Hydrobiologia 427: 167–176, 2000. © 2000 Kluwer Academic Publishers. Printed in the Netherlands.
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Habitat selection in the larvae of two species of Zygoptera (Odonata): biotic interactions and abiotic limitation Claudia Steiner, Barbara Siegert, Susanne Schulz & Frank Suhling∗ Zoologisches Institut, Technische Universität Braunschweig, Fasanenstraße 3, D-38106 Braunschweig, Germany E-mail:
[email protected] Received 7 July 1999; in revised form 10 December 1999; accepted 2 January 2000
Key words: activity patterns, foraging behaviour, growth, oxygen content, predation
Abstract Field and laboratory experiments were set up to obtain data on the reasons for different habitat selection of Enallagma cyathigerum and Platycnemis pennipes. (1) Rearing of larvae in two different ponds showed that while P. pennipes was not able to survive conditions of low oxygen content, 50% of the E. cyathigerum larvae survived. (2) In field predation experiments with sticklebacks and dragonflies as predators, we found that E. cyathigerum suffered highest predation by the fish. In P. pennipes, mortality was highest with Anax imperator. (3) Experiments regarding larval behaviour showed that E. cyathigerum was generally more active and had higher foraging success than P. pennipes. Both species reduced activity in the presence of fish, but E. cyathigerum did so to a minor extent. In contrast to P. pennipes, E. cyathigerum showed escaping behaviour. (4) In the laboratory, the growth of E. cyathigerum was faster than that of P. pennipes.
Introduction The presence of fish alters the species assemblage of Odonata and decreases overall densities compared to fish-free ponds (Macan, 1966; McPeek, 1990a; Pierce & Hinrichs, 1997). Fish particularly reduce the abundance of species that forage actively (Pierce, 1988; McPeek, 1990b; Blois-Heulin et al., 1990). In general, dragonfly larvae coexisting with fish show behavioural adaptations like hiding and reduced activity (e.g. Pierce, 1988; McPeek, 1990a, 1998). Adaptations to fish predation are associated with slow growth due to reduced foraging success: most of these odonate species are uni- or semivoltine (Johnson, 1991). Species which usually occur in fish free waters are more active and grow much faster – they are often bivoltine (Johnson, 1991). Such species are not able to survive in the presence of fish except in microhabitats where exposure to fish can be avoided, such as shallow water or dense vegetation (e.g. Macan, 1966). ∗ Author for correspondence
Ponds and lakes may be free of fish due to harsh abiotic conditions, e.g. acidic pH (Paterson, 1994; Bendell & McNicol, 1995). Under such conditions, one should expect an odonate community typical of fish free waters. Odonata usually occuring together with fish are rarely found in fishless ponds and has been interpreted as an effect of predation by actively hunting invertebrates like dragonfly larvae (BloisHeulin et al., 1990; McPeek, 1990b, 1998). Damselflies occuring with those predators show increases in caudal lamella size making them powerful swimmers, which seems to be a good escape tactic (McPeek, 1995). On the other hand, odonates may also be influenced by harsh conditions. It has been shown that only specialized species could develop in temporary or acidic waters (Sternberg, 1990; Fincke, 1992). The restriction to such types of habitats can be interpreted as evolved predator avoidance (Sih, 1987). The aim of our study was to identify the reasons for the different distribution of two species of Zygoptera: Enallagma cyathigerum (Charpentier, 1840) (Coenagrionidae) and Platycnemis pennipes (Pallas, 1771) (Platycnemididae). The holarctic E. cyathigerum lives
168 Table 1. Odonate species emerged from the two study sites in 1994. The digits are the total number of specimens emerged at the ponds’ edges in emergence cages of 1 m2 which were open to colonization throughout the emergence period. ∗ This species was extremely under-represented in the sample because it emerged on floating algae in the middle of the pond Species
Emerged specimens per 1m2 in pond A pond B
Platycnemis pennipes (Pallas) 116 Somatochlora metallica (Van der L.) 1 Sympetrum sanguineum (Müller) 1 Ischnura elegans (Van der L.) Orthetrum cancellatum (L.) Aeshna mixta (Latr.) Lestes sponsa (Hansemann) Enallagma cyathigerum (Charp.) Sympetrum vulgatum (L.) Anax imperator (Leach) Libellula depressa (L.) Erythromma viridulum (Charp.)∗
