Hatching of cladoceran resting eggs: temperature and photoperiod
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1 Freshwater Biology (2005) 50, doi: /j x Hatching of cladoceran resting eggs: temperature and photoperiod JOCHEN VANDEKERKHOVE,* STEVEN DECLERCK,* LUC BRENDONCK,* JOSÉ MARIA CONDE-PORCUNA, ERIK JEPPESEN, AND LUC DE MEESTER* *Laboratory of Aquatic Ecology, Katholieke Universiteit Leuven, Ch. de Bériotstraat, Leuven, Belgium Instituto del Agua, Universidad de Granada, Ramón y Cajal 4 (edif. Fray Luis de Granada), Granada, Spain Department of Freshwater Ecology, The National Environmental Research Institute, Vejlsøvej, Silkeborg, Denmark Department of Plant Ecology, University of Aarhus, Nordlandsvej, Risskov, Denmark SUMMARY 1. We identified temperature and photoperiod conditions under which the hatching of 45 cladoceran species could be elicited. Identification of appropriate hatching cues is of primary importance for the exploration of the ties between active and diapausing stages. 2. Incubation temperature affected the hatching success of resting eggs isolated from Danish, Belgian/Dutch and Spanish sediments. In general, most hatchlings and species were retrieved at 15 C. Danish and Belgian/Dutch resting eggs hatched more successfully under a long day photoperiod than in continuous illumination. 3. Most species could be retrieved after incubation of resting eggs isolated from a limited amount of sediment (0.4 kg) under a single, well chosen combination of temperature and photoperiod. Processing additional sediment samples under seven more incubation regimes only allowed detection of 21% (Spain) to 34% (Denmark) more species. 4. The incubation period for resting eggs to hatch was strongly influenced by incubation temperature. Our results show that hatching experiments aimed at assessing cladoceran species richness and conducted at 15 C should be continued for a period of at least 2 weeks, after which a random subset of hatchlings (e.g. n ¼ 100) can be selected from the total hatchling assemblage. Keywords: diapause, hatching, light, resting eggs, species richness, temperature Introduction Species richness in natural ecosystems is often underestimated, particularly for organisms with short generation times (Arnott et al., 1999; Melo & Froehlich, 2001) because of high variability in space and time of their community dynamics (Baur et al., 1996; Vinson & Hawkins, 1998). Considerable seasonal (Sommer et al., 1986) and inter-annual variations (Arnott et al., 1999; Grover, 1999) have been observed for zooplankton communities, and, moreover, zooplankton populations often exhibit diel vertical (De Meester et al., Correspondence: Jochen Vandekerkhove, Ch. de Bériotstraat 32, 3000 Leuven, Belgium. jochen.vandekerkhove@bio.kuleuven.ac.be 1999) or horizontal migration (Burks et al., 2002) or are restricted to specific habitats (Frey, 1986). Accumulations of resting eggs in lake sediments may integrate some spatial and temporal variability in community dynamics (Brendonck & De Meester, 2003) and analysis of resting egg banks often reveals many species (Crispim & Watanabe, 2001; Duggan, Green & Shiel, 2002; Vandekerkhove et al., 2004a). Unfortunately, the detection of zooplankton species from resting eggs in lake sediments is not free of problems, as only a limited proportion can be morphologically identified to species level (e.g. Anomopoda: Vandekerkhove et al., 2004b), thereby making it necessary to hatch the resting eggs prior to identification. The conditions appropriate for hatching of zooplankton resting eggs are species specific 96 Ó 2004 Blackwell Publishing Ltd
2 Single or multiple incubation conditions 97 (Carvalho & Wolf, 1989; Cáceres & Schwalbach, 2001) and may even differ among the eggs of a single species (De Meester & De Jager, 1993; Cáceres, 1998). Hatching cues may also differ between conspecifics from different geographic origins (Marcus, 1984; Schwartz & Hebert, 1987). In temperate regions, light and temperature are probably two of the most important proximate stimuli for the activation of zooplankton resting eggs. This is suggested by field observations of massive hatching during spring, irrespective of the local biotic and abiotic conditions (Wolf & Carvalho, 1989; Hairston, Hansen & Schaffner, 2000). Also, many laboratory studies have demonstrated a requirement for light (e.g. Shan, 1970; Sorgeloos, 1973) or high temperature (e.g. May, 1987; Schwartz & Hebert, 1987) in the hatching of zooplankton resting eggs. In the present paper we investigate how variations under optimal hatching conditions among species and regions interfere with a straightforward interpretation of species richness patterns in