to test the proposed hypotheses was isolated from Lake Vallentuna, central Sweden, in April 1988, a year before the present experiment was carried out. During the period between isolation and execution of the experiment, this clone was maintained on a mixture of Rhodomonas minuta and Scenedcsmus acutus at a temperature of 15°C and a 14L:10D light cycle. During the initial phase of the experiment, a stock culture of Daphnia, >1000 individuals, was split into two equal parts with one given Rhodomonas minuta and the other Microcystis aeruginosa during a period of 10 days. This period is 1.5 times the period from the initiation of ovarian development to release of neonates from the brood pouch at the experimental temperature (the egg development time was 3.1 ± 0.1 days, ±1 SD), so one could be certain that the neonates collected at the end of this interval were a product of the test resources. During this period fresh algae were supplied to the populations daily in overabundance, >2 jxg C ml"1. After the initial 10 day period, 100 neonates (<12 h old) were isolated from both maternal resource types. Each group of 100 neonates was randomly divided into two groups of 50 individuals, with each individual maintained in its own 50 ml beaker, and given either Rhodomonas or Microcystis as a test resource. During this phase of the experiment, zooplankters were transferred to new beakers with fresh algae, ~2 u,g C ml"1, at 3 day intervals. The algal concentrations employed were —10 times higher than the threshold for maximum population growth (Gliwicz, 1990) and were therefore adequate to assure that all responses noted were for resource quality as opposed to quantity. All beakers were checked daily for new neonates or obviously high or low algal concentrations. The zooplankters were transferred to fresh algae at intervals <3 days. The algae were cultured using the synthetic medium L16 (Lindstrom, 1984), modified with B vitamins and earth extract. This medium has an ionic composition similar to that of Lake Erken, a mesotrophic lake in central Sweden. Only algal cultures in the exponential growth phase were used. The strain of Microcystis used remained in suspension during the experiments. The biomass of the algal cultures was routinely estimated using fluorescence and previously calibrated standard curves (R2 > 0.98 for both algae). As the length of egg development was 3 days, new neonates were generally observed at this interval, at which time they were enumerated and removed. Although the initial number of observations for each treatment was 50, the 405 M.T.Brett realized sample sizes were smaller: 41-48 individuals, due to inclusion of males, lost samples (dropped or crushed) and mortality. The full contingent of samples was observed until the primiparous instar, after which 25 individuals from each treatment were randomly selected for continued observation until day 30. This was done because the sample size was larger than needed, as determined by initial standard error values, and because this experiment was very labor

intensive. Those individuals not selected for continued observation were Downloaded from https://academic.oup.com/plankt/article/15/4/403/1442975 by guest on 29 September 2021 measured for total length at an age of 12 days, during their second adult instar. These experiments were carried out at 18.6 ± 0.5°C with a 14L:10D light cycle in a temperature-controlled room during the spring of 1989. The Malthusian parameter (r) was calculated using the Euler equation according to Lotka (Krebs, 1985). Variance about these estimates was calculated using a jackknife procedure (Meyer et al., 1986). Although the life tables obtained in the present study are truncated, i.e. they do not follow individuals until their deaths, this had virtually no effect on the estimates of r. This can be shown by comparing estimates of r using the full 30 days of data with estimates of r using only the first 25 days of data. In no case did eliminating the last 5 days cause a >0.5% change in the estimate of r. The data were initially analyzed using a two-factor ANOVA. The resource term of the ANOVA was presented to show resource effects on the demographic parameters. Owing to severe inequities in variance between the treatments (see Tables I and II), the maternal and interaction terms of the ANOVA were disregarded, and the effects of maternal resource consumption in both neonate resource types were tested using individual Mests. This analysis is in accordance with the recommendations of Day and Quinn (1989), who suggested f-tests for planned comparisons when variances were unequal for ANOVA-type matrices. In practical terms, the statistical approach had no effect on the results presented in Table I; i.e. regardless of whether I used the full results of the two-factor ANOVA or used the resource term from the ANOVA plus separate Mests for the maternal effects, I found significant resource and maternal effects. The results presented in Table II were, however, influenced by my method of analysis. This was because the maternal effect was sufficiently small and the inequities in variance were sufficiently large as to preclude declaring significant effects when a simple examination of the data suggested that there was in fact an effect of maternal type on mean clutch size, total egg production and size at age 30 days when the resource type was the low-quality Microcystis. Since variances were similar for treatments with the same neonate resource, maternal effects were tested using separate /-tests for each neonate resource. The P values of these Mests were adjusted using the Bonferroni correction for multiple comparisons. Survival until day 30 was analyzed by comparing binomial distributions (Box et al., 1978).

