Damselfly Enallagma Research Articles

Synergistic effects between pesticide stress and predator cues: Conflicting results from life history and physiology in the damselfly Enallagma cyathigerum

There is increasing awareness that the negative effects of anthropogenic stressors may be magnified in the presence of natural stressors. Very few of these studies have included physiology, yet including physiological studies may help learning about the mechanistic base of such synergisms at the life history level and identify synergistic interactions not translated in life history traits. We studied in Enallagma cyathigerum damselfly larvae potential synergistic effects between exposure to the pesticide glyphosate and predator cues on a key life history trait, growth rate, its associated behavioural trait, food intake, and three types of physiological traits known to be affected by both stressors in isolation: the stress protein Hsp70, energy storage and variables related to oxidative stress and damage. The pesticide and predator cues reduced growth rate in an additive way. Food intake increased under pesticide exposure and was not affected by the predator cues, indicating physiological mediation of the growth reduction. One potential physiological mechanism was that both stressors additively increased Hsp70 levels, this may also have contributed to the reduced levels of total carbohydrates when exposed to predator cues. Chronic exposure to predator cues reduced oxygen consumption, possibly to avoid too high costs of an increased metabolic rate. This reduction did not occur in the presence of the pesticide, reflecting the need for energetically expensive defence mechanisms (such as Hsp70 upregulation). When both stressors were combined, there was a reduction of the antioxidant enzyme superoxide dismutase activity (SOD) and an associated increase of oxidative damage in lipids. While synergistic interactions were not present for growth rate and food intake, they were identified for antioxidant defence and oxidative damage. This novel type of “hidden” synergistic interaction may have profound fitness implications, and when ignored will lead to underestimations of the impact of pollutants in natural populations where predators are omnipresent.

Substratum associations and depth distribution of benthic invertebrates in saline Walker Lake, Nevada, USA

Walker Lake, a terminal salt lake in western Nevada, is undergoing rapid changes because of falling lake level and rising salinity, affecting the potential habitat of benthic invertebrates that supply food to native fish and birds. Benthic invertebrate surveys were conducted within different substratum size classes and macrophyte beds in the nearshore littoral shallows ( 10 m) zones of the lake. Samples were dominated by the chironomid midges Cricotopus ornatus and Tanypus grodhausi; the damselfly Enallagma clausum; and an oligochaete worm of the genus Monopylephorus. Midges showed distinct depth preferences, with Cricotopus found primarily in the shallow littoral, and Tanypus found in the lower littoral and profundal regions. Enallagma occurred throughout the littoral region but was reduced in abundance below 10 m. Cricotopus and Enallagma were most abundant on cobble rock substratum and macrophytes. Sand and small gravel substrata supported few invertebrates except oligochaetes, which were most common in shallow littoral areas. The extent of Ruppia beds was determined using hydroacoustic sounding and showed that these beds were most well-developed in a zone from 1.25 to 5 m depth. The estimated area of productive shallow littoral zone habitat at different lake levels showed that coverage was lowest near the current surface elevation. Rising lake levels would result in expansion of suitable habitat area, and while falling levels could also expand nearshore habitat, this would likely occur on areas of poorer substratum quality and under high salinities that may inhibit growth.

Preference of larvae of Enallagma cyathigerum (Odonata: Coenagrionidae) for habitats of varying structural complexity

In macrophyte-rich lentic ecosystems, higher numbers of damselfly larvae occur in areas where there is structurally complex vegetation than in those where the plant architecture is relatively simple. Biotic interactions rather than morphological constraints are considered to underlie this pattern. We investigated whether the preference of the larvae of the damselfly Enallagma cyathigerum for a particular habitat was retained in absence of prey, predators and/or conspecifics. A series of laboratory choice experiments was conducted in which combinations of sediment and artificial plants differing in structural complexity were offered simultaneously to the larvae. Larvae preferred patches with structurally complex vegetation over patches with simply structured vegetation or lacking vegetation. Patches with simply structured vegetation were preferred over those with bare sediment, but the number of larvae showing a clear choice, which is regarded as an indication of the strength of the preference for a particular habitat, was relatively low compared to the number of individuals responding when complex vegetation was present. Based on the results presented, we conclude that the preference of E. cyathigerum larvae for structurally complex vegetation is independent of the presence of predators, prey or competitors. This suggests that this behaviour of the larvae is either learned or an innate response.