hatchling assemblages. For this purpose, resting egg banks of 95 shallow lakes situated in Denmark, Belgium/the Netherlands and Spain were sampled. Sediment samples were incubated under four different temperatures (10 25 C, 5 C interval) and under two different photoperiods (16 h light day )1 versus continuous light). Methods Field sampling Sediment samples were collected in 95 shallow waterbodies distributed over three geographic regions: Denmark (29 lakes), Belgium/the Netherlands (34 lakes) and Spain (32 lakes). Within each region we sought to select lakes that differed markedly in size, nutrient load, macrophyte cover and degree of connectedness. In Denmark and Belgium/the Netherlands, sampling was conducted in early spring (March) 2001 after resting eggs have received a cold shock in their natural habitat, but before the onset of the zooplankton hatching peak and growing season. In Spain, weather conditions are favourable year-round for zooplankton reproduction, except in lakes that become temporarily dry. For this reason, sampling in Spain was delayed until October 2001, a period during which a large number of lakes dried out partially or completely. Sediment samples were collected at five randomly chosen locations in the littoral zone and five randomly chosen locations in the pelagic zone. The upper 3 cm of each core were wrapped in aluminium foil immediately after collection. Samples were transported to the laboratory in a cool box, where they were put in a refrigerator (4 C) in darkness upon arrival. Processing of samples After a pre-incubation period of at least 4 months at 4 C, one pooled sample was created for every lake by combining all pelagic and littoral samples. A regional sample was created by combining subsamples from these pooled samples (subsample weight: Denmark: 110 g, Belgium/the Netherlands: 94 g and Spain: 100 g). After thorough mixing, this regional sample was divided into 32 subsamples of 100 g (wet weight), each covering the within lake and within region variation in egg bank community structure. Resting eggs were isolated from the sediment by means of the sugar flotation method (Onbé, 1978; Vandekerkhove et al., 2004c) and then incubated in 2-L aquaria filled with diluted Artificial Daphnia Medium (AdaM; 200 ls cm )1 ; Kluttgen et al., 1994). Aquaria were randomly allocated to eight treatments, comprising all possible combinations of four temperatures (10 C, 15 C, 20 C and 25 C) and two photoperiods (16 h light day )1 versus 24 h light day )1 ). The incubation medium was renewed every 9 days. For a period of 30 days, cladoceran hatchlings were isolated from the aquaria at 3-day intervals. This was carried out by filtering the contents of the aquarium over a 50 lm mesh and picking out individual hatchlings under a binocular microscope. Hatchlings were individually transferred to 50 ml jars filled with filtered pond water (mesh size: 20 lm), where they were fed Scenedesmus acutus ( cells ml )1 ). They were grown until they could be identified using the key of Flößner (2000). All hatchlings could be identified to family level upon transferral. Hatchlings that died during cultivation were proportionally assigned to species that could be identified from full-grown individuals of the corresponding family. Data analysis For this paper, the terms mortality, hatchling abundance and species richness were given specific
3 98 J. Vandekerkhove et al. definitions. Mortality is defined as the percentage of hatchlings that died before reaching a morphologically identifiable stage. Hatchling abundance and species richness are the number of hatchlings and of species, respectively, detected in an aquarium during the 30 day incubation period. For each region separately, 2-way ANOVAs were carried out to test the effects of temperature and photoperiod on mortality, hatchling abundance, and species richness. Hatchling abundance data were square root transformed prior to analysis to normalise residuals. We also tested for differences in species richness among treatments after controlling for differences in hatchling numbers. This was carried out by applying 2-Way ANCOVA testing the effect of temperature and photoperiod on species richness, with hatchling abundance specified as covariable. Hatchling abundance data of the omnipresent species (i.e. species of which at least five hatchlings were retrieved from samples of each region: Ceriodaphnia pulchella, Daphnia galeata, D. magna, D. pulex and Diaphanosoma brachyurum) were used as replicate observations to test for differences between pairs of regions with respect to the temperature at which the average individual of these species hatched (paired t- tests). All parametric tests