Differential Water Mite Parasitism,Phenoloxidase Activity,and Resistance to Mites Are Unrelated across Pairs of Related Damselfly Species

Related host species often demonstrate differences in prevalence and/or intensity of infection by particular parasite species, as well as different levels of resistance to those parasites. The mechanisms underlying this interspecific variation in parasitism and resistance expression are not well understood. Surprisingly, few researchers have assessed relations between actual levels of parasitism and resistance to parasites seen in nature across multiple host species. The main goal of this study was to determine whether interspecific variation in resistance against ectoparasitic larval water mites either was predictive of interspecific variation in parasitism for ten closely related species of damselflies (grouped into five “species pairs”), or was predicted by interspecific variation in a commonly used measure of innate immunity (total Phenoloxidase or potential PO activity). Two of five species pairs had interspecific differences in proportions of individuals resisting larval Arrenurus water mites, only one of five species pairs had species differences in prevalence of larval Arrenurus water mites, and another two of five species pairs showed species differences in mean PO activity. Within the two species pairs where species differed in proportion of individuals resisting mites the species with the higher proportion did not have correspondingly higher PO activity levels. Furthermore, the proportion of individuals resisting mites mirrored prevalence of parasitism in only one species pair. There was no interspecific variation in median intensity of mite infestation within any species pair. We conclude that a species’ relative ability to resist particular parasites does not explain interspecific variation in parasitism within species pairs and that neither resistance nor parasitism is reflected by interspecific variation in total PO or potential PO activity.     

Grooming decisions by damselflies, age-specific colonisation by water mites, and the probability of successful parasitism.

We examined whether host damselflies (Ischnura verticalis) in different stages of development were differentially susceptible to parasitism by larval water mites (Arrenurus pseudosuperior). We found that mites were successful in reaching the parasitic phase more often if they colonised hosts closer to emergence. Thus, we predicted that more mites should colonise damselflies closer to emergence and damselflies closer to emergence should spend more time defending against mites. We found that mites colonised damselflies closer to emergence in one of two experiments, but that damselflies in different stages of development did not differ in time spent defending against mites.     

Parasite-host associations and life cycles of spring-living water mites (Hydrachnidia, Acari) from Luxembourg

Larval water mites are parasites of various insect species. The main aim of the present study was to analyse the host range of spring dwelling water mites. The investigation focuses on seven spring sites in Luxembourg. Some 24 water mite species were recorded either from the benthos or as parasites attached to flying insects captured in emergence traps. For 20 mite species 35 host species from four Nematocera (Diptera) families were recorded. About 80% of the host species and over 90% of the host individuals were Chironomidae, the others were Limoniidae, Dixidae and Simuliidae. For all water mite species recorded we present the observed host spectrum and/or potential hosts as well as the intensity of parasitism and the phenology of the mites. For 10 mite species the hosts were previously unknown. For another ten species the known host spectrum can be confirmed and extended. The host spectrum ranged from one host species (e.g. for Sperchon insignis) to at least 10 host species (for Sperchon thienemanni, Ljania bipapillata), but the effective host range could not be definitively estimated due to the lack of corresponding data. The hypothesised host preference of the water mites, of which most are strictly confined to spring habitats, for similarly spring-preferring hosts could not be proven. The mean intensity of parasitism was highest for Thyas palustris (10.8 larvae/host) and lowest for Sperchon insignis and Hygrobates norvegicus (1.2 larvae per host for each). The hydryphantid mite Thyas palustris occurred at maximal intensity (41 larvae per host) and the two abdominal parasites Ljania bipapillata and Arrenurus fontinalis showed higher mean intensities than the thoracic parasites did. Larval water mites parasitising chironomids did not exhibit a preference for host sex. The phenology of the larval mite species was varied, some species were only present in samples early in the year and others exclusively in the summer. Another species showed two peaks of occurrence, springtime/early summer and late summer/autumn. In conclusion, the water mite larvae in the studied springs showed differences in host spectra and phenology but there are no clear evidences in both for host partitioning. Maybe, the relative low species diversity of water mites in individual springs and the low inter-specific competition for suitable hosts in combination with the high host abundances and species richness makes springs such favourable habitats for the mites.     