Results and discussion The results of the present study show that the algal species consumed by a neonate, Rhodomonas or Microcystis, strongly influenced all of the demo-

406 Table I. The results of the life-table experiment: initial results and the population growth rate. All values presented are the mean ± 1 SD. The resource effect was tested with a two-factor ANOVA and the maternal effects were tested using two-tailed (-tests

Treatment Matcmal neonate Malthusian parameter Age at maturity Clutch size at maturity Length at age 12 days (r) (days) (m)

Microcyslis Microcyslis 0.217 ± 0.014 25 7.0 ± 0.52 3.8 ± 0.57 47 1600 ± 86 22 Rhodomonas Microcyslis 0.234 ± 0.014 24 6.8 ± 0.40 4.4 ± 0.81 48 1650 ± 79 22 Microcys(is Rhodomonas 0.277 ± 0.031 25 6.3 ± 0.26 4.6 ± 1.31 47 1780 ± 103 22 Rhodomonas Rhodomonas 0.293 ± 0.032 24 5.9 ± 0.23 5.0 ± 1 63 41 1880 ± 157 15

Significance (P) .o Resource effect 0.0001 0.0001 0.0001 0.0001 Maternal effect I versus 2 neonate Microcyslis 0.0001 0.05 0.0001 0.02 Maternal effect 3 versus 4 neonule Rhodomoiuis 0.05 0.0001 NS 0.002

NS, not significant 5- I.

I Downloaded from https://academic.oup.com/plankt/article/15/4/403/1442975 by guest on 29 September 2021 September 29 on guest by https://academic.oup.com/plankt/article/15/4/403/1442975 from Downloaded 05 3

Table II. The results of the life-table experiment: mean results at age 30 days. All values presented are the mean ±1 SD. The resource effect was tested with a two-factor ANOVA and the maternal effects were tested using two-tailed (-tests. Survival until age 30 days was tested for differences in binomial distribution

Treatment Maternal neonate Mean clutch size Number of clutches Total egg production Length at age 30 days n Survival until age 30 days (%)

1 Microcystis Microcystis 6.2 ± 1.2 6.0 ±0 37 ± 7.0 1800 ± 34 22 84 ± 7.3 2 Rhodomonas Microcystis 6.9 ± 0.48 6.0 ± 0 41 ± 2.9 1850 ± 40 22 86 ± 7.1 3 Microcystis. Rhodomonas 17 ± 3.1 7.0 ± 0.2 120 ± 22 2340 ± 97 21 79 ± 8.1 4 Rhodomonas Rhodomonas 17 ± 3.7 7.0 ± 0 120 ± 26 2360 ± 106 20 69 ± 9.4

Significance (P) Resource effect 0.0001 0.0001 0.0001 0.0001 0.05 Maternal effect 1 versus 2 neonate Microcysth 0.02 NS 0.02 0.001 NS Maternal effect 3 versus 4 neonate Rhodomonas NS NS NS NS NS