How does a pesticide pulse increase vulnerability to predation? Combined effects on behavioral antipredator traits and escape swimming

An increasing number of studies have documented that sublethal pesticide exposure can change predator–prey interactions. Most of these studies have focused on effects of long-term pesticide exposure on only one type of antipredator traits and have not directly linked changes in these traits to mortality by predation. To get a better mechanistic understanding of how short-term pesticide pulses make prey organisms more vulnerable to predation, we studied effects of 24h exposure to a sublethal concentration of the insecticide endosulfan and the herbicide Roundup on the major antipredator traits and the resulting mortality by predation in larvae of the damselfly Enallagma cyathigerum. A pulse of both pesticides affected antipredator traits involved in avoiding detection by predators as well as traits involved in escape after detection. After a pesticide pulse, larvae increased activity levels and even further increased the number of walks when predation risk was present. Further, an endosulfan pulse tended to reduce escape swimming speed. In contrast, previous exposure to Roundup caused the larvae to swim faster, yet less often when attacked. Importantly, although both studied pesticides induced maladaptive changes in overall activity, only for endosulfan this resulted in an increased mortality by predation. Our study highlights that considering changed predator–prey interactions may improve ecological risk evaluations of short pesticide pulses, yet also underscores the need (1) to consider effects on all important antipredator traits of the prey as trait compensation may occur and (2) to effectively score the outcome of predator–prey interactions in staged encounters.

Regional divergence and mosaic spatial distribution of two closely related damselfly species (Enallagma hageniandEnallagma ebrium)

North American Enallagma damselflies radiated during the Pleistocene, and species differ mainly by reproductive structures. Although morphologically very different, Enallagma hageni and Enallagma ebrium are genetically very similar. Partitioning of genetic variation (AFLP), isolation by distance and clustering analyses indicate that these morphospecies are locally differentiated genetically. Spatial analyses show that they are rarely sympatric at local sites, and their distributions form a mosaic of patches where one is clearly dominant over hundreds of square kilometers. However, these morphospecies are also not genetically more similar when they are sympatric, indicating that hybridization is probably not occurring. Given that these morphospecies are ecologically equivalent, strong assortative mating, reproductive interference and fast post-glacial recolonization may explain the origin and maintenance of these distributional patches across eastern North America. By limiting opportunities for gene flow, reproductive interference may play an unsuspected role in accelerating genetic differentiation in the early phases of nonecological speciation.

Sexual selection and temporal phenotypic variation in a damselfly population

Temporal variation in selection can be generated by temporal variation in either the fitness surface or phenotypic distributions around a static fitness surface, or both concurrently. Here, we use within- and between-generation sampling of fitness surfaces and phenotypic distributions over 2 years to investigate the causes of temporal variation in the form of sexual selection on body size in the damselfly Enallagma aspersum. Within a year, when the average female body size differed substantially from the average male body size, male body size experienced directional selection. In contrast, when male and female size distributions overlapped, male body size experienced stabilizing selection when variances in body size were large, but no appreciable selection when the variances in body size were small. The causes of temporal variation in the form of selection can only be inferred by accounting for changes in both the fitness surface and changes in the distribution of phenotypes.

Survival selection imposed by predation on a physiological trait underlying escape speed

Summary 1. In contrast to other phenotypic traits, selection on physiological traits remains largely undocumented. We have evaluated survival selection imposed by predation by dragonflies on the activity of arginine kinase (Ak), a key enzyme delivering energy for escape performance in invertebrates. 2. To accomplish this, we conducted a semi‐natural field enclosure experiment in which we manipulated predation by large dragonfly predators, and quantified escape swimming speed and Ak in the prey, the damselfly Enallagma vesperum. To avoid confounding selection on Ak with selection on other swimming speed‐related variables, we also scored all morphological and behavioural traits thought to underlie swimming speed in these damselflies. 3. Dragonfly predators imposed considerable mortality and selected for faster swimming speed and higher activity levels of Ak. Furthermore, higher Ak levels contributed to higher swimming speeds, confirming the mechanistic role of Ak for escape performance. Although morphological (size of the caudal lamellae which generate trust) and behavioural (number of beats made by the abdomen during swimming and the start angle of the C‐start) variables contribute to increasing swimming speed, we detected no selection on these variables. This may be due to functional redundancy. 4. Taken together, our results indicated selection on Ak and suggested that selection on physiological traits may be as strong as selection on morphology and life history traits.

