The effect of temperature on the interaction between larvae of a native and a range
expanding dragonfly species
Sanne Everling
Degree project inbiology, Master ofscience (2years), 2021
Abstract
Climate change might affect the distribution of species; therefore, it is important to anticipate the imminent impact of climate change. Even though climate responses have the potential to affect species interactions, most models on the effect of climate change on species distribution assume that species respond to climate individually. Hence studies on competition effects are needed. In this study, I estimated growth, mortality, and behaviour (prey capture success, activity, exploration and boldness) at 20° C and 23° C at intra- and interspecific competition conditions in larvae of a native and a northward dispersing dragonfly. The results showed that the northward expanding Sympetrum fonscolombii had a higher growth and survival rate compared to the native Sympetrum vulgatum at interspecific conditions. At intraspecific conditions the results showed that temperature had no significant effect on the performance of S. fonscolombii, but S. vulgatum showed both a higher growth rate and a higher mortality at 23
° C. A significant difference between temperatures within prey capture success rate was found in S. vulgatum only, during the second observation period. There was a correlation between activity and exploration in both species, between prey capture success rate and activity during the third observation round in S. vulgatum, and between prey capture success rate and boldness during the first observation round in S. fonscolombii. No other behaviours were correlated. Prey capture success rate was shown to be repeatable in both species, while boldness was repeatable in S. vulgatum only. The behavioural results suggests that behavioural traits are relatively plastic over ontogeny in both species, possibly caused by behavioural variation within each instar. Additionally, boldness, but not activity and exploration, might aid S. fonscolombii in their northward expansion. The majority of these results were similar at both temperatures and indicate that S. fonscolombii has a higher capacity to tolerate climate change, and their presence might negatively impact the performance of S. vulgatum.
Table of Contents
1. Introduction ... 1
2. Materials & Methods ... 3
2.1. Study organisms ... 3
2.2. Experimental design ... 3
2.3. Growth and mortality ... 4
2.4. Behavioural experiments ... 5
2.5. Statistical analyses ... 5
2.5.1. Growth & survival ... 5
2.5.2. Behaviour ... 6
3. Results ... 7
3.1. Effect of species and temperature on growth ... 7
3.1.1. Growth intraspecific ... 7
3.1.2. Growth interspecific ... 7
3.1.3. Growth individually ... 8
3.2. Effect of species and temperature on survival ... 8
3.2.1. Intraspecific ... 8
3.1.1. Interspecific ... 9
3.2. Relationship between survival and growth ... 10
3.3. Larval behaviour ... 10
3.3.1. Species differences ... 10
3.3.2. Temperature differences ... 12
3.3.3. Correlations between behaviours ... 12
3.3.4. Behaviour repeatability ... 13
4. Discussion ... 14
4.1. Survival ... 14
4.2. Growth ... 15
4.3. Behaviour ... 16
4.4. Conclusion ... 18
Acknowledgements ... 18
5. References ... 18
1. Introduction
Climate change has been shown to have a large impact on species abundance and distribution (Carlton, 1985; Grosholz, 2002; Witte et al., 2010). We have, however, little understanding on how these changes affect interaction among species. Most models assume that species respond to climate independently of each other (Gilman et al., 2010; Van der Putten et al., 2010), even though climate responses are often driven by species interactions (Park, 1954; Davies et al, 1998). However, Cahill et al. (2012), concluded that most well understood climate-induced extinctions involved indirect species interactions, instead of direct physiological impacts. It is therefore important to include species interactions in order to improve our ability to anticipate changes to current populations (Urban et al., 2017). Additionally, climate change is a large driver in the establishment of invasive species (Witte et al., 2010; Clausnitzer, 2013). This establishment may impose many negative effects on the native species due to their interaction with the invasive species (Strayer et al., 2006; Tylianakis et al., 2008).
In ectotherms, temperature has a significant impact on the metabolic rate (Gillooly et al., 2001), which in turn influence for example growth and development (Angilletta & Dunham, 2003).
This response impacts higher levels of ecological organisations (Kingsolver & Woods, 1997;
Brown et al., 2004; Angilletta, 2009; Woodward et al., 2010; Dell et al., 2011; Buckley &
Kingsolver, 2012; Dell et al, 2014). Since species differ in their physiology and phenological responses to climate change, the future climate scenario effect on species distribution can differ between species. More specifically, changes in phenology will vary with the ontogeny of interacting species, resulting in size difference, which in turn alters predation and competition levels between e.g., native and invasive species (Parmesan, 2007; Both et al., 2009; Yang &
Rudolf, 2010).
Temperature also affects an organism’s behaviour, such as activity. Organisms will move more slowly in colder temperatures, due to the deceleration of metabolic processes (Brown et al.