-
181 2 2 1
196 6 3 2
-
1225 16 8 4 1
mainly in fish-free and/or vegetation rich ponds and lakes (e.g. Johannsson, 1978; McPeek, 1990a; Paterson, 1994). Macan (1966) showed that the introduction of Salmo trutta to a pond reduced the abundance and altered the microdistribution of E. cyathigerum. Koperski (1997) reports that the larvae of E. cyathigerum reduce foraging activity in the presence of chemical stimuli of fish. On the other hand, Chowdury & Corbet (1988) found that the feeding rate of E. cyathigerum is not depressed in presence of an invertebrate predator. The eurosiberian P. pennipes breeds in rivers and in fish ponds (Martens, 1996). In the study region (see below), both species occur in lentic waters of different types but rarely co-occur (e.g. Rehfeldt, 1983). In our study, we tested the following hypotheses in field and laboratory experiments: (1) Larvae of P. pennipes are not able to survive under the abiotic conditions of a typical E. cyathigerum pond and vice versa. (2) E. cyathigerum is more vulnerable to fish predation than P. pennipes, which, in contrast, is more vulnerable to predation by large dragonfly larvae (Anisoptera). (3) P. pennipes shows better behavioural adaptation to fish predation as regards reaction to fish attacks, activity patterns and foraging. (4) As a result of higher activity E. cyathigerum grows faster than P. pennipes and may, therefore, be a better competitor in its specific habitats.
Methods Study area and organisms Our field experiments were carried out in two ponds NW of Braunschweig, N Germany. Pond A is a fish pond in the floodplain of the river Oker. Fish known to live in it are Perca fluviatilis (L.), Esox lucius (L.), Anguilla anguilla (L.), Gasterosteus aculeatus (L.) and eight species of cyprinids, the most frequent being: Scardinius erythophtalhalmus (L.), Rutilus rutilus (L.) and Leucaspius delineatus (Heckel). The maximum depth is 2.5 m; the shoreline 230 m. Nuphar lutea (Sm.) and Myriophyllum spicatum (L.) are the dominant plants. Pond B is situated 2.5 km west of A and part of the Braunschweig sewage farm. It has a shoreline of 1660 m and a maximum depth of 1.2 m. Due to occasional sewage import, it has highly eutrophic conditions, with different species of algae covering the whole surface during the summer. The submerged vegetation mainly consists of Ceratophyllum submersum (L.). Pond B contains no fish; the dominant predators are Odonata larvae (nine species), Heteroptera and Coleoptera. The odonate community of pond A consists of seven odonate species and is widely different from pond B (see Table 1). Whereas E. cyathigerum was exclusively found in B, P. pennipes larvae are restricted to A. The odonate larvae and fish used in this study were caught in the study ponds 2 weeks before the start of the respective experiment. The odonates were fed ad libitum with Chironomidae for 24 h and then starved 3 days before each treatment. To obtain eggs we exposed fresh and egg free stems of C. submersum to ovipositing females of both species (for methods see Martens, 1994). Larval survival in the study ponds To study the survival of E. cyathigerum and P. pennipes under the respective physical and chemical water conditions of the two ponds, we introduced cages containing stems of C. submersum with eggs of both species in each study pond. The eggs of P. pennipes were collected on 19 July 1994, those of E. cyathigerum on 20 July. The cages were 10 l tubes (diameter = cm, height = cm) made of plastic frames fitted with gauze (meshwidth: 0.25 mm) at the sides and bottom and closed at the top with a lid of gauze. A polystyrene float was attached to the upper level of each cage, ensuring flotation and holding a constant volume of 8 l of pond water. For each species three
169 cages with 200 eggs, which had been reared in the laboratory at 20 ◦ C since the collecting date, were introduced into each pond. At this time, in all eggs, the development was nearly complete. Beginning on 14 August, the oxygen content in pond B decreased rapidly to 0.3 mg l −1 . Therefore, the experiment was terminated on 17 August. The larvae were counted and their density per litre was calculated. To test differences in density between the study ponds and the species, Mann–Whitney U-tests were used (Sokal & Rohlf, 1995).
