Life-history evolution when Lestes damselflies invaded vernal ponds

We know little about the macroevolution of life-history traits along environmental gradients, especially with regard to the directionality compared to the ancestral states and the associated costs to other functions. Here we examine how age and size at maturity evolved when Lestes damselflies shifted from their ancestral temporary pond habitat (i.e., ponds that may dry once every decade or so) to extremely ephemeral vernal ponds (ponds that routinely dry completely each year). Larvae of three species were reared from eggs until emergence under different levels of photoperiod and transient starvation stress. Compared to the two temporary-pond Lestes, the phylogenetically derived vernal-pond Lestes dryas developed more rapidly across photoperiod treatments until the final instar, and only expressed plasticity in development time in the final instar under photoperiod levels that simulated a later hatching date. The documented change in development rate can be considered adaptive and underlies the success of the derived species in vernal ponds. Results suggest associated costs of faster development are lower mass at maturity and lower immune function after transient starvation stress. These costs may not only have impeded further evolution of the routine development rate to what is physiologically maximal, but also maintained some degree of plasticity to time constraints when the habitat shift occurred.     

Life history plasticity to combined time and biotic constraints in Lestes damselflies from vernal and temporary ponds

Little is known about the ecological correlates and macro-evolution of life history plasticity to time constraints. Here, we compared age and mass at emergence and their plasticity toward combinations of time constraints (delayed larval development), food level and predation risk (caged dragonfly larvae) by rearing two temporary-pond Lestes damselflies ( L. congener and L. forcipatus ) and the derived vernal-pond L. dryas from the eggs until adult emergence in outdoor tubs. Life history plasticity under time constraints, low food and predation risk was as predicted by optimality models. Delayed larvae in all three species accelerated development and showed a lower fat content and a substantially elevated mortality rate. At low food, all species emerged later at a smaller mass. Also under predation risk adults of all species emerged later, and (at high food) at a smaller mass. Unexpectedly, delayed larvae did not show a smaller life history response to predation risk imposed by dragonfly larvae. Compared to the two temporary-pond Lestes studied, the derived species that invaded more ephemeral vernal ponds showed a faster development rate and a lower deceleration of development to low food. It also showed a lower acceleration of development to time constraints, possibly reflecting that it reached development rates near to its physiological maximum. Unexpectedly, the vernal-pond Lestes did not slow its development less under predation risk. Our results stress the importance of evaluating ecological and evolutionary correlates of life history plasticity under as realistic conditions as possible.     

Correcting the short-term effect of food deprivation in a damselfly: mechanisms and costs

1. Mass at emergence is a life-history trait strongly linked to adult fitness. Therefore, when faced with transient food shortage in the larval stage, mass-correcting mechanisms are common. 2. These correcting mechanisms may carry costs with them. On one hand, these costs may be overestimated because they can be confounded with the direct effects of the transient food shortage itself. On the other hand, costs may be underestimated by ignoring physiological costs. Another largely neglected topic is that correcting mechanisms and costs may critically depend upon other stressors that often co-occur. 3. Here, we identify the mass-correcting mechanisms and their associated costs at emergence in the damselfly Coenagrion puella, after being stressed by a transient period of starvation and a subsequent exposure to pesticide stress during the larval stage. We introduce path analysis to disentangle direct costs of starvation and the mass-correcting mechanisms in terms of immune response. 4. As predicted, we found no differences in mass at emergence. Starvation directly resulted in a costly delayed emergence and a decreased immune response at emergence. Mass-correcting mechanisms included a prolonged post-starvation period, reduced mass loss at emergence and compensatory growth, although the latter only in females under pesticide stress. 5. The mass-correcting mechanisms were associated with beneficial effects on investment in immune response, but only in the absence of pesticide stress. Under pesticide stress, these beneficial effects were mostly undone or overruled, resulting in negative effects of the mass-correcting mechanisms in terms of immune response. 6. Our results stress the importance of and introduce a statistical way of disentangling direct costs of starvation and the mass-correcting mechanisms themselves, and the importance of including physiological endpoints in this kind of studies.     

