Effect of body size and temperature on generation time in zooplankton
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1 Journal of Plankton Research Vol.22 no.2 pp , 2000 Effect of body size and temperature on generation time in zooplankton James F.Gillooly Department of Zoology, 430 Lincoln Drive, University of Wisconsin, Madison, WI 53706, USA Abstract. The relationships of generation time to both adult body mass and temperature are critical to our understanding of numerous aspects of zooplankton behavior, ecology and evolution, yet these relationships remain poorly understood. Here, I use a meta-analysis to define the relationship of generation time to body mass and temperature for both marine and freshwater zooplankton species (rotifers, copepods and cladocera), for temperatures from 5 20 C. I also define a relationship for the constituent parts of generation time (embryonic and postembryonic development time) as a function of egg and body mass for zooplankton across this temperature range. These relationships provide powerful tools for evaluating differences in generation time between individual zooplankton species. Introduction Generation time is the single most important determinant of the rate of population growth in species (Cole, 1954) and thus, differences in generation time affect numerous ecological processes, including intra- and interspecific interactions (e.g. competition, predation). Differences in generation time (time from egg to maturity) among species are sometimes attributed to differences in body mass, as generation time has been shown to scale positively to body mass for diverse assortments of plants and animals (Yarwood, 1956; Blueweiss et al., 1978), and within taxonomic groups of endotherms [e.g. (Taylor, 1968) for birds and mammals]. However, for ectotherms, the value of body mass scaling relationships is limited because they do not account for the influence of temperature on generation time. Generation times of ectotherms are generally thought to increase with body size, but also decrease with increasing temperature for a given body size. Thus, for a scaling relationship to be useful to the study of ectotherms, it must account for the effects of both body size and temperature. The question of how generation time varies with temperature and/or body mass remains poorly understood in ectotherms. Zooplankton are an excellent group of organisms for evaluating the combined effects of body mass and temperature on generation time because they have relatively short generation times and are conducive to laboratory studies. Moreover, the manner in which generation time relates to body mass and temperature is critical to understanding the ecology, behavior and evolution of zooplankton. For example, knowledge of the relationship of generation time to body size and temperature could contribute to the understanding of zooplankton seasonal dynamics (e.g. species abundance or species interactions) because generation times of many zooplankton occur in a seasonal context. Yet, as with most ectotherms, knowledge of the effects of body mass and Oxford University Press
2 J.F.Gillooly temperature on generation time, or its constituent parts [embryonic development time (egg to hatch) and postembryonic development time (hatch to maturity)], remains sparse and disparate. Research has typically focused on a single group (i.e. rotifers, cladocerans or copepods), partially because based on the classic work of Allan, these traits have long been considered specific to each group (Allan, 1976). The lack of understanding of the relationship between generation time, body mass and temperature in zooplankton is reflected in the long-standing debate regarding the nature of the relationship, and in the numerous and diverse models formulated to predict generation time (Huntley and Lopez, 1992; Hirst and Sheader, 1997). Some investigators have concluded that generation time scales positively to body mass among certain groups [(Hirst and Sheader, 1997 ) for copepods], while others contend there is no such relationship (Kiørboe and Sabatini, 1995), and that generation time is uniquely a function a temperature (McLaren, 1978; Allan and Goulden, 1980). Yet, even