SPECIES RECOGNITION AND PATTERNS OF POPULATION VARIATION IN THE REPRODUCTIVE STRUCTURES OF A DAMSELFLY GENUS

The selection pressures imposed by mate choice for species identity should impose strong stabilizing selection on traits that confer species identity to mates. Thus, we expect that such traits should show nonoverlapping distributions among closely related species, but show little to no variance among populations within a species. We tested these predictions by comparing levels of population differentiation in the sizes and shapes of male cerci (i.e., the clasper structures used for species identity during mating) of six Enallagma damselfly species. Cerci shapes were nonoverlapping among Enallagma species, and five of six Enallagma species showed no population variation across their entire species ranges. In contrast, cerci sizes overlapped among species and varied substantially among populations within species. These results, taken with previous studies, suggest that cerci shape is a primary feature used in species recognition used to discriminate conspecific from heterospecifics during mating.

Fish predation selects for reduced foraging activity

Despite the importance of foraging activity for the growth/predation risk trade-off, studies that demonstrated predator-induced survival selection on foraging activity under semi-natural conditions are relatively rare. Here, we tested for fish-induced selection for reduced foraging activity in two larval Enallagma damselflies using a field enclosure experiment. Fish imposed considerable mortality in both damselfly species and survival selection on foraging activity could be detected in Enallagma geminatum. We did not detect selection in Enallagma hageni, probably because this species already was not eating very much in the absence of fish compared to E. geminatum. Both species responded strongly to the presence of predators by reducing their foraging activity. The documented survival selection on foraging activity was detected despite the already low activity levels in fish lake prey species and despite strong predator-induced plasticity in this trait.

Exposure to perfluorooctane sulfonic acid (PFOS) adversely affects the life-cycle of the damselfly Enallagma cyathigerum

We evaluated whether life-time exposure to PFOS affects egg development, hatching, larval development, survival, metamorphosis and body mass of Enallagma cyathigerum (Insecta: Odonata). Eggs and larvae were exposed to five concentrations ranging from 0 to 10 000 μg/L. Our results show reduced egg hatching success, slower larval development, greater larval mortality, and decreased metamorphosis success with increasing PFOS concentration. PFOS had no effect on egg developmental time and hatching or on mass of adults. Eggs were the least sensitive stage (NOEC = 10 000 μg/L). Larval NOEC values were 1000 times smaller (10 μg/L). Successful metamorphosis was the most sensitive response trait studied (NOEC < 10 μg/L). The NOEC value suggests that E. cyathigerum is amongst the most sensitive freshwater organisms tested. NOEC for metamorphosis is less than 10-times greater than the ordinary reported environmental concentrations in freshwater, but is more than 200-times smaller than the greatest concentrations measured after accidental releases.

Survival selection on escape performance and its underlying phenotypic traits: a case of many‐to‐one mapping

Selection often operates not directly on phenotypic traits but on performance which is important as several traits may contribute to a single performance measure (many-to-one mapping). Although largely ignored in the context of selection, this asks for studies that link all relevant phenotypes with performance and fitness. In an enclosure experiment, we studied links between phenotypic traits, swimming performance and survival in two Enallagma damselflies. Predatory dragonflies imposed survival selection for increased swimming propensity and speed only in E. annexum; probably E. aspersum was buffered by the former species' presence. Accordingly, more circular caudal lamellae, structures involved in generating thrust while swimming, were selected for only in E. annexum. Other phenotypic traits that contributed to swimming speed were apparently not under selection, probably because of many-to-one mapping (functional redundancy). Our results indicate that not only the phenotypic distributions of syntopic prey organisms but also many-to-one mapping should be considered when documenting phenotype-performance-fitness relationships.