Short‐term larval food stress and associated compensatory growth reduce adult immune function in a damselfly

Abstract 1. In animals with a complex life cycle, larval stressors may carry over to the adult stage. Carry‐over effects not mediated through age and size at metamorphosis have rarely been studied. The present study focuses on the poorly documented immune costs of short‐term food stress both in the larval stage and after metamorphosis in the adult stage. 2. The present study quantified immune function [number of haemocytes, activity of prophenoloxidase (proPO) and phenoloxidase (PO)] in an experiment where larvae of the damselfly Lestes viridis were exposed to a transient starvation period. 3. Directly after starvation, immune variables were reduced in starved larvae. Levels of proPO and PO remained low after starvation, even after metamorphosis. In contrast, haemocyte numbers were fully compensated by the end of the larval stage, yet were lower in previously starved animals after metamorphosis. This can be explained as a cost of the observed compensatory growth after starvation. Focusing only on potential costs of larval stressors within the larval stage may therefore be misleading. 4. The here‐identified immunological cost in the adult stage of larval short‐term food stress and associated compensatory growth strongly indicates that physiological costs may explain hidden carry‐over effects bridging metamorphosis. This adds to the increasing awareness that the larval and adult stages in animals with a complex life cycle should be jointly studied, as trade‐offs may span metamorphosis.     

Compensatory growth and oxidative stress in a damselfly

Physiological costs of compensatory growth are poorly understood, yet may be the key components in explaining why growth rates are typically submaximal. Here we tested the hypothesized direct costs of compensatory growth in terms of oxidative stress. We assessed oxidative stress in a study where we generated compensatory growth in body mass by exposing larvae of the damselfly Lestes viridis to a transient starvation period followed by ad libitum food. Compensatory growth in the larval stage was associated with higher oxidative stress (as measured by induction of superoxide dismutase and catalase) in the adult stage. Our results challenge two traditional views of life-history theory. First, they indicate that age and mass at metamorphosis not necessarily completely translate larval stress into adult fitness and that the observed physiological cost may explain hidden carry-over effects. Second, they support the notion that costs of compensatory growth may be associated with free-radical-mediated trade-offs and not necessarily with resource-mediated trade-offs.     

Winter compensatory growth under field conditions partly offsets low energy reserves before winter in a damselfly

Despite the survival value of high energy reserves during winter, animals often face energy deficits when entering winter. Compensatory growth in energy reserves during the winter period to buffer such deficits may increase winter survival and alleviate the need for costly compensatory mechanisms before or after winter when predation risk is much higher. However, such compensatory responses in energy reserves during winter have not been demonstrated under field conditions. We explored if Lestes eurinus damselfly larvae can compensate for suboptimal energy reserves during winter at 4°C when their ponds are covered with ice. In a field enclosure experiment, we demonstrated compensatory growth in terms of body mass and energy reserves in larvae whose energy status was previously manipulated in the laboratory. These results were supported by patterns in body mass and energy reserves over winter in two natural unmanipulated populations. Winter survival was high overall and not affected by compensatory growth. We hypothesize that the observed compensatory growth in energy reserves during winter may shape life history decisions in autumn and spring, and may make resource availability during winter as or more important than energy reserves before winter.     

Life history responses depend on timing of cannibalism in a damselfly

1. Cannibalism has often been suggested as an important mechanism to reach the necessary developmental stage and size before a critical time horizon is reached, but this role has been largely unexplored. We studied effects of cannibalism on the life history of the damselfly Lestes viridis under combinations of a time constraint (by manipulating the perceived time available in the growth season) and a biotic constraint (density). 2. Larvae had a faster development and growth rate when reared at high time stress (late photoperiod). They also had a higher growth rate and mass at emergence when cannibalism occurred (density 2 and 4). Cannibalism occurred earlier at higher density. Accelerated life history responses (faster development and growth rate) and a higher mass at emergence were dependent upon the timing of cannibalism. Responses were more pronounced or only present if cannibalism occurred early in the larval period. 3. Our data suggest that cannibalism may not only act as a lifeboat mechanism by enabling cannibals to survive detrimental ecological conditions, but may also act as a compensatory mechanism to keep life history variables near‐optimal at life history transitions, even under sub‐optimal conditions.     