the relationship of generation time with temperature is unclear as zooplankton growth rates have been found to be both dependent and independent of temperature for different groups of species (Hirst and Lampitt, 1998). In this study, I address the combined effects of body mass and temperature on generation time for all major zooplankton groups (rotifers, copepods and cladocera), both marine and freshwater species. I begin by establishing the relationship of generation time to body mass and temperature across a wide range of body sizes at each of four temperatures (5, 10, 15 and 20ºC) from data obtained from the published literature. Next, I investigate the relationship between body mass and temperature (5, 10, 15 and 20ºC) for a portion of generation time, postembryonic development time. Last, I describe the proportion of time spent in the embryonic versus postembryonic development phases of generation time as a function of relative egg size (egg mass/adult mass). Method Zooplankton generation times and postembryonic development times were obtained from published studies of individual species cultured at one or more of four constant temperatures (5, 10, 15 and 20 C) (Appendix I). In a small number of cases, development times at one or more of these four temperatures were estimated from fitted lines describing these relationships across a broader range of temperatures. Adult body mass values were obtained from synthesis papers unless these sizes were specifically noted in the studies of generation times (Appendix I). Species included in our analyses comprise a broad range of body sizes from all major zooplankton groups (cladocera: 14 spp.; cyclopoid copepods: five spp.; calanoid copepods: 17 spp.; rotifers: four spp.). In general, I consider all zooplankton species together because small sample sizes and/or a narrow range of body sizes within groups prohibit robust comparisons of generation time within or between groups. Embryonic development times and egg size data used to calculate the proportion of time spent in the embryonic versus postembryonic phase of generation time were obtained from Gillooly and Dodson (Gillooly and Dodson, 1999a). 242
3 Generation time in zooplankton Fresh egg mass values cited in Gillooly and Dodson (Gillooly and Dodson, 1999a) were converted to dry mass values using a conversion factor of 0.4 (DuMont et al., 1975; Huntley and Lopez, 1992). Relationships between any two variables in the present study were evaluated using least squares linear regression on double log-transformed data. Differences in slope and intercept between regression lines were tested using ANCOVA. When two or more lines were not significantly different (P < 0.05) in slope or intercept, data were pooled and described with a single regression line (Zar, 1996). Results Generation time Generation time (embryonic + postembryonic development time) was positively correlated (P < 0.001) to adult body mass at each of four temperatures ( r 2 = 0.83, 0.74, 0.66 and 0.77 for 5, 10, 15 and 20 C, respectively) (Figure 1, Table I). Within groups (e.g. cladocera), generation time appears to follow the same basic pattern despite limited data, with no clear differences between groups. For example, generation time was significantly positively correlated (P < 0.05) with body mass for cladocera and calanoid copepods at 5 and 10 C, and at 20 C for cladocerans only. When redefined in terms of degree days ( C d), the relationships of generation time to adult body mass did not significantly differ in slope or intercept for Fig. 1. Zooplankton generation times (d) as a function of adult body mass at 5, 10, 15 and 20 C. Data sources listed in Appendix I. 243
4 J.F.Gillooly Table I. Relationships of postembryonic development time (PEDT) and generation time (GT) to adult dry body mass (µg) for marine and freshwater zooplankton (rotifers, copepods, cladocerans). Development time is expressed in units of degree days for zooplankton cultured at four different constant temperatures. For each equation, P < Data sources are listed in Appendix I Development time Water temperature Equation n r 2 95% Confidence interval (ºC) (PEDT/GT =) Slope Intercept Low High Low High Postembryonic m Generation m Postembryonic m Generation m Postembryonic m Generation m Postembryonic m Generation m Postembryonic m Generation m