Are sexes equally parasitized in damselflies and dragonflies?

Parasitism plays an essential part in ecology and evolution of host species and understanding the reasons for differential parasitism within and among hosts species is therefore important. Among the very important factors potentially affecting parasitism is the gender of the host. Here, we studied whether either females or males are more likely to harbour parasites among Odonatan insects, by relying on an extensive literature review and new field data. We collected data on numerous dragonfly and damselfly species and their ectoparasites (water mites) and endoparasites (gregarines) to examine the generality of similarities and differences in prevalence, intensity and maximum number of parasites of male and female hosts. We found three main results. Firstly, most of the odonate host species showed no differences between sexes in either gregarine or water mite prevalence and intensity. The only exception was female damselflies’ higher gregarine prevalence and intensity compared to conspecific males. These inequalities in gregarine parasitism may be due to behavioral and physiological differences between conspecific males and females. In comparison, there were no differences in dragonflies between sexes in water mite or gregarine prevalence and intensity. Secondly, damselflies had higher prevalence and intensity levels of both gregarine and water mite parasites compared to dragonflies. Finally, we found a strong species level pattern between female and male parasitism: a certain level of gregarine or water mite parasitism in one sex was matched with a similar parasitism level for the other. This indicates similar exposure and susceptibility to parasites on both sexes. Even though significant differences of parasite levels between the sexes were observed within certain host species, our results strongly suggest that on a general level a more parasitized sex does not exist in the order, Odonata.     

Effects of water mites on the damselfly Ceriagrion tenellum

1. Water mite parasitism is expected to have an important effect on damselfly survivorship and reproductive success, because mites drain considerable amounts of body fluids from their hosts. This study tests the effect of water mite parasitism in a marked population of the damselfly Ceriagrion tenellum during 1995 (individuals marked as mature adults) and 1996 (individuals marked as tenerals).
2. Almost all teneral individuals were parasitized (98%) and mites were aggregated strongly on some individuals. Parasite load increased during the season.
3. Parasites had no effect on the probability of recapture of hosts as mature adults. The average daily survival rate of lightly- and heavily-parasitized individuals, estimated with Jolly's stochastic method, did not differ significantly.
4. In 1995 parasites had a significant effect on host mating success. The probability of mating was about 25% lower for heavily-parasitized males than for lightly-parasitized males. Lightly-parasitized males also mated more times than heavily-parasitized males, even if heavily-parasitized males lived longer. In 1996, parasitism did not have an effect on male mating success. In both years mites had no effect on female lifetime mating success.
5. These results indicate that water mite parasitism does not reduce damselfly survivorship, but it could reduce male mating success in some circumstances. Further long-term studies are needed, especially in populations with a lower incidence of parasitism.     

Lack of trade-off between direct and indirect defence against grape powdery mildew in riverbank grape

Abstract.  1. The hypothesis that plants that invest more in an indirect defence will invest less in direct mechanisms was tested using genotypes of the riverbank grape Vitis riparia that varied in expression of acarodomatia, tufts of non-glandular trichomes on underside of leaves that are frequently occupied by mycophagous mites. Mycophagous mites in this system have been shown to protect vines from grape powdery mildew caused by the fungus Uncinula necator .
2. Multiple cane cuttings from 24 genotypes of V. riparia , a species native to North America, were obtained from the USDA grape genetics repository and planted out in a common garden.
3. Genotypes varied in size of acarodomatia by threefold and varied in density of mycophagous mites by over 10-fold. Genotypes originating from the western part of the distribution had smaller acarodomatia and fewer mycophagous mites than genotypes from the eastern part of the distribution. There was a positive genetic correlation between acarodomatia size and mite density.
4. In a separate experiment, where vines were kept free of mycophagous mites, genotypes showed 10-fold variation in percentage leaf surface colonised by mildew. There was, however, no relationship between mildew on leaves and size of acarodomatia. Mildew did not vary depending on origin of genotype, although female vines tended to have greater levels than males.
5. No evidence was found for a trade-off between investment in an indirect defence mediated through acarodomatia and investment in direct defence against grape powdery mildew. Mite/plant defence mutualisms are contrasted with ant/plant defence mutualisms where there is better evidence for trade-offs under field conditions.     