Perfectly nested or significantly nested – an important difference for conservation management

The trade off between age and size at emergence, which plays a central role in life history theory, is hypothesized to be more pronounced under stressful conditions, especially when these conditions are combined. Empirical evidence for this is equivocal. We tested the hypothesis by imposing combinations of two types of time stress (pond drying and late hatching date) in larvae of the damselfly Lestes viridis . Larvae from a temporary pond and a permanent pond population were reared in outdoor tubs from egg hatching until emergence. Unexpectedly, larvae did not accelerate their life history in response to simulation of pond drying. Instead, larvae reared in temporary tubs generally had a slower development and growth than larvae reared in permanent tubs. Probably deteriorating growth conditions in temporary tubs associated with higher densities and lower food levels caused this pattern. In agreement with a higher time stress in late hatched larvae, they generally had faster development and growth than larvae that hatched early in the season. Drying regime and hatching date shaped the covariation pattern between age and size at emergence, but the tradeoff was only apparent when time stress was relaxed. The tradeoff between age and size at emergence was only present in early hatched larvae, especially in permanent tubs (lowest time stress). Conversely, in late hatched larvae there was a strongly negative relationship between age and size at emergence, especially in temporary tubs (highest time stress). Our results support an alternative hypothesis that deteriorating growth conditions (i.e. pond drying) may decouple the tradeoff under time stress. The absence of a tradeoff in more time-stressed late hatched larvae can be explained by their higher intrinsic growth rates, independent of deteriorating growth conditions. We hypothesize that the pattern of less clear tradeoffs under the imposed types of time stress may be general.     

Photoperiod affects compensating developmental rate across latitudes in the damselfly Lestes sponsa

1. Although there is a great deal of theoretical and empirical data about the life history responses of time constraints in organisms, little is known about the latitude‐compensating mechanism that enables northern populations' developmental rates to compensate for latitude. To investigate the importance of photoperiod on development, offspring of the obligatory univoltine damselfly Lestes sponsa from two populations at different latitudes (53°N and 63°N) were raised in a common laboratory environment at both northern and southern photoperiods that corresponded to the sites of collection. 2. Egg development time was shorter under northern photoperiod regimes for both populations. However, the northern latitude population showed a higher phenotypic plasticity response to photoperiod compared with the southern latitude population, suggesting a genetic difference in egg development time in response to photoperiod. 3. Larvae from both latitudes expressed shorter larval development time and faster growth rates under northern photoperiod regimes. There was no difference in phenotypic plastic response between northern and southern latitude populations with regard to development time. 4. Data on field collected adults showed that adult sizes decreased with an increase in latitude. This adult size difference was a genetically fixed trait, as the same size difference between populations was also found when larvae were reared in the laboratory. 5. The results suggest phenotypic plasticity responses in life history traits to photoperiod, but also genetic differences between north and south latitude populations in response to photoperiod, which indicates the presence of a latitudinal compensating mechanism that is triggered by a photoperiod.     

Larval behavioral syndrome does not affect emergence behavior in a damselfly (<Emphasis Type="Italic">Lestes congener</Emphasis>)

Activity is a key behavioral trait that often mediates a trade-off between finding food for growth and evading predation. We investigated how activity of the damselfly Lestes congener is affected by larval state and predator presence and if larval behavioral type (BT) can be used to predict larval emergence behavior. Activity level of individual larvae was studied without predators at two different physiological states (hungry, fed) and in two predator treatments (familiar or unfamiliar predator cues). Larvae did not adjust their activity depending on state or when subjected to unfamiliar predator cues but a general reduction in activity was seen in the familiar predator treatment. Hence, active individuals remained active compared to their conspecifics, independent of state or predator treatment illustrating the presence of a behavioral syndrome. However, we found no correlation between larval BT and emergence behavior. Active individuals did not differ from less active individuals in any emergence characteristics. The results illustrate that the larval BT occurs in many situations keeping active larvae active even in maladaptive situations. Furthermore, we show that damselfly emergence behavior can be completely decoupled from larval BT, indicating a loss of stability in individual BT during critical stages in ontogeny.     