5 Generation time in zooplankton the four temperatures (P > 0.05). Generation time (GT), then, occurring over a range of temperatures (5 20 C), may be expressed with a single equation: GT = 184 (adult body mass ) 0.21, n = 111, P < , r 2 = 0.72). This expression of generation time as a function of body mass is similar to the expression of embryonic development time as a function of egg mass previously described (Gillooly and Dodson, 1999a). Postembryonic development time Postembryonic development time scales to adult body mass for zooplankton at each of four temperatures (5, 10, 15 and 20 C), much as embryonic development scales to egg mass (Gillooly and Dodson, 1999a) (Figure 2a, b). No differences between groups were distinguishable from the general pattern. Expressed as degree days ( C d), the relationships of postembryonic development time to adult body mass did not significantly differ in slope or intercept at the four temperatures (P > 0.05). Thus, postembryonic development time (PEDT) for all temperatures (5 20 C) could be expressed, as could generation time, with a single equation: PEDT ( C d) = 138 (adult mass) 0.30, n = 68, P < , r 2 = 0.84) (Table I). Embryonic versus postembryonic development time As embryonic development time scales to egg mass (Gillooly and Dodson, 1999a), and postembryonic development time scales to body mass (current study), the proportion of time spent in the embryonic versus postembryonic periods can be described as a function of relative egg size (egg mass/adult mass) Fig. 2. Zooplankton embryonic and postembryonic development time at 5, 10, 15 and 20 C as a function of dry egg and adult mass, respectively. The relationship of embryonic development time to egg mass (Fig. 2a) is used here with permission from Gillooly and Dodson (1999a). Lines are fit with power law equations (Table I). Data sources listed in Appendix I. 245
6 J.F.Gillooly (Figure 3). Simply stated, the smaller a species egg mass relative to its body mass, the smaller proportion of time spent in embryonic versus postembryonic development. The proportion of time spent in the embryonic versus postembryonic periods is positively linearly related to relative egg size at 5 (n = 13, P = , r 2 = 0.72), 10 (n = 19, P < , r 2 = 0.86), 15 (n = 19, P < , r 2 = 0.86) and 20 C (n = 15, P < , r 2 = 0.86). These four lines were homogeneous in slope and intercept (P > 0.05), indicating that the proportion of time spent in each period is constant across temperatures. At 15 C (the temperature with the most data), the linear relationship is expressed as: embryonic: postembryonic development time = 0.68 (relative egg size) 0.37, (Figure 3). The position of the zooplankton groups along this line reflects their different life histories. Rotifers spend the greatest proportion of time in embryonic development, whereas copepods spend the least amount of time in this phase. The percentage of generation time spent in embryonic development across the four temperatures ranged from 8 16% for copepods, 21 39% for cladocera and 24 44% for rotifers. Discussion Generation time and postembryonic development time The relationships of generation time and postembryonic development time to body mass presented here apply for rotifers, cyclopoid and calanoid copepods, and cladocera groups that have historically been considered distinct in numerous life history traits including generation time and postembryonic development time (Hutchinson, 1967; Allan and Goulden, 1980). Thus, while groups such as cladocera (born as miniature adults) and copepods (undergo complete metamorphosis from birth to adulthood) take very different developmental paths to Fig. 3. Proportion of time spent in embryonic versus postembryonic development as a function of relative egg size (egg mass/adult mass) for zooplankton cultured at 15 C. Data sources listed in Appendix I. 246