Do Larval Damselflies make Adaptive Choices When Exposed to Both Parasites and Predators?

The importance of multiple enemies from different trophic levels on investment in defence by prey has, with some exceptions, received little attention. Some defences may make the victim more susceptible to other enemies; this latter situation applies to predators and parasites of larval damselflies. Baker and Smith [Oecologia 109 (1997) 622) showed that larval damselflies were as active in the presence of both mites and fish as they were when only mites were present, an apparently maladaptive behaviour that results in higher fish predation. In this paper, we further examine this maladaptive behavioural response to multiple enemies (fish predators and mite parasites) and test whether their defence responses are a result of the order in which they experience the parasite or predator, and/or if behavioural ‘personalities’ exist, such that some individuals show anti‐predator behaviours and other show anti‐parasite behaviours. Order of experience did not affect the four main behaviours (groom, crawl, turn and swim) exhibited when larval damselflies were simultaneously exposed to fish and mites. Grooming levels increased in response to mites, decreased in response to fish and when exposed to both mites and fish were similar to when they were exposed to mites alone. Duration of the other three behaviours was lower in the presence of both mites and fish. The crawling ‘personalities’ were evident. The apparently maladaptive response of high grooming levels in the presence of mites and fish is not a result of order of experience or ‘personalities’. It may be a result of relatively high encounter rates with mite parasites, compared with the encounter rates with fish. Lower encounter rates can result in diminishing investment in defence against an enemy.     

Immune expression in a damselfly is related to time of season, not to fluctuating asymmetry or host size

1. Variation in immune responsiveness within and among species is the subject of the emerging field of ecological immunology. The work reported here showed that individuals of Lestes forcipatus Rambur differ in their likelihood of mounting immune responses, and in the magnitude of those responses, against a generalist ectoparasite, the water mite Arrenurus planus Marshall. 2. Immune responses took the form of melanotic encapsulation of mite feeding tubes, occurred in the few days after host emergence, and resulted in mites dying without engorging. Such immune responses were more probable and stronger for hosts sampled later rather than earlier in the season. Such responses may act as selection affecting seasonal patterns of egg hatching and larval abundance of mites. 3. Contrary to expectation, metrics of host size (wing length) and wing cell fluctuating asymmetry were not related to the likelihood of immune responses. 4. The importance of season on immune expression of insects has not been explored in detail. These results suggest possible trade‐offs in allocation of melanin (or its precursors) to maturation versus immunity, and indicate the need for studies on the synergistic effects of weather and parasitism on host species that use melanotic encapsulation to combat parasites and pathogens.     

Species and sex biases in ectoparasitism of dragonflies by mites

An important problem in understanding the evolution of parasite host range is determining the extent to which parasite fitness varies among host species and the factors affecting that fitness variation. We present a detailed investigation on the patterns of host use and successful parasitism of two dragonfly species by the ectoparasitic water mite, Limnochares americana Lundblad. In our field surveys, we found both species biases and sex biases in parasitism by mites, which appear explained by differences in exposure. Differential habitat use by dragonflies helped explain male biases in parasitism in both host species, but was not useful in explaining species biases in parasitism. Species biases in parasitism may be explained by more subtle variation in habitat use not explored in this study, or perhaps by differences in timing of emergence, as we found for the two dragonfly species. Despite species differences in parasitism in nature, we found that mites attached equally successfully to both dragonfly species during experimental infestations. However, mites failed to engorge more often on the dragonfly species less often used as a host in nature. This host species also was more likely to have dead mites in natural infestations as compared to the other host species, which was more often and more heavily parasitized. Our results are consistent with previous research suggesting parasites are less successful on less often used hosts. Such research has implications for understanding determinants of host range for animal parasites.     