were computed in Statistica 6.0 (Statsoft, Inc., 2003). For ANOVA and ANCOVA models, Bartlett tests were carried out to test assumptions of homogeneity of variances, and normal probability plots were visually checked for normality of residuals. In the ANCOVA analyses, slopes of regressions of the covariate (hatchling abundance) with the dependent variable (species richness) were homogeneous among treatments (test for homogeneity of slopes: P > 0.05; Statsoft, Inc., 2003). Results Mortality Of all 4050 hatchlings that emerged, 82.1% could be identified to species level. Average hatchling mortality tended to be slightly lower in sediments from Belgium/the Netherlands (14.7%) than from Denmark (19.7%) and Spain (20.2%) and was not affected by temperature nor by photoperiod (Table 1). Average mortality was relatively low for Daphniidae (15.6%), Bosminidae (16.6%) and Sididae (25.8%) Table 1 Results of ANOVA and ANCOVA analyses testing for the effects of temperature and photoperiod on mortality, species richness and hatchling abundance in hatchling assemblages obtained from resting egg bank samples. Samples were collected in three European regions: Denmark (DK), Belgium/the Netherlands (BNL) and Spain (SP). and relatively high for Chydoridae (37.7%), Moinidae (39.1%) and Macrothricidae (46.2%). Species richness d.f. F DK F BNL F SP Mortality (ANOVA) Temperature Photoperiod Temperature photoperiod Species richness (ANOVA) Temperature *** * Photoperiod *** 4.2* 0.9 Temperature photoperiod 3 4.2* Species richness (ANCOVA, correcting for hatchling abundance) Temperature Photoperiod * Temperature photoperiod Hatchling abundance (ANOVA) Temperature *** 6.0** 7.2** Photoperiod *** ** Temperature photoperiod *P < 0.05; **P < 0.01; ***P < In total, 45 cladoceran species, belonging to 24 different genera, hatched from the egg bank samples (Table 2). Species richness differed significantly between temperature and photoperiod treatments (Fig. 1a; Table 1), but this was mainly because of the variation in hatchling abundance between treatments (Fig. 1b; product-moment correlation coefficient between species richness and hatchling abundance: r ¼ 0.83, P < 0.001). Indeed, after partialling out the effect of hatchling abundance, there was no longer a significant treatment effect on species richness for Denmark and Belgium/the Netherlands (Table 1). This indicates that the number of species that could be detected for a specific hatching condition mainly depended on the number of hatched individuals rather than the intrinsic hatching conditions. This was, however, not completely true for Spain, where samples incubated under long day conditions yielded fewer species for a given number of hatchlings than samples supplied with a continuous light stimulus.
4 Region Denmark Belgium/The Netherlands Spain Temperature ( C) Photoperiod (hours light per day) Acroperus harpae (Baird 1835) Alona affinis (Leydig 1860) Alona costata Sars 1862 Alona quadrangularis (O.F. Müller 1776) Alona rectangula Sars 1861 Alonella exigua (Lilljeborg 1853) Alonella nana (Baird 1843) Bosmina coregoni Baird 1857 Bosmina longirostris (O.F. Müller 1785) Camptocercus rectirostris Schoedler 1862 Ceriodaphnia dubia Richard 1894 Ceriodaphnia laticaudata P.E. Müller 1867 Ceriodaphnia megops Sars 1862 Ceriodaphnia pulchella Sars 1862 Ceriodaphnia quadrangula (O.F. Müller 1785) Ceriodaphnia reticulata (Jurine 1820) Chydorus sphaericus (O.F. Müller 1776) Daphnia ambigua Scourfield 1946 Daphnia galeata/cucullata Sars 1863 Daphnia magna Strauss 1820 Daphnia parvula Fordyce 1901 Daphnia pulex Leydig 1860 Diaphanosoma brachyurum (Liévin 1848) Disparalona rostrata (Koch 1841) Dunhevedia crassa King 1853 Eurycercus lamellatus (O.F. Müller 1776) Graptoleberis testudinaria (Fischer 1848) Ilyocryptus silvaeducensis Romijn 1919 Ilyocryptus sordidus (Liévin 1848) Latona setifera (O.F. Müller 1776) Leydigia acanthocercoides (Fischer 1854) Leydigia leydigi (Schoedler 1863) Macrothrix laticornis (Jurine 1820) Macrothrix rosea (Jurine 1820) Moina brachiata (Jurine 1820) Oxyurella tenuicaudis (Sars 1862) Pleuroxus aduncus (Jurine 1820) Pleuroxus laevis Sars 1861 Pleuroxus letourneuxi (Richard 1988) Pleuroxus trigonellus (O.F. Müller 1776) Pleuroxus uncinatus Baird 1850 Scapholeberis mucronata (O.F. Müller 1776) Sida cristallina (O.F. Müller 1776) Simocephalus vetulus (O.F. Müller 1776) Tretocephala ambigua (Lilljeborg 1901) Single or multiple incubation conditions 99 Table 2 Categorical number of hatchlings obtained at different temperatures, photoperiods and regions of each of the cladoceran species that hatched during the experiments 1 hatchling; 2 5 hatchlings; 6 10 hatchlings; hatchlings; hatchlings.