Table 2. Laboratory experiments on predation success by larval Enallagma cyathigerum and Platycnemis pennipes (10 larvae per species). Listed are the density of zooplankton per liter, origin (pond A, B) and date of sampling and the number of replicates with E. cyathigerum, P. pennipes and without Zygoptera larvae (control) Origin and date of Density of Number of replicates with sampling zooplankton P. pennipes E. cyathigerum control Pond B: 24 June Pond B: 15 June Pond A: 15 June Pond A: 25 July Pond A: 03 July Pond A: 24 June
140 344 1695 1977 3002 4095
2 2 2 5 3 2
2 2 2 5 3 2
2 2 2 5 3 1
Predation experiment We studied the effect of three species of predators on the larvae of E. cyathigerum and P. pennipes using field enclosures situated in pond A. The predators were Anax imperator, Orthetrum cancellatum (Odonata) and Gasterosteus aculeatus (Pisces). A. imperator and O. cancellatum represented the large invertebrate predators in pond B. O. cancellatum is restricted to the bottom, A. imperator hunts on the bottom, as well as between emerged plants. The stickleback represented the fish-predators of pond A. The cages were constructed as described above (growth experiment) but with gauze of 840 µm meshwidth. The cages contained three stems of C. submersum without branching (length: 18 cm) and some mouldering leaves serving as refuges for the zygopteran larvae. To allow colonisation of prey, the cages were introduced into the pond 10 days before the start of the experiment. We performed a two-way ANOVA design with the predator treatment (with A. imperator, with O. cancellatum, with G. aculeatus, without predator, DF = 3) and the prey species (P. pennipes, E. cyathigerum, DF = 1) as independent variables. The cages were stocked with 20 larvae of E. cyathigerum or 20 larvae of P. pennipes–which is an initial density of 2.5 larvae l−1 (≈ 400 larvae m−2 ) and with one of the predators; cages without predators served as controls (n = 10 replicates in each treatment). After 1 week, the remaining larvae were counted. For pairwise comparisons, a posteriori analyses on means (Fischer’s PLSD; see Sokal & Rohlf, 1995) were used. Larval response to predator attacks To test the direct reaction of the two damselflies, we imitated a fish attack according to Henrikson (1988). The experiment was carried out in the laboratory (20 ◦ C) in plastic dishes (11 cm high, 25 cm in diameter)
the bottom filled with sand. A single larva was introduced into the centre of a dish so that it could accustom to the new surroundings for 4 h. Afterwards, a pasteur pipette with a wide opening was used to imitate a fish attack by pumping twice at the back of the larva. The direct reactions of the larva in the following 2 min were recorded. This experiment was carried out with 20 larvae of each species. To evaluate the results, we classified the observed reactions into two categories. Fast movement: this category includes immediate fast swims or walks. Slow or no movement: this category includes either a very slow and cautious movement of single legs with a distance covered of maximally 0.5 cm or no motion or other reaction at all. For statistical analysis a contingency table test was performed. Foraging experiments The foraging of E. cyathigerum and P. pennipes was studied in the laboratory using zooplankton in different natural densities from the two study ponds. From each pond 30 l samples were taken and mixed; 2 l were filled into plastic aquaria (volume: 2.5 l), which contained a piece of gauze as a vertical structure to enable the larvae to reach the whole volume. Each aquarium was stocked with 10 larvae of E. cyathigerum or P. pennipes. Aquaria without larvae remained as controls. The zooplankton treatments and numbers of replicates are shown in Table 2. After 5 days under laboratory conditions (see above), the remaining zooplankton in each aquarium was filtered through a gauze (meshwidth: 80 µm), filled into 100 ml of ethanol (70%) and from each case the zooplankton of 10 × 1 ml was counted and identified. We distinguished four groups of zooplankton: Copepoda, large Cladocera, Scapholeberis mucronata and others.