Recapture of male and female dragonflies in relation to parasitism by mites, time of season, wing length and wing cell symmetry

For aquatic mites parasitic on dragonflies, completion of their life cycle depends on their being returned to appropriate water bodies by their hosts, after completion of engorgement. We examined whether differences among hosts in timing of emergence or phenotypic attributes might affect their probability of return to an emergence pond, and hence success of mites. Parasitized males and females of the dragonfly Sympetrum obtrusum (Hagen) did not differ in overall recapture rates. Females that had wing cell symmetry and emerged early were more likely to be recaptured than females that emerged later or had wing cell asymmetry, but there were no consistent relations between these variables and parasitism by mites. No such relations between wing cell asymmetry, emergence date, and recapture likelihood were found for males. Using randomization tests, we found that mean intensities of Arrenurus planus (Marshall) mites at host emergence were the same for recaptured females and females not recaptured; however, males that were recaptured had lower mean intensities of mites at emergence than males not recaptured. Further, mature females carried more mites than mature males, and the latter had fewer mites than newly emerged males not recaptured. Biases in detachment of engorging mites do not explain the differences in parasitism between mature males and females, nor the differences in mite numbers between mature males and newly emerged males that were not recaptured. Rather, heavily parasitized males appear to disperse or die and are not recaptured, which should have implications for dispersal of mites and fitness of male hosts.     

Recapture of male and female dragonflies in relation to parasitism by mites, time of season, wing length and wing cell symmetry

For aquatic mites parasitic on dragonflies, completion of their life cycle depends on their being returned to appropriate water bodies by their hosts, after completion of engorgement. We examined whether differences among hosts in timing of emergence or phenotypic attributes might affect their probability of return to an emergence pond, and hence success of mites. Parasitized males and females of the dragonfly Sympetrum obtrusum (Hagen) did not differ in overall recapture rates. Females that had wing cell symmetry and emerged early were more likely to be recaptured than females that emerged later or had wing cell asymmetry, but there were no consistent relations between these variables and parasitism by mites. No such relations between wing cell asymmetry, emergence date, and recapture likelihood were found for males. Using randomization tests, we found that mean intensities of Arrenurus planus (Marshall) mites at host emergence were the same for recaptured females and females not recaptured; however, males that were recaptured had lower mean intensities of mites at emergence than males not recaptured. Further, mature females carried more mites than mature males, and the latter had fewer mites than newlyemerged males not recaptured. Biases in detachment of engorging mites do not explain the differences in parasitism between mature males and females, nor the differences in mite numbers between mature males and newly emerged males that were not recaptured. Rather, heavily parasitized males appear to disperse or die and are not recaptured, which should have implications for dispersal of mites and fitness of male hosts.     

Diffuse coevolution: constraints on a generalist parasite favor use of a dead-end host

Many evolutionary models and empirical studies of parasite-host interactions consider single species of parasites exploiting single host species. However, many parasites are generalists in that they parasitize more than one host species (often many more) and establish associations with other hosts that cannot be described as true parasitism. We identify such an association, explain how constraints may maintain it, and indicate why such diffuse interactions are deserving of attention. We describe the use of two closely related Sympetrum dragonfly species by larvae of the water mite Arrenurus planus Marshall. Adults of one dragonfly species are resistant whereas adults of the other species are almost wholly susceptible to A. planus . However, A. planus attaches as often to the resistant host as it does to the susceptible host species when relative abundance and seasonal timing of adult emergence of both species is considered. We present evidence that mites track the susceptible host and are most active early in the season, when early-emerging unsuitable hosts are also present. Thus, use of resistant hosts appears an unavoidable outcome of constraints promoting discovery and use of susceptible hosts. Such findings have implications for studies of local adaptation and host switching.     

Phenotypic variation in male and worker encapsulation response in the bumblebee Bombus terrestris

Abstract.  1. Life-history traits such as immunity are often characterised by the presence of large phenotypic variation, but it often remains unclear how and why this variation is maintained by selection.
2. Here an annual social insect, the bumblebee Bombus terrestris , was used to study variation in encapsulation response of males and workers. Bumblebees are a suitable system to study offspring immunity because they are host to a broad variety of different parasites. Bumblebee males, in particular, have a long lifespan compared with other social insect males and their immunity should therefore be an important element for colony reproductive success.
3. Encapsulation response, which was used here as a measurement for the generalised immune defence capacity of an individual, was found to be a highly variable trait. High levels of worker response correlated with low levels of colony parasitism rates.
4. Encapsulation response was found to be (a) lower in males compared with sister workers, and (b) lower in late-produced cohorts compared with early ones.
5. In colonies with delayed sexual reproduction, males had a lower encapsulation response. Thus, investments into immunity seemed reduced in later male cohorts and those eclosing later in the season, perhaps because males had a shorter expected remaining time to acquire matings. The results presented add further evidence that immune defence is a key variable defining colony fitness in social insects.     