7 Generation time in zooplankton adulthood, generation time and postembryonic development time are still largely a function of adult body mass. The relationship of generation time or postembryonic development time with body mass may partially explain differences within or between groups previously attributed simply to species-specific traits. These relationships, then, provide a framework for evaluating species-specific differences. I speculate that the relationships of generation time or postembryonic development time with body mass and temperature have not been previously described due to the use of prohibitively small ranges of species sizes in past studies. Inclusion of temperature in the relationships of generation time and postembryonic development time to body mass permits the quantification of differences between species that may occur in natural systems with variable temperature regimes. This, in turn, provides new insights as to the importance of generation time and postembryonic development time for zooplankton ecology. For example, generation time of the cladoceran Eurycercus lamellatus is 88 days longer than the rotifer Notholca caudata at 5 C, but only 15 days longer at 20 C. The nearly 3 month difference in generation time between these large and small bodied zooplankton at 5 C is a significant advantage to the population growth of smaller bodied species in these colder waters. To the extent that generation time constrains population growth rate, this relationship also predicts a gradient of increasing zooplankton size and abundance from colder to warmer waters. Indeed, the dominance of smaller bodied zooplankton in colder waters, both seasonally in temperate lakes and in more northerly latitudes (Gillooly and Dodson, 1999b), suggests that body size and temperature do constrain generation time and subsequent population growth of larger bodied zooplankton in colder waters. Embryonic versus postembryonic development time Postembryonic development time scales to body mass in much the same way as embryonic development time scales to egg mass (Gillooly and Dodson, 1999a), yet I observed greater variability in the relationship of postembryonic development time with body mass (Figure 2a, b). The greater variability in postembryonic development time is not surprising as growth in juveniles and adults is likely influenced by many more environmental variables [e.g. food concentration (Threlkeld, 1987)] than is growth of embryos in eggs. Still, some variability may simply be explained by differences in the quality of published data and the necessary use of mean adult body sizes from the general literature to evaluate the relationship of generation time with body size. These results also indicate that because postembryonic development time scales to body mass, and embryonic development time scales to egg mass, the proportion of time spent in each phase is a function of relative egg size (Figure 3). That is, generation time is relatively constant for zooplankton of a given body size, but the proportion of time spent in the embryonic versus postembryonic phase is a function of the size of a species s egg relative to its adult size. The relationship between relative egg size and the proportion of time spent in each development phase lends partial support 247
8 J.F.Gillooly to the view that isochronal development (development with equal stage durations) occurs in zooplankton as originally proposed by Miller et al. for copepods (Miller et al., 1977). At the same time, this relationship does not support the premise that there is no relationship between embryonic and postembryonic development time in copepods (Landry, 1983). These results also indicate the nature of the relationship between embryonic and postembryonic development time with respect to relative egg size. Previous work with cladocera has shown that postembryonic development time is negatively correlated with relative egg size (Lynch, 1980). These results further demonstrate that while a species with a larger relative egg size spends less time in the postembryonic phase, it spends more time in the embryonic phase. Thus, the total time to maturity (embryonic + postembryonic periods) does not vary with relative egg size. The proportion of time spent in the embryonic phase of life is as much as 45% of total generation time and so cannot be discounted when considering the time to