170 In the treatment with a zooplankton density of 1977 l−1 , an ANOVA was performed to analyse differences in zooplankton density between the Zygoptera treatments and the controls. For pairwaise comparisons of mean densities, we used a posteriori analyses (Fischer’s PLSD). The zooplankton compositions between the treatments were compared with contingency tables. To examine the assumption that the difference in zooplankton density between the controls and the aquaria containing larvae is the mortality due to the Zygoptera larvae, the zooplankton density in the controls at the end of the treatment was compared with the initial values. After 5 days, the zooplankton in the control did not differ significantly in density (ANOVA, F = 1.17, P = 0.307) nor in composition (contingency table, chi2 = 1.74, P > 0.05) from the freshwater caught in the field at the start of the experiment. Activity modes To compare the activity modes of the two species, we used video with time lapse (one record of 1/4 second per min). We varied two factors: prey availability and the presence of fish. In the first treatment we studied the influence of prey availability on the activity modes. We used zooplankton (see above) in a density of 3500 individuals per l (N = 5 replicates per species). In the second treatment, we used sticklebacks which were isolated from the larvae by a pane of glass (N = 5 replicates). Nine hours before starting the record, the sticklebacks were put into their part of the experimental aquarium. The fish was visible to the larvae and also perceivable by vibration. There was no prey available in this treatment. The activity patterns without prey or predator were also recorded and served as controls (N = 10 replicates). Two larvae per species together were recorded for 24 h in an aquarium (length: 24 cm, width: 7.5 cm, height: 24 cm) which contained 4 l dechlorinated water, the bottom was covered with sand and one big leaf (out of a pond) and there were two stalks of C. submersum. The experiments were carried out at 16 ◦ C, 13 h light (500– 600 lux) and for an 11 h period with red light (50 lux). The larvae had head widths (HW) between 3.1 and 3.7 mm and were collected in the study ponds. Three days before the experiment, the larvae were fed ad libitum and then they remained without food. Nine hours before starting the record, the larvae were dropped into the experimental aquarium to have time to settle. The animals were used only once.
While analysing the videotapes we distinguished three types of behaviour: 1. The larva still stayed in the same position in the aquarium in two consecutive records (= inactive). 2. The larva altered its position in the aquarium in two consecutive records (= active). 3. The larva stayed in the same position and only moved its abdomen from one side to the other (= abdominal waving). Not all sequences of the video-tapes could be analysed due to technical problems. Due to this, the number of sequences recorded per replicate was uneven and we decided to use contingency tables for statistical analysis. The data of all replicates per treatment were added up, so that the statistical analyses are based on the total number of sequences registered per treatment. Larval growth We studied larval growth under laboratory conditions starting on 3 August 1994. Eggs were reared in 1 l jars in the laboratory at 25 ◦ C and 16:8 hours light:dark. The water was replaced with original water of pond B once per week. Each jar was provided with stems of C. submersum. The number of eggs was 211 of E. cyathigerum and 172 of P. pennipes. After hatching, the larvae were fed daily with zooplankton from the ponds. Dead or emerged individuals were registered in weekly intervals. After 40, 80 and 120 days, the HW was measured using a binocular microscope (accuracy: 0.01 mm). We used t-tests for comparisons of means in HW between the species.