Parasitism ofAcyrthosiphon pisum byAllothrombium pulvinum (Acariformes: Trombidiidae): Host attachment site,host size selection,superparasitism and effect on host

Several aspects of parasitism of the pea aphid,Acyrthosiphon pisum (Harris), by the mite parasiteAllothrombium pulvinum Ewing, were examined in the laboratory. Larvae ofA. pulvinum were fastmoving mites that find their host by contact of their foretarsi with the host. They can attach to all parts of the host body, but insert their chelicerae only into weakly sclerotized parts such as intersegmental membranes. Of the attached larval mites, most (63.5–74.1%) were on the thorax of their hosts, regardless of host size. In hosts of small and medium size, the ventral side receives most parasitism, whereas in large hosts the lateral sites are most often attacked. Larval mites prefer large hosts when allowed to select between pairs of large and small hosts, but show no significant preference when allowed to choose between pairs of large and medium hosts or pairs of medium and small hosts. In two-choice tests, larval mites prefer previously parasitized hosts to umparasitized hosts, which results in superparasitism of the hosts. When the mite load is fiveA. pulvinum kills all small hosts within three days, and all medium hosts and 50% of large hosts within four days, the reproduction of surviving adult aphids were significantly reduced. Host-finding behavior, attachment site preference, host size selection, superparasitism, and effect on hosts are briefly reviewed for larval parasites of Trombidiidae. The potential role of larvalAllothrombium in integrated and biological aphid control is also discussed.     

Success of ectoparasites: how important is timing of host contact?

Hosts often differ in their degree of parasitism and their expression of resistance. Yet very little is known about how the availability (and allocation) of resources to parasites at pre-infective stages influences their success in initiating parasitism, or in inducing and succumbing to resistance from hosts. We studied a damselfly-mite association to address how experimental variation in the age of first contact with hosts (timing) influenced subsequent parasite fitness. We demonstrate that timing influenced the ability of larval mites to make the transition to parasitism, but was not associated with measures of physiological resistance by hosts. Timing presumably relates to the availability of resources remaining for individuals to exploit their hosts. More research is needed on the importance of such factors, from variation in host resistance and parasite success and, ultimately, to the numbers and distributions of parasites on hosts.     

No Correlation Between Ectoparasitism and Male Mating Success in a Damselfly: Why Parasite Behavior Matters

The mating success of individually marked male damselflies parasitized by water mites was closely followed. The number of ectoparasites could be determined exactly from knowledge of the parasite's life cycle. In contrast to previous studies, no correlation between water mite infestation and male mating success was revealed. The reasons for this discrepancy may be explained by the inclusion of the parasite's behavior. The body fat content of the males was negatively correlated with the mite load, indicating that parasitism reduces host's condition. It is hypothesised that the water mites damselfly system is not valuable for testing the Hamilton and Zuk hypothesis. Furthermore, selection exerted or mediated by parasites should act during the teneral phase.     

Effects of eugregarine parasites on adult longevity in the polymorphic damselfly Mnais costalis Selys

Abstract.  1. The relationship between the abundance of midgut parasites (eugregarine trophozooites) and the survival of hosts (field-collected damselflies, Mnais costalis ) was investigated under laboratory conditions.
2. Males of M. costalis are morphologically and behaviourally polymorphic, typically existing as clear-winged non-territorial sneaks and orange-winged territorial fighters (the latter are larger in size). The survival cost of eugregarine infection for the two morphs was compared.
3. Orange-winged males showed shorter longevity compared to clear-winged males when they were fed at levels lower than the natural feeding rate, or when they were deprived of food. In contrast, morph longevity did not differ when they were fed until satiation every day.
4. Within each morph, the survival of damselflies was negatively correlated with the parasite abundance except when damselflies were fed until satiation.
5. The results suggest that the abundance of eugregarine parasites exerts a substantial cost, which is associated with the maintenance of alternative mating strategies, together with the higher developmental cost and energy expenditure of the fighter morph.     