2004, Dell et al. 2011). In contrast, warming might increase biochemical reactions, allowing faster movement, and thus increasing contact between consumer and resource. This often results in an increased interaction strength at higher temperatures (Jiang and Morin, 2004; Rall et al., 2010; Kratina et al., 2012; Novich et al., 2014).
Interestingly, the encounters between predators and prey might also depend on the foraging mode of the organisms. It has been suggested that temperature may play little to no role in predator-prey interaction strength in sit-and-wait predators (Novich et al., 2014). The reason being that sit-and-wait predators do not move while searching for prey, as such their velocity will be the same at any temperature (Novich et al., 2014). Even though their attack speed does increase with temperature, capture success itself is influenced by accuracy instead of velocity and might therefore be affected by temperature (Quenta Herrera et al., 2018). Other behaviours, such as exploration (Biro & Stamps 2010; Réale et al. 2010; Pruitt et al. 2011) and aggression (Biro et al, 2010; Pruitt et al., 2011) have been shown to increase with temperature as well.
Behavioural syndromes are a set of correlated and/or consistent behavioural traits across multiple situations in a population (Sih et al., 2004; Sih & Bell, 2008; Dingemanse et al., 2010;
Sih et al., 2012). For example, behavioural syndromes encompassing both high exploration and boldness are common (Wilson & Godin, 2009; Mazué et al., 2015). These correlations imply a limitation in behavioural plasticity and have been suggested to be caused by genetic correlations among these traits (Wilson, 1998; Sih et al., 2004; Sih & Bell, 2008), which might result in a constraint on the evolution of behaviour. However, in some environments behavioural correlations can provide selective advantages as well (Dall et al. 2004;
Dingemanse and Réale 2005). For example, Dingemanse et al. (2007) found that populations of the three-spined stickleback showed within-population positive associations between aggressiveness and boldness under strong predation pressure, but populations under low predation pressure show no correlations between these traits. However, less is known about how abiotic stressors such as temperature affects behavioural syndromes.
Ontogeny is the development of an organism from the egg stage until maturation. Both behaviour (Hinde, 1970) and preferred temperature (Abdullah, 1961) may change over ontogeny. For example, activity might be influenced by size (Werner & Anholt, 1993), as smaller juveniles will reduce their activity to a greater degree than larger individuals (Stein &
Magnuson 1976; Lawler 1989). Brodin et al. (2006) found that predator diet influenced prey activity in damselfly larvae, but this effect was only present early in ontogeny. Additionally, Hopkins et al. (2011) found that older dragonfly larvae display significantly more aggressive behaviour towards predators than younger larvae. This illustrates the importance of considering the development of an organism during their study. Furthermore, very few studies have examined the effect of temperature on behaviour over ontogeny.
Temperature has been demonstrated to influence behavioural response e.g. in the larvae of several odonate species (Suhling & Suhling, 2013; Frances & McCauley, 2018). The aquatic dragonfly larvae are well suited to address the effects of warming on interactions and behaviour, as their response to temperature changes have been reflected in e.g. development (Frances et al., 2017), growth (Suhling et al., 2015), and phenology (McCauley et al. 2015).
Furthermore, dragonfly larvae both compete for prey and prey on each other, in other words, they are intraguild predators (Polis et al., 1989). Therefore, understanding the effects of temperature on multiple traits, such as growth, mortality, behaviour and competition, may provide insight into the rate with which climate change will affect interactions among species.
This study focussed on the interaction between two odonate species, the native Sympetrum vulgatum and the invasive Sympetrum fonscolombii. In order to understand how the two species interact, mortality and growth were measured at intra- and interspecific level at two different temperatures. Additionally, behavioural experiments were conducted to assess the influence of temperature and competition on activity, exploration, boldness and prey capture.
Larvae of both species are sit-and-wait predators and thus have zero velocity while they search
temperature, as organisms with higher metabolic rate need more food in order to keep up with increased energetic demands (Elliott, 1976). Furthermore, the increased temperature should lead to increased activity in the prey animals, leading to higher predation rates (Lima & Dill, 1990; Werner & Anholt, 1993). Lastly, increased intraguild predation (Frances & McCauley, 2018) may lead to higher mortality rates at higher temperatures. The behaviours studied might help for a mechanistic interpretation of the potential temperature driven changes in interactions within and between species.