Compensating for delayed hatching reduces offspring immune response and increases life‐history costs

Organisms are exposed to multiple sources of stress in nature. When confronted with a stressful period affecting growth and development, compensatory responses allow the restoration of individual fitness, providing an important buffering mechanism against climatic and other environmental variability. However, tradeoffs between increased growth/development and other physiological traits are predicted to prevent these high growth and development rates from becoming constitutive. Here, we investigated how compensatory responses in growth and development affect immune responses. By using low temperature to stop embryonic development, we exposed moor frog Rana arvalis tadpoles to two levels of time‐constraints: non‐delayed hatching and 12‐day delayed hatching. In a common garden experiment, we recorded larval growth and development, as well as their immune response, measured as the inflammatory reaction after the injection of phytohaemagglutinin (PHA). Tadpoles originating from delayed hatching treatments had a lower immune response to PHA challenge than those from the non‐delayed hatching treatment. In general, tadpoles from the delayed hatching treatment reached metamorphosis faster and at a smaller size than control tadpoles. However, immune‐challenged tadpoles were not able to accelerate their development in response to delayed hatching. Our results indicate that 1) the innate immune response can be reduced in organisms undergoing compensatory developmental responses in growth and development and 2) compensatory capacity can be reduced when organisms are immunologically challenged. These dual findings reveal the complexity of handling multiple stressors and highlight the importance of examining the costs and limits of mounting an immune response in the context of increasing phenological instability ascribed to climate change.     

Integrating life history and physiology to understand latitudinal size variation in a damselfly

Our understanding of latitudinal life history patterns may benefit by jointly considering age and mass at maturity and growth rate. Additional insight may be gained by exploring potential constraints through pushing growth rates to their maximum and scoring physiological cost‐related variables. Therefore, we reared animals of a univoltine Spanish and Belgian population and of a semivoltine Swedish population of the damselfly Enallagma cyathigerum (spanning a latitude gradient of ca 2350 km) in a common environment from the eggs until adult emergence and exposed them to a transient starvation period to induce compensatory growth. Besides age and mass at maturity and growth rate we also scored investment in energy storage (i.e. triglycerides) and immune function (i.e. total activity of phenoloxidase). At emergence, body mass was greater in Spain and Sweden and lower in Belgium, suggesting a genetic component for the U‐shaped latitudinal pattern that was found also in a previous study based on field‐collected adults. The mass difference between univoltine populations can be explained by the shorter development time in the Belgian population, and this despite a higher growth rate, a pattern consistent with undercompensating countergradient variation. In line with the assumed shorter growth seasons, Belgian and Swedish animals showed higher routine growth rates and compensatory growth after transient starvation. Despite a strong link with metabolic rates (as measured by oxygen consumption) populations with higher routine growth rates had no lower fat content and had higher immune function (i.e. immune function decreased from Sweden to Spain), which was unexpected. Rapid compensatory growth did, however, result in a lowered immune function. This may contribute to the absence of perfect compensating countergradient variation in the Belgian population and the lowest routine growth rates in the Spanish population. Our results underscore the importance of integrating key life historical with physiological traits for understanding latitudinal population differentiation.     

Cannibalism-mediated life history plasticity to combined time and food stress

There is increasing awareness that combinations of biotic and time stress interact in shaping life history plasticity. Despite being widespread and abundant, the role of cannibalism in linking both types of constraints to life history plasticity has been largely neglected. Moreover, no studies disentangled direct (due to the extra meal) and indirect (due to the elimination of the competitor) life history effects of cannibalism, and little is known about their differential dependency on these constraints. We studied effects of cannibalism on the life history of the damselfly Lestes viridis under combinations of time stress (by manipulating the perceived time available in the growth season) and food stress. We reared larvae per two and disentangled direct and indirect effects of cannibalism by preventing cannibalism in half of the cups and by manipulating the per capita food increase after cannibalism. Cannibalism was more frequent under both time stress and food stress and our results show it may help cannibals to compensate for the negative effects of these constraints imposed on life history. Both direct and indirect benefits of cannibalism (increased development and growth rates, larger mass at emergence) were dependent on the timing of cannibalism, being more pronounced or only present when cannibalism occurred early. Moreover, we found that the ecological constraints (time stress and food stress) also differentially shaped some of the direct and indirect effects. Given the differential context-dependency of direct and indirect effects and the fact that direct and indirect life history effects may be both important in shaping life history, disentangling these effects is critical to mechanistically understand under which conditions cannibalism is expected to be adaptive or not.     