NS, not significant. Downloaded from https://academic.oup.com/plankt/article/15/4/403/1442975 by guest on 29 September 2021 September 29 on guest by https://academic.oup.com/plankt/article/15/4/403/1442975 from Downloaded Resource quality effects on D.longispina offspring graphic parameters measured (Tables I and II). Rhodomonas produced a higher rate of population growth; an earlier age and larger clutch size at maturity, and a larger individual size immediately after the primiparous instar; and a larger average clutch size, number of clutches, total egg production, and individual size up to and on age 30 days. The only parameter which showed a higher value for Microcystis was survival to age 30 days. A comparison of fitness (as determined by the population rate of growth, which includes components of age at maturity, Downloaded from https://academic.oup.com/plankt/article/15/4/403/1442975 by guest on 29 September 2021 fecundity and mortality) across treatments shows that neonate consumption of Rhodomonas, relative to Microcystis, increased fitness 25-28%, while maternal consumption of Rhodomonas increased fitness by 6-8%. Thus, the present results clearly show that neonate resource consumption is more important than maternal resource consumption, as is logically expected. However, the effect of maternal resource consumption is large relatively speaking, i.e. ~26% of the neonate resource effect. Regardless of neonate resource, maternal consumption of Rhodomonas produced a greater population growth rate, a reduced age at maturity and an increased size immediately after the primiparous instar (Table I). When the neonate resource was Microcystis, effects of maternal algal consumption were persistent, i.e. they affected aggregate parameters represent- ing the first 30 days. Those neonates which were produced by mothers consuming Rhodomonas had a larger average clutch size and total egg production over 30 days, and a larger individual size at 30 days (Table II). Relative to the maternal effects for neonates consuming Microcystis, however, the maternal effects on neonates consuming Rhodomonas were transitory, and did not influence average clutch size, total egg production, and individual size up to and on age 30 days. This suggests that maternal influences on neonate fitness may partially compensate for environmental stress in the form of algal communities composed of nutritionally poor species, while maternal influences will have a lesser effect when the ambient resource base is of high nutritional quality. Adult daphnids consuming Rhodomonas produced both more neonates and neonates of higher fitness. The present study is the first to show maternally mediated resource quality influences on zooplankton neonate fitness. To the extent that these results are representative of other crustacean zooplankters, the results suggest a strong driving force behind strategies optimizing the intake of high-quality resources. This should have a strong influence on interspecific competition independent of interspecies differences in feeding mode, resource optima, susceptibility to interference from filamentous algae, tolerance of starvation, predator evasiveness and temperature optima. Those zooplankton species most effective in obtaining high-quality resources will produce more offspring and offspring of higher fitness. Crustacean zooplankton species are known to differ markedly in their ability to preferentially select specific algae. All species are assumed to select algae based on size, although selection efficiencies vary between species and life stages (Burns, 1968; Gliwicz, 1977; Vanderploeg and Paffenhofer, 1985). Some groups such as Daphnia are thought to rely exclusively on size selection, while several 409 M.T.Brett copepods have been shown to select particles based on taste or some other chemical clue and are able to distinguish between particles of virtually identical size and shape (DeMott, 1986, 1989; Butler ctal., 1989). Phytoplankton species tend to stratify vertically to optimize temperature, light intensity and nutrient availability. Zooplankton species are known to differ in their patterns of vertical distribution and migration (Stich, 1989). In addition to avoiding visually

oriented predators (Gliwicz, 1986; Gabriel and Thomas, 1988), zooplankton Downloaded from https://academic.oup.com/plankt/article/15/4/403/1442975 by guest on 29 September 2021 may use vertical migration to detect patches of high-quality algae (Johnsen and Jakobsen, 1987; Leibold, 1990). The present results suggest a mechanism by which more highly discriminating zooplankton can gain a competitive advantage over less selective species, particularly when resources of varying quality are present simultaneously. The particular strategy of discrimination would prob- ably depend on the zooplankton group. For instance groups such as calanoid and cyclopoid copepods and Bosmina are effective preferential selectors, while Daphnia would be forced to rely on vertical migration to optimize their intake of high-quality resources. To the extent that genotypes differ in their ability to maximize their intake of high-quality resources, the present study suggests a mechanism for interspecific competition and ultimately evolutionary change within species. No study of crustacean zooplankton, however, has documented genotype, or even indi- vidual, differences in neonate fitness mediated by maternal influences. Exper- iments have only documented environmentally induced, i.e. phenotypic, maternal influences on neonate fitness (Tessier et al., 1983; Cowgill etal., 1984; the present study). Changes in resource quality, i.e. species succession, exert strong influences on demographic parameters of freshwater zooplankton (Lundstedt and Brett, 1991). These changes can be very pronounced and occur very rapidly, and together with selective predation, temperature changes and cycles in total algal availability, constitute one of the major determinants of zooplankton inter- and intraspecific competitive interactions. The present results show that by consum- ing high-quality resources Daphnia are able to produce both more offspring and offspring of higher fitness. When the ambient resource base was high quality, maternal effects on neonate fitness were transitory. However, when the resource base was low quality, maternal effects were persistent. In that crustacean zooplankton are known to have different feeding modes, with some species highly selective, the present results suggest a mechanism whereby highly selective species would gain a strong competitive advantage when the ambient algal community is composed of both high- and low-quality species. For instance a highly selective species such as Bosmina could maintain a relatively high rate of egg production and produce high-quality eggs even when the majority of the phytoplankton is of low quality. A higher output of better eggs could also drive behavioral strategies, such as vertical migration, for optimizing grazing on high- quality algal patches. During times when the algal resource base exerts a strong influence on population dynamics, clonal differences in the ability to optimize uptake of high-quality resources may drive species evolution and particularly genotype succession. 410 Resource quality effects on D.longispina offspring

Acknowledgements I thank J.Bengtsson, B.Pejler, L.Bern, S.Schoenberg and W.Lampert for valuable comments to this manuscript. Ann-Sofie Lundback and Lisa Lundstedt provided valuable assistance in the laboratory. I also thank Kare Lindstrom who taught me the art of culturing microorganisms. Downloaded from https://academic.oup.com/plankt/article/15/4/403/1442975 by guest on 29 September 2021 References

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Received on September 22, 1992; accepted on December 12, 1992

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