Results Larval survival in the study ponds The density of larvae of both species found in the cages was significantly lower in pond B than in A (U test, U = 0.000, P ≤ 0.05). The density of Enallagma cyathigerum was significant higher in both ponds (U test, U = 0.000, P ≤ 0.05). Whereas in Platycnemis pennipes, the density per 1 l was 17 ± 0.6 (SD) in pond A and 0.2 ± 0.3 in pond B, the density of E. cyathigerum was 21 ± 1.6 in A and 12.6 ± 3.1 in B. In pond B, four living larvae of P. pennipes were found counting all cages; in E. cyathigerum the total number was 303.
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Figure 1. Mean larval density (± SD) of Enallagma cyathigerum and Platycnemis pennipes after 1 week in the presence of Anax imperator, Orthetrum cancellatum or Gasterosteus aculeatus or without predator (n = 10 replicates, each). The initial density was 2.5 ind per 1 l in both damselflies. A posteriori analyses (Fischer’s PLSD); between the species: NS = not significant, ∗∗∗ = P < 0.001; between the treatment in each species: A = significant comparedt to all other treatments, B = significant compared to A.
Effects of different predators on larval mortality The density of remaining larvae after 1 week in the cages (Figure 1) varied significantly with the predator treatment and the prey species (two-way-ANOVA: predator: F = 35.43, P = 0.001; prey: F = 20.15, P ≤ 0.001; predator × prey: F = 19.28, P = 0.001). In both prey species, survival was significantly reduced with each predator compared with the controls, except for P. pennipes, in which there was no significant reduction with Orthetrum cancellatum (Figure 1). Whereas in E. cyathigerum, the reduction was higher in the presence of sticklebacks than in the presence of Anax imperator or O. cancellatum, P. pennipes suffered the highest mortality in the presence of A. imperator (Figure 1). A posteriori comparisons of means showed that the density of remaining larvae did not differ significantly between E. cyathigerum and P. pennipes in the presence of the dragonflies. In contrast, there was a significant difference between E. cyathigerum and P. pennipes in the presence of the stickleback (Figure 1). Survival of E. cyathigerum was reduced to a significantly greater extent in the presence of this predator than the survival of P. pennipes.
Figure 2. Effect of the predation by larvae of Enallagma cyathigerum and Platycnemis pennipes on zooplankton density and composition with an initial zooplankton density of 1977 ind l−1 . The bars indicate the mean density (A) of remaining zooplankton and (B) the percent composition after 120 h in enclosures with 10 E. cyathigerum, 10 P. pennipes or without Zygoptera larvae (controls) (n = 5 replicates in each treatment). (A) U -test; (B) Contingency table: NS = not significant, ∗ = P < 0.05, ∗∗ = P < 0.01, ∗∗∗ = P < 0.001.
Figure 3. Effect of the initial zooplankton density on the predation rates of larval Enallagma cyathigerum and Platycnemis pennipes (see Table 2).
four larvae made only slow movements. In contrast, no larva of P. pennipes moved quickly, three larvae moved slowly and no did so over a longer distance (max. 0.5 cm).
Response to simulated predator attacks Foraging The reactions of E. cyathigerum and P. pennipes larvae to a simulated fish attack were significantly different (contingency table, chi2 = 26.67, P ≤ 0.001). Sixteen out of 20 E. cyathigerum larvae responded immediately with fast movements over a distance of 2–8 cm;
In the presence of both Zygoptera species, the zooplankton density was significantly reduced compared to the controls (ANOVA, F = 372.41, P = 0.001) (Figure 2A). Moreover, the density was significantly
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Figure 4. Activity modes of Enallagma cyathigerum and Platycnemis pennipes in control without zooplankton and fish, in the presence of zooplankton, in the presence of one stickleback (Gasterosteus aculeatus). The pies are the percent share of the behavioural categories inactive, walking/swimming and abdominal waving of the recorded intervalls over 24 h. The digits indicate the number of intervals recorded. Contingency tables: ∗∗∗ = P = 0.001.