2. Materials & Methods
2.1. Study organisms
S. vulgatum and S. fonscolombii both inhabit the wetlands of Europe, breeding in a wide range of standing waters (Boudot et al. 2009, Kalkman, 2010). S. vulgatum is a common and widespread dragonfly species in central and northeast Europe, including Sweden. It has a large distribution, extending eastwards to China and Japan. In the most southern countries of Europe, the species is mainly confined to higher elevations (Boudot et al. 2009, Kalkman, 2010). S.
fonscolombii is commonly found in Africa, southern Europe, the Middle East, Central Asia, the Indian Subcontinent and the Indian Ocean Islands. The species used to be less common in the Northern Hemisphere, however, during the last decades its range has extended significantly and by now S. fonscolombii is common in most of central Europe. It has been found on the island of Öland in Sweden in 2013, and was predicted to keep extending its range as climate change continues (Clausnitzer, 2013). Indeed, S. fonscolombii has been found as far north as the region of Umeå in 2018 and 2019 (Artportalen, 2021).
2.2. Experimental design
Two kinds of experiment were performed: one competition experiment and one behavioural experiment. The competition experiment was performed at two temperatures: 20 °C and 23 °C.
The larvae from the behavioural experiments were reared at 20 °C and 23 °C as well, while all behavioural observations were performed at 20 °C.
Eggs from the two species were collected in the summer prior to the start of the project.
The eggs of S. vulgatum were collected August 12, 14 and 17 in Uppsala (43.475105°N, 4.818020°E.). The eggs of S. fonscolombii were collected the 3d of September in France (43.597955, 4.472223). Eggs were collected by dipping the abdomen of females in a glass jar with water upon which females released their eggs. After eggs had been collected they were transported to a laboratory at Uppsala University, Department of Animal Ecology, where they were kept at 20 °C and a day light cycle at 14:10 (light:dark). The eggs from S. vulgatum were kept at this temperature for 3 weeks after which they were moved to a walk-in climate room with a temperature of 4 °C and no light. This treatment simulates winter conditions which are needed to stimulate egg hatching in the spring. After the three weeks these eggs were moved back to the laboratory with 20 °C and a day light cycle at 14:10. Eggs from S. fonscolombii do not need simulated winter conditions to stimulate egg hatching and were therefore kept in the lab until all eggs had hatched.
The eggs of S. fonscolombii started hatching on the 13th of September. The intraspecific competition experiment with S. fonscolombii ran from October 5 till November 11, while the larvae for the behavioural experiments of the same species were reared from October 8 till December 25. The three rounds of behavioural observations were conducted on October 12/16, November 16/20 and December 21/25. The eggs of S. vulgatum started hatching on the 19th of October. Their intraspecific competition ran from November 11 till December 29, while the larvae for the behavioural experiments of the native species were reared from October 30 till January 14. Three rounds of behavioural experiments were conducted on November 2/5, December 7/10 and January 11/14. Lastly, the interspecific competition experiment ran from October 26 till December 12.
For the competition experiments the larvae were reared at a density of 10 individuals with either a mix of the two species (5 + 5: interspecific) or a single species (intraspecific) in small plastic containers with a diameter of 18.5 cm. The containers were filled with 1.5L conditioned water and 15 stems of grass were added to simulate natural vegetation. Thus a 2 (temp.) x 3 (interaction) experimental design was used. The intraspecific experiment including S.
fonscolombii had 15 replicates per temperature, the intraspecific experiment including S.
vulgatum had 12 replicates per temperature, and the intraspecific experiment involving both species had 10 replicates per temperature. Growth and mortality were checked throughout the experiment.
For the behavioural experiments, larvae were placed individually into small plastic cups with a diameter of 7 cm, filled with 100 mL of conditioned water and a small piece of a grass stem.
The small containers were placed into larger plastic containers (18.5 cm diameter) in order to prevent them from floating around freely. The behaviour of 44 S. fonscolombii and 33 S.
vulgatum larvae was measured on three separate occasions.
The containers and the plastic cups in the competition and behavioural experiment respectively were kept in water baths set to the experimental temperatures. Each bath had length of 145 cm, depth of 55 cm and hight of 15 cm and was filled with water unto 7-8 cm. Lights were providing from above with led light (6400 K, 2200 lumen). Three baths were used per temperature and containers and cups were rotated among the baths and within batch randomly with a two weeks cycle.
2.3. Growth and mortality
Growth and mortality of the larvae from the competition experiment were recorded after 17 days and at the end of the experiment, day 34. To estimate growth larval head width was measured. This was done by placing the larvae in a petri dish with a piece of graph paper as a reference. Larvae where then photographed, and head width was estimated from photos using the software ImageJ v.1.53. Head width was estimated as the distance between the other part of the eyes and was used as the size of the larvae. At the end of the interspecific competition experiment mortality was estimated as the number of survivors of each species. Species were
identified by comparing the presence and size of dorsal and lateral spines in the larvae (Askew, 2004).