5 100 J. Vandekerkhove et al. 16 h light per day 24 h light per day 20 Denmark Belgium/ The Netherlands Spain 15 Species richness Hatchling abundance Temperature ( C) Fig. 1 Number of cladoceran species (a) and hatchlings (b) retrieved after incubation at different temperatures and photoperiods of resting eggs isolated from 0.1 kg of lake sediment collected in three different geographic regions in Europe. Error bars denote 2 standard errors. Hatchling abundance Temperature had a significant effect on the overall hatchling abundance from the resting egg banks of all three regions (Fig. 1b; Table 1). In general, hatchling abundance was highest at 10 and 15 C, and declined with increasing temperature (e.g C). The effect of photoperiod on overall hatchling abundance varied among regions, from insignificant (Belgium/the Netherlands) to strong (Denmark and Spain; Table 1).
6 Single or multiple incubation conditions 101 For Denmark and Spain, resting eggs hatched more successfully in a long day photoperiod than under continuous illumination. A marginally significant interaction between temperature and photoperiod was found for Denmark (Table 1; P ¼ 0.087). At low temperatures, Danish samples yielded 2.4 (15 C) to 2.6 (10 C) times more hatchlings in a long day photoperiod than under continuous illumination, while at high temperatures this ratio was substantially higher (8.4 at 25 C to 9.6 at 20 C; see also Fig. 1b). Resting eggs of each of the omnipresent species hatched on average at lower temperatures when isolated from Danish samples than when isolated from Spanish samples (Paired t-test: d.f. ¼ 4, t ¼ 3.8, P ¼ 0.020), with an average difference over these species between both regions of 1.7 C. Incubation period Almost all species able to hatch at a given temperature, hatched within 1 week at 25 C and within 2 weeks at 10 C (Fig. 2). Incubation at low temperatures allowed detection of a larger proportion of the regional species pool. For all regions, over 70% of all species detected in each region was hatched at least once within 12 days when incubated at 15 C. At other temperatures, an average of 55% (25 C) to 64% (20 C) of all regional species hatched within 12 days. Incubation at a single temperature allowed detection of at most 75% for Denmark (15 C) and 77% for Belgium/the Netherlands (15 C) of all regional species within 30 days. For Spain, all but one species were found within 1 month in the low temperature aquaria (10 C, 96% of regional species). Denmark Belgium/The Netherlands Spain C 15 C Fraction of regional species (%) C 25 C Incubation period (days) Fig. 2 Cumulative percentage of all cladoceran species found within one of the three geographic regions at subsequent points in time during the experiment for different incubation temperatures. For each incubation temperature, all identifiable hatchlings from all four replicates from both the 16 L/8 D and 24 L/0 D are combined. Regional species richness is here defined as the total number of species found in a given region in our study, i.e. after incubation of resting eggs isolated from a 3.2 kg sediment sample, covering lakes, under eight different incubation conditions.