lower in the E. cyathigerum-treatment than in the P. pennipes-treatment. With E. cyathigerum, there was a tendency to a strong increase of predation with increasing densities of zooplankton up to 3000 ind l−1 (Figure 3). In contrast, the predation rate of P. pennipes tended to increase only moderately with the increase of food density up to 3000 ind. l−1 . Above this density, the predation rate of P. pennipes highly increased. The zooplankton composition was significantly altered in the presence of E. cyathigerum (Figure 2B) due to a reduction of large cladocera (mainly Daphnia magna). In contrast, P. pennipes had no significant effect on the community composition. Behavioural responses to the presence of food or predators The activity modes in the controls differed significantly between the Zygoptera species (Figure 4). Whereas E. cyathigerum were inactive in 51% of the observed time, P. pennipes spent 82% without activity. In the presence of zooplankton, E. cyathigerum larvae changed their activity patterns. The abdominal waving increased from 12% to 32% of the observed time and walking/swimming was reduced to half. In P. pennipes, walking/swimming and abdominal waving enhanced moderately. Although both species stopped abdominal waving and reduced their activity in the presence of a stickleback, E. cyathigerum were much more active (27% of the observed time) than P. pennipes (6%).
Figure 5. Growth of larvae of Enallagma cyathigerum and Platycnemis pennipes shown as HW frequency diagrams after (from the top) 40 days (28, 29 August), 80 days (7, 8 October), and 120 days (16, 17 December) of development in the laboratory at 25 ◦ C. In both species, the first hatch was on 8 August 1994. The digits indicate (a) the number of larvae and – in parentheses – the cumulative number of emerged individuals and (b) the mean HW ± SD. The HW of the final instars remained in the dataset even after the emergence of the individuals.
Larval growth After hatching, the larvae of both species had similar HW (0.3 mm). Across the whole rearing period, the growth of E. cyathigerum larvae (mean HW) was faster and tended to be less synchronised than that of P. pennipes (Figure 5). After 40 days, there was no significant difference in mean HW between the species (t-test, t = 1.02, P = 0.311). However, after 80 days and after 120 days, the mean HW of E. cyathigerum was significantly higher than that of P. pennipes (ttests, t = 2.77, P = 0.008; t = 4.85, P < 0.001). One P. pennipes and six E. cyathigerum emerged during our experiment. This was 3.6% and 31.6% of the surviving individuals, respectively.
Discussion Our study indicates that the adaptation to the prevailing top-predators does not automatically determine the occurrence of species of Zygoptera. In the case of P. pennipes, the larvae are independent of fish predation; the constraints for the establishment of populations seem to be abiotic. In E. cyathigerum, fish predation seems to be of major importance for its occurence, whereas this species is tolerant to harsh abiotic condition – in this case oxygen lack. In contrast to other studies (see below), we could not detect any strong
173 effects of invertebrate predation on the species which is adapted to fish predation. Top predators are a main factor structuring the odonate community of freshwater ecosystems (Sih, 1987). Enallagma species from fish ponds are better adapted to fish predation than Enallagma species from fish free ponds (Blois-Heulin et al., 1990; McPeek, 1990a). In field enclosure-experiments, we found that in the presence of sticklebacks more larvae of P. pennipes survived than those of E. cyathigerum which were caught in a fish-free pond (Figure 1). Interpreting the effects of fish on odonate larvae one should take into account that the losses due to predation may depend on fish species and on substrate complexity (Dionne & Folt, 1991; Suhling, 1999). Most experiments dealing with fish predation on odonate larvae did not study the effect of more than one species of usually visually foraging fish (Blois-Heulin et al., 1990; McPeek, 1990b; Dionne & Folt, 1991; this study). Macan (1966) found that E. cyathigerum was able to survive the introduction of trout to a pond in zones densely covered by aquatic vegetation. Perca fluviatilis (L.) exerts a similar mortality of P. pennipes and E. cyathigerum (up to 90% in