2.4. Behavioural experiments
Three types of behaviours, prey capture, activity and boldness, were estimated on three separate occasions: during the start, the middle, and the end of the experiment.
For the prey capture trials, the larvae were placed in a petri dish with a diameter of 8.8 mm and given three minutes to acclimate. The petri dish was filled with conditioned water and kept at an ambient temperature of 20 °C. After three minutes, 100 artemia were added in order to exceed the amount of prey that is generally consumed (Frances & McCauley, 2018). The number of prey consumed per larvae was noted for 5 minutes. The larvae were not fed before the start of the trial for a period of at least 24 hours.
For the activity trial, a 1x1 cm coordinate grid was attached to the bottom of an experimental plastic container with a diameter of 17 cm. The container was filled with 0,5 L conditioned water. The larva was placed in the middle of the container and given three minutes to acclimate, after which the position of the head within the two-dimensional grid was recorded every 10 minutes for 180 minutes (Johansson, 2000). All activity trials were conducted from 12:30 till 15:30.
In order to measure boldness, the larvae were placed in a petri dish with a diameter of 8.8 cm and given three minutes to acclimate, after which they were gently flipped on their back.
Thereafter, the time until they start moving was measured. The larvae were observed for a maximum of five minutes, after which the observation was terminated if no movement had occurred. All larvae were fed at least an hour before the start of both the boldness and the activity trials.
2.5. Statistical analyses
All statistical analyses were conducted in R v. 1.2.1335.
2.5.1. Growth & survival
The growth rate was quantified as log(final size) – log(initial size). A two-way Anova was used to test for differences in growth within the interspecific competition experiments, and a two- way Anova for unequal sample size was used to test for differences in growth within the intraspecific competition experiment and the individual larvae. In both cases temperature and species were set as independent variables. An independent t-test was used to test for the effect of temperature within S. vulgatum.
Survival was defined as the number of surviving larvae per bucket at the end of the experiment.
To test for differences in survival between treatments, a binomial two-way Anova was conducted, with temperature and species as independent variables.
Linear regression models were used to test for the relationship between growth and survival within the intra- and interspecific competition experiments.
2.5.2. Behaviour
For the activity and exploration traits, total distance travelled and percentage of grid covered were calculated using custom source code (Wyckmans, 2021)
Mann-Whitney U tests were used to test for differences between species and temperature in all four behaviours. Tests with species as a variable were run for each observation period independently, while tests with temperature as a variable were run for each observation period within each species independently.
To test for correlations between all four behaviours, a Spearman’s rank correlation test was performed per observation period per species.
To test for behavioural change over ontogeny, a Friedman test was performed for each behaviour per species per temperature, with time as repeated measure variable.
3. Results
3.1. Effect of species and temperature on growth 3.1.1. Growth intraspecific
Growth in the intraspecific competition experiment was higher in S. fonscolombii and it ranged from 0.95 to 1.58 in 20° C and 1.01 to 1.69 in 23° (Fig 1). In S. vulgatum it ranged from 0.91 to 1.36 in 20° C and 1.08 to 1.67 in 23° C (Fig 1a). The ANOVA results showed no significant effect of species or temperature, but the interaction term between temperature and species was significant (Table 1a), suggesting that S. vulgatum had a higher growth rate at 23 °C. This was supported by a significant effect of temperature in this species (p<0.001: Independent t-test).
Figure 1. The growth per larvae in each treatment combination: species and temperature.
Growth is defined as log(final size in mm) - log(initial size in mm).
3.1.2. Growth interspecific
Within the interspecific competition experiment, growth ranged from 1.64 to 1.98 in 20° C and 1.50 to 2.08 in 23° C in S. fonscolombii (Fig 1b). In S. vulgatum growth ranged from 1.41 to 1.58 in 20° C, and in 23° C there was only one surviving S. vulgatum, with a growth of 1.81 (Fig 1b). The Anova showed a non-significant interaction effect. When this interaction effect was dropped, there was a significant species effect, but no significant temperature effect, suggesting that S. fonscolombii was growing faster at both temperatures (Table 1b).