Variation in flight morphology in a female polymorphic damselfly: intraspecific, intrasexual, and seasonal differences

In aerial animals, flight morphology needs to be designed to allow daily behavioural activities. Within species differences in behaviour can therefore be expected to relate to differences in flight morphology, not only between males and females but also between same-sex members when they use different behavioural strategies. In female polymorphic damselflies, one female morph is considered a male mimic that resembles the male’s body colour and behaviour (andromorph), whereas the other is dissimilar (gynomorph). Here, we questioned whether males, andromorphs, and gynomorphs of the damselfly Enallagma cyathigerum (Charpentier, 1840) differ in flight morphology, with andromorphs being more similar to males than gynomorphs. In addition, we evaluated whether differences in flight morphology are consistent or whether some morphs are more plastic in response to seasonal environmental fluctuations. Most morphometrics showed similar seasonal plasticity for males and both female morphs, which could only partly be explained from allometry. Consistent with high manoeuvrability in flight, males had broader wings and lower wing loading than females. Variation between female morphs was less pronounced, with no consistent differences in length, aspect ratio, total surface, and wing loading. However, we detected morph-specific differences in shape and width, with andromorphs having broader wings than gynomorphs similarly to males.

Female morphs of a colour polymorphic damselfly differ in developmental instability and fecundity

Abstract Sex-limited colour polymorphism occurs in several animal taxa and is usually explained in the context of sexual selection. Specifically, for polymorphism restricted to the female sex, multiple phenotypes may have evolved in response to male harassment. Such male harassment is generally considered to entail differential costs to female morphs, which may ultimately result in fitness differences. However, contrary to this prediction, most previous studies do not support that female morphs (andromorphs and heteromorphs) differ in measures of quality and (or) fitness components. In this study, we evaluate quality and fitness differences between mated female morphs of the damselfly Enallagma cyathigerum. We suggest that many earlier studies may have failed to observe morph differences in quality or fitness because selection by male harassment was weak. Here, we selected a study population for which our expectation was that levels of per female capita male harassment were high. Nevertheless, also in this population mated female morphs did not differ in body size or condition (body mass/body length). However, mated female morphs did differ in levels of developmental instability: heteromorphs consistently showed a higher level of fluctuating asymmetry than andromorphs. Also, mated female morphs differed in fecundity: andromorphs had a lower clutch size than heteromorphs. In addition, larger females contained more eggs, but the slope of this relationship was steeper in heteromorphs. In conclusion, mated female morphs of the damselfly E. cyathigerum at our study site clearly differed in one quality estimate (developmental instability) and in our measure of fitness (fecundity).

Behaviour of damselfly larvae ( Enallagma cyathigerum) (Insecta, Odonata) after long-term exposure to PFOS

Perfluorooctane sulfonic acid (PFOS) is a persistent and ubiquitous environmental contaminant that has been detected in organisms worldwide. Here, we evaluate whether long-term (1 and 4 months) exposure to PFOS contamination affects the behavioural performance of freshwater larvae of the damselfly Enallagma cyathigerum (Insecta: Odonata). Our results show reduced behavioural performance with increasing PFOS concentration. In 1 month exposed larvae, no observed effect concentrations (NOECs) were 100 μg/L for general activity. In 4 months exposed larvae, NOECs were 10 μg/L, for each behavioural trait, except swimming acceleration of male larvae where the NOEC was 100 μg/L. When faced with PFOS concentrations above the NOEC, E. cyathigerum larvae were less active, less capable to escape a simulated predator attack and less efficient in foraging. Together, our results show that damselfly larvae suffer reduced survival-related behavioural performance.

MODELING THREE-DIMENSIONAL MORPHOLOGICAL STRUCTURES USING SPHERICAL HARMONICS

Quantifying morphological shape is a fundamental issue in evolutionary biology. Recent technological advances (e.g., confocal microscopy, laser scanning, computer tomography) have made the capture of detailed three-dimensional (3D) morphological structure easy and cost-effective. In this article, we develop a 3D analytic framework (SPHARM-spherical harmonics) for modeling the shapes of complex morphological structures from continuous surface maps that can be produced by these technologies. Because the traditional SPHARM methodology has limitations in several of its processing steps, we present new algorithms for two SPHARM processing steps: spherical parameterization and SPHARM registration. These new algorithms allow for the numerical characterization of a much larger class of 3D models. We demonstrate the effectiveness of the method by applying it to modeling the cerci of Enallagma damselflies.