both species) (Steiner, 1995). However, we suppose that the higher survival of P. pennipes was caused particularly by behavioural adaptation against predation by fish, which may be corroborated by our behavioural experiments. Simulating a fish attack showed that in contrast to P. pennipes, most E. cyathigerum tried to escape. Moreover, P. pennipes was basically less active and, therefore, less conspicuous to visually hunting fish than the relatively active E. cyathigerum (Figure 4) Several studies describe that species co-occurring with fish show inactive behaviour, whereas those from fish-free ponds are more conspicuous to fish due to quick, short movements, swimming and the use of exposed habitats (e.g. Pierce, 1988; McPeek, 1990b). However, even E. cyathigerum reduces foraging behaviour in the presence of fish chemical stimuli (Koperski, 1997). We observed a reduction in activity of E. cyathigerum in the presence of fish, even though the fish could only be recognised visually or through vibrations (Figure 4). However, in E. cyathigerum the reduction of activity was less extreme than in P. pennipes. It is remarkable that both species stopped their abdominal waving in the presence of fish (Figure 4). This behaviour may be more conspicuous to fish than other activities. Besides swimming there is a respiratory function of the caudal lamella (Eriksen, 1986;
Burnside & Robinson, 1995). Abdominal waving may be a behaviour to support this function. We observed that in the presence of zooplankton prey this behaviour increased in both species. Richardson & Baker (1996) registered a positive correlation between feeding and abdominal waving in Ischnura verticalis, but did not find any influence of changed oxygen conditions on the frequency of abdominal waving. Abdominal waving may occur to supply higher oxygen demand only during digestion (see also Johnson, 1991). The activity patterns of E. cyathigerum and P. pennipes seem to be widely reflected in their predation success. Feeding on zooplankton E. cyathigerum was significantly more successful than P. pennipes. Moreover, the species differed in their effect on the prey composition: E. cyathigerum consumed proportionally more Cladocera and fewer Copepoda than P. pennipes (Figure 2). Other studies indicate that inactive odonate species are more successful in feeding on Copepoda than active ones (e.g. Johansson, 1992). Cladocera, in contrast, in our investigation were hunted more successfully by the more active predator than by the inactive one. Comparing predation at different zooplankton densities, we found that in the case of very low and very high availability of prey, there was no or little – but significant – difference in zooplankton reduction between the treatments with E. cyathigerum and P. pennipes. At medium zooplankton densities, the differences became evident. Our results may indicate different types of functional response (FR): the graph of E. cyathigerum corresponds with the FR of type 2 (see Chowdury et al., 1989); that of P. pennipes seems to correspond with type 3 (Figure 3). A type 3 response may result as a consequence of predators increasing their search rate as prey density increases (Johansson, 1992). This may be similar in P. pennipes. Due to this, their predation success is usually low and their development time may generally be longer than that of E. cyathigerum (see below), in which the food intake increases with its availability. Type 3 FR may have consequences for the regulation of zooplankton populations affected by predation (Begon et al., 1996). With a type 3 response at lower densities – in the case of P. pennipes below 3000 ind l−1 (Figure 4) – individuals at lower densities have less chance of being affected than individuals at higher densities, and this density dependence tends to stabilize the population dynamics. Zygoptera which perform type 2 response – like E. cyathigerum – would be more effective at lower prey densities, but do