Table 1. Results of Two-way Anova on growth rate
Variable Sum. Sq. Df F-value P-value
1. Intraspecific
Species 0.0647 1 1.7219 0.1956
Temperature 0.0336 1 0.8674 0.3562
Species*Temperature 0.1556 1 4.1407 <0.05
Residuals 1.8414 49
2. Interspecific
Species 0.1549 1 4.8461 <0.05
Temperature 0.0027 1 0.0832 0.7760
Residuals 0.6392 20
3. Individual larvae
Species 0.364 1 7.7729 <0.01
Temperature 0.003 1 0.0618 0.8043
Residuals 3.462 72
3.1.3. Growth individually
The individual larvae growth ranged from 1.14 to 2.05 in 20° C and 1.13 to 2.16 in 23° C within S. fonscolombii, while it ranged from 1.12 to 1.82 in 20° C and 1.30 to 1.76 within 23° C in S.
vulgatum (Fig. 1c). There was no significant interaction effect and hence the interaction term was dropped. The Anova showed that temperature had no significant effect on growth while species was significant (Table 1c). Thus, S. fonscolombii grew significantly faster compared to S. vulgatum at both temperatures in the absence of competitors.
3.2. Effect of species and temperature on survival 3.2.1. Intraspecific
Survival ranged from one to four larvae in 20 ° C and 1 to 5 larvae in 23° C within S.
fonscolombii in the intraspecific competition experiment (Fig 2a). The survival of S. vulgatum ranged from 2 to 5 larvae in 20° C and 1 to 3 larvae in 23° C in the intraspecific competition experiment (Fig 2b). The Anova showed that the interaction was non-significant. After removing the interaction, there was no significant species or temperature effect on survival (Table 2a). However, a significant effect of temperature was found within S. vulgatum separately (t-test: p<0.05), suggesting that S. vulgatum had lower mortality at 20° C.
3.1.1. Interspecific
Survival of both species within the interspecific competition experiment ranged from 1 to 2 larvae in 20° C and 1 to 3 larvae in 23° C (Fig 2c). After removing the non-significant interaction between species and temperature, the Anova showed that there was a significant species effect, but no significant temperature effect (Table 2b), suggesting that S. fonscolombii had a higher survival rate.
Table 2. Results of binomial Anova’s on survival within the intra- and interspecific competition experiments.
Variable Df Chi-sq. P-value
a) Intraspecific
Species 1 1.1775 0.2779
Temperature 1 1.6840 0.1944
b) Interspecific
Species 1 14.4876 <0.001
Temperature 1 1.1328 0.2396
Figure 2. The number of surviving larvae at the end of the experiment per treatment combination: species and temperature.
3.2. Relationship between survival and growth
Growth was strongly negatively correlated with the number of surviving larvae within all treatment combinations, except for the interspecific competition experiment at 23° C (Table 3). This suggest that larvae grew faster without competitors.
Table 3. The correlation between growth and number of surviving larvae within each treatment combination and the corresponding p-value, obtained correlation tests.
Correlation P-value Interspecific 20° C -0.807 <0.01 Interspecific 23° C -0.558 0.093 S. fonscolombii
Intraspecific 20° C -0.696 <0.01 Intraspecific 23° C -0.765 <0.001 S. vulgatum
Intraspecific 20° C -0.763 <0.01 Intraspecific 23° C -0.827 <0.001
3.3. Larval behaviour
3.3.1. Species differences
A Mann-Whitney U tests found a significant difference between species in the second period of boldness observations (p<0.05), but not during the first and third observation periods.
Suggesting S. fonscolombii was bolder than S. vulgatum during the second period of observations (Fig. 3a-c).
No significant difference between species was found within prey capture success rate in any of the observation periods (p>0.05: Fig 3d-f).
There was a significant difference between species in activity during the first (p<0.001) and second period of observations (p<0.05), but not during the third observation period, suggesting that S. vulgatum was more active than S. fonscolombii during the first and second observation periods (Fig. 3g-i).
Lastly, according to the Mann-Whitney U tests there was a significant difference between species in the first exploration observations (p<0.001), but no significant difference between the second and third observation periods, suggesting that S. vulgatum had a higher exploration rate than S. fonscolombii during the first period of observations (Fig. 3j-l).
Figure 3. Larval behaviour of both species at both temperature treatments. Four behaviours were observed (boldness, prey capture success rate, activity and exploration) at three periods in time with approximately five weeks between each observation period.
3.3.2. Temperature differences
The Mann-Whitney U tests showed no significant difference between temperatures for boldness, activity and exploration in all behavioural observation periods in any of the species (p<0.05: Fig 3).
The Mann-Whitney U tests showed no significant difference between temperatures for prey capture success rate in S. fonscolombii during any of behavioural observation periods (p>0.05:
Fig 3d-f). However, there was a significant difference between temperatures for prey capture success rate in S. vulgatum during the second observation period (p<0.05), but not during the first and third period of observations, suggesting that S. vulgatum larvae had a higher success rate at 23° C during the second observation period (Fig. 3e).
3.3.3. Correlations between behaviours
The Spearman rank correlation tests showed a significant correlation between prey capture success rate and boldness in the first observation period in S. fonscolombii (Table 4a).