7 102 J. Vandekerkhove et al. Discussion Species richness and hatchling abundance Light is a universal proximate cue for termination of dormancy (e.g. plants: Leblanc et al., 1998; insects: Tauber, Tauber & Masaki, 1986; cladocerans: 1971; copepods: Williams-Howze, 1997; rotifers: Gilbert, 1974; mites: Veerman, 1994). Photoperiod is likely to be a key factor explaining the seasonal pattern of emergence observed for many temperate zooplankton populations (Herzig, 1974; Hairston et al., 2000). Our results suggest that resting eggs from Danish samples are more responsive to changes in photoperiod length than are Belgium/the Netherlands and Spanish resting eggs. Danish populations may experience a stronger selection pressure for phasing their active periods with seasonal cycles because the time available for population development is relatively short. Also, the amplitude of the within-year fluctuations in photoperiod length is higher in Denmark (10.5 h) than in Belgium/the Netherlands (8.5 h) and Spain (5.0 h). Therefore, photoperiod may be a more reliable cue for the synchronisation of life cycle phases to seasonal cycles in Denmark than in Belgium/the Netherlands and Spain. Among zooplankton species, a number of factors may alter the hatching success at a given day length, such as temperature (May, 1987, this study), light intensity (Vanhaecke, Cooreman & Sorgeloos, 1981), oxygen concentration (Lutz, Marcus & Chanton, 1992), salinity level (Nielsen et al., 2003) and food quality (Irigoien et al., 2002). Alekseev & Lampert (2001) showed that the combined perception of photoperiod and food availability resulted in two peaks of sexual reproduction in a German Daphnia pulicaria clone, one in June and one in November. Our results suggest the occurrence of a photoperiod by temperature interaction effect on the hatchling abundance of Danish resting eggs. This might explain why resting eggs from this latitude hatch predominantly in April (Herzig, 1974; Hairston et al., 2000) and not in September. Photoperiod length is similar in both months, but lake water temperature differs in most years (E. Jeppesen, unpublished data water temperatures of eight shallow lakes for 12 years). The absence of a photoperiod by temperature interaction effect on the hatchling abundance of Belgian/Dutch and Spanish resting eggs may reflect the fact that the within-year variation in temperature also decreases along the north-to-south gradient. In high latitude lakes, the combined response to temperature and photoperiod might not only allow perception of the time of the year, but also allow a better synchronisation of egg emergence with timing of ice-out (Cáceres & Schwalbach, 2001) or enhance a more discrete switch from one reproductive mode to another (Hairston & Kearns, 1995). In general, the highest hatchling abundances were found under low temperature conditions (10 and 15 C). This is in agreement with the results of other studies to determine the optimal incubation temperature for hatching of cladoceran resting eggs from temperate regions (Schwartz & Hebert, 1987; Carvalho & Wolf, 1989). In our experiments, resting eggs of the five omnipresent species hatched on average at higher incubation temperatures when isolated from Spanish compared with Danish sediment samples. Schwartz & Hebert (1987) similarly found that arctic clones of Daphnia pulex required a low hatching temperature (7 C), whereas clones from warmer climates hatched best at C. The stimuli for induction and termination of diapause appear adjusted to the prevailing climatic conditions by natural selection to maximise survival, growth and reproduction of the local populations. Incubation period At 15 and 20 C, most species started to hatch after 3 6 days. This is comparable with the incubation periods reported in several earlier studies (Schwartz & Hebert, 1987; De Meester & De Jager, 1993). At lower temperatures, hatching is delayed by several days. Schwartz & Hebert (1987) recorded the first hatching of Daphnia pulex at 7 C after 9 days of incubation. In our study, most of the species hatched after 9 12 days when incubated at 10 C. Carvalho & Wolf (1989) observed most Daphnia resting eggs to hatch at 12 C 7 10 days after exposure to light (88.3%). In the latter study, increasing the incubation temperature from 6 to 20 C resulted in a decrease from 15 to 4 days in the time required to hatch 50% of the resting eggs. Despite the negative correlation between incubation temperature and incubation period, it is advisable to incubate resting eggs from sediments from Europe and other temperate areas at relatively low temperatures when the main goal is retrieval of many individuals or species. Our results clearly indicate that 15 C is a good compromise. For
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