174 not affect population dynamics at high prey density (Johnson et al., 1975). In our experiment, the growth of P. pennipes was slower than that of E. cyathigerum (Figure 5). One third of the latter emerged during the study period, first of them 82 days after deposition of the eggs. Though most of the larvae may be univoltine, we assume that due to high water temperature in the field, which ranged from 25 ◦ C to 38 ◦ C in 1994, at least some larvae should have been able to emerge in their first year. In P. pennipes, only a single individual emerged. In its natural habitat the species may generally be univoltine (Martens, 1996). Similar differences in development are described in the case of two north American Enallagma: E. aspersum, which live in fish-free ponds, overwinters in widely spread stages and has a univoltine life cycle, whereas due to cohort splitting, some larvae are bivoltine. The development of the fish pond dwelling E. hagenii is more synchronized (Ingram & Jenner, 1976). We expected an adaptation of E. cyathigerum to invertebrate predators. Enallagma-larvae from fish ponds suffered higher mortality due to dragonfly larvae than those from fish free ponds (Blois-Heulin et al., 1990; McPeek 1990b). Escaping behaviour as performed by E. cyathigerum in our fish attack experiment has been mentioned to compensate for the generally higher susceptibility to visually hunting dragonfly larvae. According to McPeek (1995), the caudal lamellae of Enallagma from fish-free ponds are broader than those from fish-ponds, which he interprets as an adaptation to escape invertebrate predators, e.g. dragonfly larvae. Consequently, we found that with Anax or Orthetrum – which are among to the top predators in our fish free pond B – E. cyathigerum was reduced to a lower extent than with fish, whereas the mortality of P. pennipes was higher with Anax than with fish. We also expected the mortality of E. cyathigerum due to dragonfly larvae to be lower than that of P. pennipes. However, we found no differences in predation by dragonflies. This result indicates that inconspicuous behaviour like that of P. pennipes may be effective in avoiding predation by dragonfly larvae as well. On the other hand, one may assume that the behavioural response to invertebrate predators is less developed in E. cyathigerum than in other Enallagma-species. Ischnura verticalis, which is able to survive with fish as well as with invertebrate predators can adopt both strategies but suffers higher mortality with both predators than the ‘specialists’
because its adaptations are less developed (McPeek, 1998). There is some evidence that in fish free ponds the pressure to develop efficient anti-predator behaviour is reduced because the importance of invertebrate predators is lower than that of fish (Benke, 1978; Pierce et al., 1985). So, in fish free ponds, other factors may play a determinative role instead, e.g. interspecific competition (Blois-Heulin et al., 1990; Wissinger, 1992) or harsh abiotic conditions. Under harsh abiotic conditions, biotic interaction generally seem to play a minor role (Peckarsky, 1983; Sih, 1987). Only few studies are known to us reporting on clear effects of physical or chemical stressors on odonates, e.g. acidic stress (Bell, 1971; Gorham & Vodopich, 1992), high temperatures (Martin et al., 1976), oxygen lack (Zahner, 1959; Miller, 1993) or pesticides (see Muirhead-Thomson, 1987). We found that only a very small minority of P. pennipes larvae was able to survive in pond B, whereas in the laboratory, the larvae did survive in water of the same pond. The main differences in abiotic water quality was the oxygen concentration which was near zero in pond B in August. P. pennipes seems to have a relatively high oxygen requirement during its development (see also Carchini & Rota, 1985). So, P. pennipes may generally not be able to develop in ponds with unpredictable periods of oxygen deflation, e.g. shallow polytrophic ponds or eutrophic lakes under ice cover during winter (see Martens, 1996). E. cyathigerum, on the other hand, possesses a remarkable tolerance against low oxygen availability – half of the larvae in our experiment survived – although it is not restricted to such types of habitats (see Macan, 1966; Johannsson, 1978; McPeek 1990a; Paterson, 1994). Thus, the occurence of fish and unpredictable periods of oxygen deflation appear to be relevant factors of sorting the two species into the proper habitats.
Acknowledgements We like to thank Berndt Strobach who kindly corrected the manuscript. Andreas Martens and Jens Rolff read drafts of the ms. Dan M. Johnson gave helpful comments on the ms. The work was partly supported by the Deutsche Forschungsgemeinschaft.
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