Additionally, the tests showed a significant correlation between prey capture success rate and activity in S. vulgatum in the third observation period (Table 4f). Lastly, the correlation tests showed a significant correlation between exploration in activity in all observation periods in both species (Table 4).
Table 4. Correlation between the four behaviours (boldness, prey capture success rate, activity and exploration) in each species during all three observation periods. Significant correlations are indicated in bold.
S. fonscolombii Boldness Success rate Activity Exploration
a) Observation Boldness - 0.38 -0.17 -0.05
period 1 Success rate - -0.02 -0.01
Activity - 0.83
Exploration -
b) Observation Boldness - 0.05 0.03 0.00
period 2 Success rate - 0.09 0.23
Activity - 0.77
Exploration -
c) Observation Boldness - 0.09 0.07 0.09
period 3 Success rate - -0.11 -0.06
Activity - 0.75
Exploration -
S. vulgatum
d) Observation Boldness - -0.10 0.16 0.06
period 1 Success rate - 0.10 0.27
Activity - 0.85
Exploration -
e) Observation Boldness - -0.08 0.31 0.12
period 2 Success rate - 0.03 0.23
Activity - 0.67
Exploration -
f) Observation Boldness - 0.20 0.08 0.04
period 3 Success rate - 0.40 0.13
Activity - 0.60
Exploration -
3.3.4. Behaviour repeatability
The Friedman tests found a significant difference between all observation periods for boldness in S. fonscolombii in 20° C and 23° C (p<0.001), but not in S. vulgatum in either temperature, suggesting that the behaviour boldness was only repeatable over time in the latter species (Fig 3).
The Friedman tests found no significant difference between observation periods for prey capture success rate in both S. vulgatum and S. fonscolombii in either temperature, suggesting that this behaviour was repeatable over time for both species (Fig. 3).
Lastly, the Friedman tests found a significant difference between observation periods in activity and exploration in both temperatures for S. fonscolombii (activity 20° C & 23° C: p<0.001;
exploration 20° C & 23° C: p<0.001) and S. vulgatum (activity 20° C: p<0.01; 23° C p<0.001;
exploration 20° C & 23° C: p<0.001) respectively, suggesting that both behaviours were not repeatable over time for either of the species (Fig. 3).
4. Discussion
The results showed that the northward expanding Sympetrum fonscolombii had a higher growth rate and a higher survival compared to the native S. vulgatum at interspecific conditions. This result is important because, despite the large impact of temperature on numerous life-history traits (Pétavy et al., 2001; Clarke, 2006; Angiletta, 2009; Fischer & Karl, 2010), many studies have neglected how climate change will affect species interaction. In fact, most climate models assume that species respond to climate independently (Gilman et al., 2010; Van der Putten et al., 2010). Furthermore, climate change is largely responsible for the introduction of invasive species (Witte et al., 2010; Clausnitzer, 2013), possibly increasing competitive interactions for many native organisms (Strayer et al., 2006; Tylianakis et al., 2008). By measuring growth, mortality, and behaviour at two different temperatures in intra- and interspecific competition settings, I was able to provide a mechanistic explanation of temperature driven changes within and between a native and northward dispersing odonate species in growth and survival.
4.1. Survival
Within the intraspecific competition experiments, the results showed no significant effect of temperature on survival in S. fonscolombii, but a significant temperature effect was found for S. vulgatum, indicating that mortality only increased with temperature in the latter species. This might suggest that S. fonscolombii has a greater capacity to acclimate, which is supported by previous studies that indicate acclimation is stronger in mid-latitude taxa (Nilsson-Örtman et al., 2013; Nilsson-Örtman & Johansson, 2017). Research has shown that the effect of intraspecific competition on multiple life history traits is strongly dependent on temperature (Ritchie, 1996; Laws & Belovsky, 2010, Amarasekare & Coutinho, 2014). For example, studies have indicated that cannibalism increases with temperature in damselflies (Start et al., 2017; Sniegula et al., 2019).