maturity. Variation in the time spent in each life history phase has often been explained as species-specific adaptations to environmental conditions. The results presented here suggest that scaling relationships must also be considered in addressing this variation. Questions at the level of populations, communities or ecosystems may benefit from the relationships of generation time to body mass and temperature. These relationships provide a new tool for use in investigations of the ecology, behavior and evolution of zooplankton. Acknowledgements I thank Mary Berthold, Matthew Brewer, Stanley Dodson and Beth Sanderson for helpful comments on this manuscript. I also thank Tony Ives, Bill Karasov, Jim Kitchell, John Magnuson, Tom O Keefe, Warren Porter and Carlos Santos- Flores for beneficial discussions regarding this work. This work was partially supported by NSF grant GER References Allan,J.D. (1976) Life history patterns in zooplankton. Am. Nat., 110, Allan,J.D. and Goulden,C.E. (1980) Some aspects of reproductive variation among freshwater zooplankton. In Kerfoot,C.W. (ed.) Evolution and Ecology of Zooplankton Communities. University Press of New England, Hanover, pp Blueweiss,L., Fox,H., Kudzma,V., Nakashima,D., Peters,R. and Sams,S. (1978) Relationships between body size and some life history parameters. Oecologia, 37, Bottrell,H.H. (1975) Generation time, length of life, instar duration and frequency of moulting and their relationship to temperature in eight species of Cladocera from the River Thames, Reading. Oecologia, 19, Cole,L.C. (1954) The population consequences of life history phenomena. Quart. Rev. Biol., 29, DuMont,H.J., Van de Velde,I. and DuMont,S. (1975) The dry weight estimate of biomass in a selection of Cladocera, Copepoda and Rotifera from the plankton, periphyton and benthos of continental waters. Oecologia, 19, Gillooly,J.F. and Dodson,S.I. (1999a) The relationship of neonate mass and incubation temperature on embryonic development time in a range of animal taxa. J. Zool. (Lond.), in press. 248
9 Generation time in zooplankton Gillooly,J.F. and Dodson,S.I. (1999b) Latitudinal patterns in the size distribution and seasonal dynamics of Cladocera. Limnol. Oceanogr., in press. Hann,B.H. (1982) Two new species of Eurycercus (Bullatifrons) from Eastern North America (Cladocera, Chydoridae). Int. Revue Ges. Hydrobiol., 67, Hann,B.J. (1984) Influence of temperature on life history characteristics of two sibling species of Eurycercus (Cladocera, Chydoridae). Can. J. Zool., 63, Hirst,A.G. and Lampitt,R.S. (1998) Towards a global model of in situ weight-specific growth in marine planktonic copepods. Mar. Biol., 132, Hirst,A.G., and Sheader,M. (1997) Are in situ weight-specific growth rates body size independent in marine planktonic copepods? A re-analysis of the global syntheses and a new empirical model. Mar. Ecol. Prog. Ser., 154, Huntley,M.E., and Lopez,M.D.G. (1992) Temperature-dependent production of marine copepods: A global synthesis. Am. Nat., 140, Hutchinson,G.E. (1967) A Treatise on Limnology. John Wiley and Sons, New York, Vol. 2, pp Kiørboe,T. and Sabatini,M. (1995) Scaling of fecundity, growth and development in marine planktonic copepods. Mar. Ecol. Prog. Ser., 120, Korpelainen,H. (1986) The effects of temperature and photoperiod on life history parameters of Daphnia magna (Crustacea: cladocera). Freshwater Biol., 16, Landry,M.R. (1983) The development of marine calanoid copepods with comment on the isochronal rule. Limnol. Oceanogr., 28, Laxhuber,R. and Hartmann,U. (1988) The influence of temperature on developmental stages of the cold-steno thermal rotifer Notholca caudata Carlin. Verh. Int. Verein. Theor. Limnol., 23, Lei,C.H. and Armitage,K.B. (1980) Growth, development and body size of field and laboratory populations of Daphnia ambigua. Oikos, 35, Lynch,M. (1980) The evolution of cladoceran life histories. Quart. Rev. Biol., 55, Maier,G. (1994) Patterns of life history among cyclopoid copepods of central Europe. Freshwater Biol., 31, McLaren,I.A. (1978) Generation lengths of some temperate marine copepods: estimation, prediction and implications. J. Fish. Res. Bd Can., 35, Miller,C.B., Johnson,J.K. and Heinle,D.R. (1977) Growth