Immune response to nylon filaments in two damselfly species that differ in their resistance to ectoparasitic mites

1. Insects commonly resist parasites using melanotic encapsulation. Many studies measuring immune response use the amount of melanin deposited on an artificial object that has been inserted into the animal as a proxy of the amount of resistance that the host is capable of mounting to natural parasites. 2. The relevance of this methodology to immune response in natural insect populations needs further study. Here, we examined two temperate damselfly species to elucidate the relationships among damselfly size, natural resistance to mites, and the immune response mounted by the same damselflies against nylon filaments. 3. The damselfly species that had high rates of melanotic encapsulation of mites in nature deposited more melanin on the nylon inserts than the species with low rates of natural resistance. 4. In females of this species, those that had resisted mites naturally melanised the nylon filament more aggressively than those that did not resist mites. 5. Our results show some support for the use of nylon filaments to assess natural patterns of immune response in these damselflies, but also suggest that caution should be used in interpreting the responses.     

The evolution of acceptance and tolerance in hosts of avian brood parasites

Avian brood parasites lay their eggs in the nests of their hosts, which rear the parasite's progeny. The costs of parasitism have selected for the evolution of defence strategies in many host species. Most research has focused on resistance strategies, where hosts minimize the number of successful parasitism events using defences such as mobbing of adult brood parasites or rejection of parasite eggs. However, many hosts do not exhibit resistance. Here we explore why some hosts accept parasite eggs in their nests and how this is related to the virulence of the parasite. We also explore the extent to which acceptance of parasites can be explained by the evolution of tolerance; a strategy in which the host accepts the parasite but adjusts its life history or other traits to minimize the costs of parasitism. We review examples of tolerance in hosts of brood parasites (such as modifications to clutch size and multi‐broodedness), and utilize the literature on host–pathogen interactions and plant herbivory to analyse the prevalence of each type of defence (tolerance or resistance) and their evolution. We conclude that (i) the interactions between brood parasites and their hosts provide a highly tractable system for studying the evolution of tolerance, (ii) studies of host defences against brood parasites should investigate both resistance and tolerance, and (iii) tolerance and resistance can lead to contrasting evolutionary scenarios.     

Can mite parasitism affect the condition of bat hosts? Implications for the social structure of colonial bats

Ectoparasitism may be recognized as one of the main costs of coloniality, but little is known about how it affects the fitness and social structure of bats, the most gregarious of mammals. We studied these issues using the colonial bat Miniopterus schreibersii and its haematophagous parasitic mite Spinturnix psi as a model. Body condition is an important indicator of individual fitness that is potentially affected by ectoparasitism. Thus, we measured host body condition and mite loads in a total of 969 bats throughout the annual cycle. Mites were rare while hosts hibernated, increased in abundance in spring and peaked during nursing season of bats, when they were particularly abundant on lactating females and young bats. This strong seasonal variation in mite loads is related to the reproductive cycle of mites, which in turn appears to be synchronized with the reproductive cycle of their hosts. Mite loads and the condition of bats were negatively correlated, and information available suggests that this may be due to an effect of parasitism, although other possible causes for this trend cannot be excluded. However, a negative correlation was only observed during the bat's nursing season, when mites were most abundant, and heavily parasitized bats lost about 10% of their weight. Mite parasitism did not seem to be a significant disadvantage of coloniality, except in nurseries, where it might impose some costs. However, as females and young usually aggregate in these colonies, we presume that for them such costs are probably offset by advantages of group living. Adult males, however, are usually absent from nurseries, which may be a strategy to minimize mite parasitism. Overall, the results suggest that ectoparasitism may play a role in determining the social structure of M. schreibersii and of many other temperate bats that have similar life cycles and ectoparasitic loads.