When the two species were reared together, i.e. simulating what would happen when the northward expanding S. fonscolombii encounters S. vulgatum in north Europe, results showed a significantly higher survival rate for S. fonscolombii in the interspecific competition experiment, suggesting that the presence of a novel competitor negatively impacts S. vulgatums performance. Current research is slowly uncovering the extent of the interaction between temperature and indirect effects caused by other species within a community (Davis et al., 1998; Suttle et al., 2007; Tylianakis et al., 2008; Gilman et al., 2010; González-Megías &
Menéndez, 2012; Liancourt et al., 2013). A similar result as mine was discovered in another dragonfly pair comparison by Suhling & Suhling (2013), who found that a northern dragonfly
temperature competition effects have been established in other organism groups as well. For example, Alexander et al. (2015) showed that the performance of alpine plants that were transplanted into warmer climates experienced a greater decrease due to novel competitors compared to current competitors. Comeault and Matute (2021) found that two Drosophila sister species performed similarly in isolation, however, when experiencing interspecific competition, temperature caused performance disparity. A similar effect was found by Vafeiadou and Moens (2021) who established that interspecific competition had a negative effect on fitness and behaviour at multiple temperatures within marine nematodes, with a stronger effect at the highest temperature. Taken together, my results and the cited studies suggest that that at increasing temperatures the presence of a competitor species may alter a species’ ability to tolerate environmental change.
4.2. Growth
There was no significant effect of species and temperature on growth in the intraspecific competition experiments, except for the significant effect of temperature on growth in S.
vulgatum. There was, however, a significant interaction term between temperature and species.
These results suggest that S. vulgatum had a higher growth rate a 23 °C, but both species perform comparable under both temperature regimes. This higher growth rate was not an indirect effect of mortality since mortality was not higher in S. vulgatum compared to S.
fonscolombii at 23 °C.
At the interspecific and individual rearing conditions, there was a significant species effect, but no temperature effect, indicating that S. fonscolombii was growing faster at both temperatures.
In addition, there was no significant interaction effect between temperature and species in interspecific and individual conditions, suggesting that S. fonscolombii had a growth advantage at both temperatures. Lastly, there was a significant correlation between survival and growth in nearly all treatment combinations, except for the interspecific competition experiment at 23°
C, suggesting that the larvae grew faster as the number of competitors went down.
In ectotherms, temperature has a large influence on performance such as growth and development (Angilletta & Dunham, 2003). The relationship between performance and temperature is described as the thermal performance curve, with peak performance at the organisms optimal temperature (Huey & Stevenson, 1979; Huey & Kingsolver, 1989). Since species differ in their thermal performance curves, the species might differ in the shape of their curves. This might explain why a growth increase at the higher temperature was observed in S.
vulgatum at the intraspecific conditions, but not in S. fonscolombii. An alternative explanation could be the increased activity level in S. vulgatum during the first two observation periods. A higher level of activity might lead to an increased energy expenditure, in turn leading to a lower level of growth.
Interestingly, S. fonscolombii had a higher growth rate at both temperatures when larvae were grown individually, i.e. without competitors. This suggests that the higher growth rate in S.
fonscolombii might have led to size advantage and increased predation at the interspecific
conditions, which would explain the higher mortality on S. vulgatum. My results support Suhling & Suhlings (2013) findings, who also showed a reduced growth rate of a native dragonfly species in the presence of a northward expanding competitor. These results imply that if S. fonscolombii continues to expand its range, S. vulgatum might experience a significant decrease in population size regardless of temperature increase.
My results showed very few significant interactions between temperature and species on both growth and survival in the interspecific competition experiments, suggesting that S.
fonscolombii outperforms S. vulgatum at both temperatures. Since the purpose of my study was to predict the effect of this range expansion specifically, I used northern range S. vulgatum and southern range S. fonscolombii larvae. However, both species do occur together in central Europe, even though S. vulgatum becomes relatively rare towards central and southern Europe (Boudot et al., 2009; Kalkman, 2010; Clausnitzer, 2013). Studies have shown that temperature adaption occurs along a latitudinal gradient (Irlich et al., 2009; Nilsson-Örtman et al., 2013), therefore, competition between two southern populations of both species might show a different result.
4.3. Behaviour
My results indicated that S. fonscolombii was significantly bolder during the second period of observations, while S. vulgatum was significantly more active during the first and second period of observations, but only had a higher exploration rate during the first observation period. Some studies suggest when predation risk is increased, reduced boldness is favoured (Lawler, 1989; Smith & Blumstein, 2007; Carter et al., 2010), while others indicate no relationship (Bell & Sih, 2007; Carlson & Langkilde, 2014) or a positive relationship between survival and boldness (Godin & Davis, 1995; Smith & Blumstein, 2010). My results would support the latter, because S. fonscolombii had a higher growth rate and survival in the presence of competitors, which are potential predators (cannibals). Additionally, reduced activity can be a behavioural modification to avoid predation (Stoks et al., 2003; Suhling et al., 2005), suggesting that the lower activity level in S. fonscolombii may have attributed to their lower mortality. It would have been interesting to compare these behaviours in the presence and absence of competitors, since such a comparison would inform about the adaptive contribution of these behaviours.