rules in the marine copepod genus Acartia. Limnol. Oceanogr., 22, Pauli,H.R. (1989) A new method of estimating individual dry weights of rotifers. Hydrobiologia, 186, Sanoamuang,L. (1993) The effect of temperature on morphology, life history and growth rate of Filinia terminalis (Plate) and Filinia cf. pejleri (Hutchinson) in culture. Freshwater Biol., 30, Taylor,St C.S. (1968) Time taken to mature in relation to mature weight for sexes, strains, and species of domesticated mammals and birds. Anim. Prod., 10, Threlkeld,S.T. (1987) Daphnia life history strategies and resource allocation patterns. In Peters,R.H. and De Bernardi,R. (eds) Daphnia. Mem. Instit. Idrobiol., Italy, pp Vijverberg,J. (1980) Effect of temperature in laboratory studies on development and growth of cladocera and Copepoda from Tjeukemeer, The Netherlands. Freshwater Biol., 10, Walz,N. (1983) Comparative population dynamics of rotifers Branchionus angularis and Keratella cochlearis. Hydrobioogia, 147, Yarwood,C.E. (1956) Generation time and the biological nature of viruses. Am. Nat., 90, Zar,J.H. (1996) Biostatistical Analyses. Prentice Hall, New Jersey, pp Received on January 12, 1999; accepted on August 16,
10 J.F.Gillooly Appendix I. Zooplankton generation time Species Adult mass Generation time (days) Reference µg 5 C 10 C 15 C 20 C Adult mass Generation time Cladocera Acroperus harpae Bottrell (1975) Bottrell (1975) Alona affinis Bottrell (1975) Bottrell (1975) Chydorus sphaericus Bottrell (1975) Bottrell (1975) Chydorus sphaericus 9.40 *** *** *** DuMont et al. (1975) Hann (1984) Daphnia ambigua Lei and Armitige (1980) Lei and Armitige (1980) Daphnia magna *** *** DuMont et al. (1975) Korpelainen (1986) Eurycercus lamellatus Bottrell (1975) Bottrell (1975) Eurycercus longirostris *** *** Hann (1982) Hann (1984) Eurycercus vernalis *** *** Hann (1982) Hann (1984) Graptoleberis testudinaria Bottrell (1975) Bottrell (1975) Pleuroxus denticulatus 4.54 *** *** *** DuMont et al. (1975) Hann (1984) Pleuroxus uncinatus Bottrell (1975) Bottrell (1975) Sida crystallina *** Bottrell (1975) Bottrell (1975) Simocephalus vetulus *** Bottrell (1975) Bottrell (1975) Cyclopoida Acanthocyclops robustus Maier (1994) Vijverberg (1980) Cyclops strennus Maier (1994) Maier (1990) Cyclops vicinus vicinus Maier (1994) Vijverberg (1980) Eucyclops serrulatus Maier (1994) Maier (1990) Mesocyclops leuckarti Maier (1994) Vijverberg (1980) Calanoida Acartia californiensis 5.12 *** *** Huntley and Lopez (1992) Huntley and Lopez (1992) Acartia clausi 5.11 *** Huntley and Lopez (1992) Huntley and Lopez (1992) Acartia tonsa 5.72 *** *** Huntley and Lopez (1992) Huntley and Lopez (1992) Calanoides carinatus *** *** Huntley and Lopez (1992) Huntley and Lopez (1992) Calanus finmarchicus *** Huntley and Lopez (1992) Huntley and Lopez (1992) 250
11 Generation time in zooplankton Appendix I. continued Species Adult mass Generation time (days) Reference µg 5 C 10 C 15 C 20 C Adult mass Generation time Calanus pacificus *** *** Huntley and Lopez (1992) Huntley and Lopez (1992) Calanus sinicus *** *** *** Huntley and Lopez (1992) Huntley and Lopez (1992) Centropages hamatus *** *** *** Huntley and Lopez (1992) Huntley and Lopez (1992) Eurytemora herdmanni *** Huntley and Lopez (1992) Huntley and Lopez (1992) Labidocera trispinosa *** *** *** Huntley and Lopez (1992) Huntley and Lopez (1992) Paracalanus parvus 6.98 *** *** *** Huntley and Lopez (1992) Huntley and Lopez (1992) Pseudocalanus elongatus *** Huntley and Lopez (1992) Huntley and Lopez (1992) Pseudocalanus minutus *** *** Huntley and Lopez (1992) Huntley and Lopez (1992) Pseudocalanus sp *** Huntley and Lopez (1992) Huntley and Lopez (1992) Pseudodiaptomus marinus *** *** *** Huntley and Lopez (1992) Huntley and Lopez (1992) Sinocalanus tenellus 10.8 *** *** Huntley and Lopez (1992) Huntley and Lopez (1992) Temora longicornis *** *** Huntley and Lopez (1992) Huntley and Lopez (1992) Rotifera Filinia terminalis Pauli (1989) Sanoamuang (1993) Filinia pejleri Pauli (1989) Sanoamuang (1993) Keratella cochlearis Pauli (1989) Walz (1983) Notholca caudata Pauli (1989) Laxhuber and Hartmann (1988) 251
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