The conspicuousness of colour cues in male pond damselflies depends on ambient light and visual system

The colours of male coenagrionid damselflies have been interpreted by some as intraspecific signals that reduce intrasexual harassment by advertising the unprofitability of pursuing conspecific males as potential mates. As visual cues, male colours should be conspicuous to other males under the specific light environments where males search for females. We tested this prediction by using spectroradiometry and two models of damselfly colour vision to determine the chromatic and achromatic contrast of males from six species of Enallagma damselflies with pond backgrounds under the ambient light conditions when each species was most active. The males of five species were active at the time when their colour was most conspicuous against aquatic vegetation. Three blue species were most active and attained their highest levels of contrast during midday, while species that became active in late afternoon or evening reflected longer wavelengths and increased in brightness contrast under low sun angles. A sixth species, Enallagma pictum, departed from this pattern. We propose that colour may serve as a signal of both sexual and species identity among males.

Predation risk induces stress proteins and reduces antioxidant defense

Summary 1Despite its wide ecological relevance, we know little about the physiological mechanisms underlying the growth vs. mortality by predation trade-off. Here, we test for two costly, potential physiological correlates of the fight-or-flight response that may contribute to the growth reduction under predation risk: induction of stress proteins (Hsp60 and Hsp70) and of antioxidant enzymes (superoxide dismutase, SOD and catalase, CAT), in larvae of the damselfly Enallagma cyathigerum. 2Under predation risk, there was a growth reduction and an increase in oxygen consumption, indicative of the fight-or-flight response. Predation risk did not affect Hsp60 levels but induced an increase in energetically costly Hsp70 levels. 3Under predation risk, levels of SOD remained constant and those of CAT decreased. Together with the increase in respiration, this should inevitably result in oxidative stress. 4Our results suggest that induction of stress proteins may contribute to the partly physiologically mediated growth reduction under predation risk and that oxidative stress is a novel cost of predation risk that may have important long-term negative fitness consequences for the prey. The latter adds to the recent insight that costs of stressors and life-history trade-offs may not always directly operate through increased energy consumption and differential allocation, but, may also work through the increased production of reactive oxygen species.

The Tempo and Mode of Three‐Dimensional Morphological Evolution in Male Reproductive Structures

Various evolutionary forces may shape the evolution of traits that influence the mating decisions of males and females. Phenotypic traits that males and females use to judge the species identify of potential mates should evolve in a punctuated fashion, changing significantly at the time of speciation but changing little between speciation events. In contrast, traits experiencing sexual selection or sexually antagonistic interactions are generally expected to change continuously over time because of the directional selection pressures imposed on one sex by the actions of the other. To test these hypotheses, we used spherical harmonic representations of the shapes of male mating structures in reconstructions of the evolutionary tempo of these structures across the history of the Enallagma damselfly clade. Our analyses show that the evolution of these structures is completely consistent with a punctuated model of evolutionary change and a constant evolutionary rate throughout the clade's history. In addition, no interpopulation variation in shape was detected across the range of one species. These results indicate that male mating structures in this genus are used primarily for identifying the species of potential mates and experience little or no selection from intraspecific sexual selection or sexual antagonism. The implications of these results for speciation are discussed.

Effects of phenotypic variation onto body temperature and flight activity in a polymorphic insect

Abstract According to biophysical principles, colour and size are important phenotypic factors that may influence body temperature and activity in ectothermic insects. In taxa showing female‐limited polymorphism, males and female morphs differ in body colour, size and activity pattern. However, no previous study has evaluated whether such phenotypic and behavioural variation relates to differences between males and female morphs in thermal properties. In the present study, the relationships between body colour, size, activity and body temperature are examined under laboratory and field conditions, for the polymorphic damselfly Enallagma cyathigerum (Charpentier, 1840) (Odonata: Zygoptera). Contrary to expectation, males and female colour morphs of this species do not differ in thermal properties (i.e. heating characteristics or field body temperatures). When questioning phenotype and activity, temperature does not appear to be relevant for understanding the maintenance of female‐limited polymorphism.

Effects of Chemical Cues on Foraging in Damselfly Larvae, Enallagma antennatum

Animals experiencing a trade-off between predation risk and resource acquisition must accurately predict ambient levels of predation risk to maximize fitness. We measure this trade-off explicitly in larvae of the damselfly Enallagma antennatum, comparing consumption rates in the presence of chemical cues from predators and injured prey. Damselflies distinguished among types of chemical cues based on species of prey injured or eaten. Injured coexisting heterospecific and unknown heterospecific chemical cues did not reduce foraging relative to starved predator cues, while cues arising from predators eating a coexisting heterospecific did decrease foraging. This study shows a cost in terms of reduced foraging in response to chemical cues and further defines the ability of prey to respond discerningly to chemical cues.