Interestingly, prey capture success rate showed no significant differences between species in either of the observation periods. This suggests that the difference in growth rate observed did not have a direct effect on prey capture, even though other studies have found that species do differ in prey capture rate (Johansson & Suhling, 2004).
There was no significant difference between temperatures for boldness, activity and exploration in any of the species. Several studies have found an increase in boldness with temperature (Biro et al., 2010; Forsatkar et al., 2016), but White et al. (2020) found no significant temperature effect on boldness. Studies have also shown conflicting results on the
positive correlation between the two (Gannon et al., 2014; Start et al., 2017), while Frances and McCauley (2018) found no change in activity with increasing temperature in several dragonfly species. This indicates that temperature driven behavioural change is species specific. It also indicates that the relationship between behaviour and temperatures might be related to where on the thermal performance curve the experimental temperature used in the experiments are situated. S. vulgatum did have a significantly higher prey capture success rate at 23° C, but only during the second observation period.
The results showed a strong correlation between activity and exploration during all observation periods in both species. Additionally, correlations were found between prey capture success rate and activity during the third observation round in S. vulgatum, and between prey capture success rate and boldness during the first observation round in S. fonscolombii. Thus, I found that some correlations where similar between species while other correlations differed between species. Previous studies have shown that boldness, activity and exploration are associated (Cote et al., 2010), and connected to dispersal (Dingemanse et al., 2003; Hoset et al., 2011).
For instance, Monceau et al. (2015) found evidence for a correlation between activity, exploration and boldness in both a native and invasive hornet species, however, the invasive species outperformed the native species for each behavioural trait. Interestingly, the higher activity and exploration by S. vulgatum suggests that the boldness-activity-exploration syndrome is not present in either species. In other words, if higher boldness is observed in S.
fonscolombii, one would also expect them to express higher activity and exploration if a boldness-activity-exploration syndrome were to be present. Furthermore, activity and exploration seem not to be related to dispersal since the dispersing species performed lower in both traits.
The results indicated that boldness was repeatable in S. vulgatum, while prey capture success rate turned out to be repeatable in both species. Consistent individual behavioural differences have been found in many different animals (Clark & Ehlinger, 1987; Gosling, 2001; Bell, 2007), including insects (Sih & Waters, 2005). Ectotherms are often less repeatable in behavioural traits compared to endotherms, likely due to their higher sensitivity to their environment (Bell et al., 2009). The propensity to express higher boldness in S. fonscolombii larvae would be consistent with studies that have showed a correlation between boldness and dispersal (Dingemanse et al., 2003; Hoset et al., 2011), as they are dispersing northward. In addition, it would be interesting to examine whether the observed higher boldness in the larval stage would be expressed in the adult stage as well, as Brodin (2009) found that boldness carries over from the larval into the adult stage. However, larvae only expressed higher boldness during the second observation period, suggesting that the behavioural trait is relatively plastic.
Similarly, S. vulgatum expressed a higher level of activity during the first and second observation period, while they only expressed a higher level of exploration during the first observation period, indicative of plasticity in both behavioural traits. One explanation for the plasticity in behaviour over ontogeny in the larval stage could be that larval behaviour fluctuates over the course within an instar. A more accurate way of estimating repeatability over ontogeny would therefore be to perform behavioural observations e.g. after a certain time frame after a change to a new instar has occurred.
4.4. Conclusion
S. fonscolombii might have a greater capacity to tolerate climate change, given their similar mortality rate at both temperatures, whereas S. vulgatum showed a higher mortality at an increased temperature. In addition, the outperformance by S. fonscolombii in both temperatures, both in growth and survival, adds to a growing body of research showing that native species’ performance decreases in the presence of a novel competitor (Suhling &
Suhling, 2013; Alexander et al., 2015; Comeault & Matute, 2021; Vafeiadou & Moens, 2021).
This suggests that if S. fonscolombii continues to expand northward, S. vulgatum might be significantly negatively impacted. The results on behavioural correlation and plasticity suggest that boldness, and not activity and exploration, might aid S. fonscolombii in their northward dispersal. An interesting continuation of the work and results found by in this study, would be including the effect of intra- and interspecific competition on behaviour. In this study, behavioural observations were conducted on individual larvae. However, the presence of competitors might significantly impact behavioural traits, giving further insight in the effect of behaviour on growth and survival which potentially could affect a species’ range expansion.
Acknowledgements
First of all, I thank Frank Johansson, my supervisor, for his great guidance and feedback throughout this project. I would also like to thank Philippe Lambret, for collecting the S.
fonscolombii eggs in France. To my other colleagues, I would like to thank you for your warm welcome. The occasional fika has served me well. Lastly, a special thanks to both my parents and my partner, who have always provided me with love and moral support when I needed it.
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