Evolutionary and Ecological Effects of Multi-Generational Exposures to Anthropogenic Stressors

Biological and ecological responses to stress are dictated by duration and frequency, as well as instantaneous magnitude. Conditional compensatory responses at the physiological and behavioral levels, referred to as ‘acclimation’, may mitigate effects on individuals experiencing brief or infrequent periods of moderate stress. However, even modest stress over extended periods may reduce the fitness of some or all exposed individuals. In this way, specific stress that persists over multiple generations will increase probabilities for extinction of populations composed of sensitive individuals. For populations whose members demonstrate variance and heritability for stressor response, this selective loss of sensitive individuals may result in populations dominated by resistant individuals. The formation of these ‘adapted’ populations may be considered an ecological compensatory mechanism to multi-generational stress. Paradoxically, the biological costs to individuals of toxicity and physiological acclimation may result in obvious signs of stress in affected wildlife populations while the costs of genetic adaptation may be more covert. It is important to consider such costs because recent evidence suggests that anthropogenic stressors have acted as powerful selection agents that have modified the composition of wildlife populations subjected for successive generational exposures to specific stressors. This essay focuses on a case study where adaptation has been demonstrated in fish populations with a history of chronic exposure to persistent, bioaccumulative and toxic environmental contaminants. Because the magnitude, breadth and long-term outcomes of such changes are unknown, ecological risk assessments that are limited in focus to short-term exposures and consequences may seriously underestimate the ecological and evolutionary impacts of anthropogenic stressors.     

Comparison of compensatory growth responses of juvenile three-spined stickleback and minnow following similar food deprivation protocols

The compensatory growth responses of individual juveniles of two co- existing species were compared after identical periods of starvation to determine inter-specific similarities and differences. The carnivorous stickleback Gasterosteus aculeatus was compared with the omnivorous minnow Phoxinus phoxinus. Both species experienced 1 or 2 weeks of starvation before being re-fed ad libitum. The two species differed in their response to the starvation periods, with minnows showing a lower weight-specific loss. Both species showed compensatory responses in appetite, growth and to a lesser extent, growth efficiency. Minnows wholly compensated for 1 and 2 weeks of starvation. At the end of the experiment, sticklebacks starved for 2 weeks were still showing a compensatory response and had not achieved full compensation. The compensatory responses of the sticklebacks showed a lag of a week before developing in the re-feeding phase, whereas the response of the minnows was immediate. Analysis of lipid and dry matter concentrations suggested that the compensatory response restored reserve lipids while also bringing the fish back to the growth trajectory of continuously fed fish.     

Photoperiod and variation in life history traits in core and peripheral populations in the damselfly Lestes sponsa

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Indirect Monitoring of Agonistic Encounters in Larvae of Lestes viridis (Odonata: Lestidae) Using Exuviae Lamellae Status

Differences in interference competition between larvae of the damselfly Lestes viridis (Vander Linden) were examined using caudal lamellae status of exuviae. Exuviae from a small temporary fishless pond near Antwerp (Belgium) where L.viridis was the only odonate present were studied. No lamellae loss during emergence was seen. Therefore, the lamellae status of the exuviae reflects the lamellae status of the final instar larvae. The deviations of the distribution of the number of missing lamellae per individual from a binomial distribution suggested that lamellae are not always lost separately or that some animals are more prone to agonistic encounters. I found no difference in agonistic encounters between sexes. In accordance with the hypothesis of Pierce et al. (1985) interference competition was higher in the lestid species inhabiting small, temporary fishless ponds than in the coenagrionid damselfly Ischnura posita inhabiting large permanent fish containing water bodies that was studied by Robinson et al. (1991).