Aquarius Remigis Research Articles

Protease activation and the signal transduction pathway regulating motility in sperm from the water strider Aquarius remigis

Many motile processes are regulated such that movement occurs only upon activation of a signaling cascade. Sperm from a variety of species are initially quiescent and must be activated prior to beating. The signaling events leading to the activation and regulation of sperm motility are not well characterized. Mature seminal vesicle sperm from the water strider Aquarius remigis are immotile in vitro, but vigorous motility is activated by trypsin. Trypsin-activated motility was blocked by pretreatment of the sperm with BAPTA-AM to chelate intracellular Ca(2+) and was partially rescued by subsequent addition of A23187 and Ca(2+). Thapsigargin stimulated motility in the absence of trypsin, suggesting that intracellular Ca(2+) stores are available. In addition, motility could be fully activated by the phosphatase inhibitor calyculin A, suggesting that the immotile state is maintained by an endogenous phosphatase and that kinase activity is required for motility. The MEK1/2 inhibitor U0126 significantly reduced trypsin activated motility, and MPM-2, an antibody which recognizes proline-directed phosphorylation by kinases such as MAPK, recognized components of the water strider sperm flagellum. Antibodies specific for the mouse protease activated receptor PAR2 recognized an antigen on the sperm flagellum. These results suggest that trypsin stimulates a Ca(2+) and MAPK mediated signaling pathway and potentially implicate a PAR2-like protein in regulating motility.

Reproductive allometry does not explain the temperature-size rule in water striders (Aquarius remigis)

Most ectotherms follow the temperature-size rule meaning that individuals growing up under cool conditions are larger as adults than those growing up in warm conditions. This pattern is difficult to explain because growth is usually slower in the cold meaning it takes longer to reach a larger adult size. One potential explanation for this pattern is that the typical increase in fecundity with body size is steeper in cool environments than it is in warm environments. As such, the relative gain in fecundity for being larger in the cold would compensate for the extra time it takes to grow to that size. We present the first empirical test of this model using the water strider Aquarius remigis. Individuals were reared at either 20° or 25°C with subsampling at each instar to estimate growth trajectories. At adult eclosion, half were switched to the alternate temperature and all females isolated, mated, and reproductive output measured for 3 weeks. We found that A. remigis does follow the temperature-size rule but that fecundity was highly plastic with respect to laying temperature such that the slightly greater fecundity of those reared at 20°C was due to their larger size. Overall, those laying at 25°C were more fecund and showed a positive relationship between body size and fecundity. Those laying at 20°C did not show a significant relationship between size and fecundity. As such, the reproductive allometry shows a pattern reverse to what would be needed for a larger size in the cold to be adaptive in this species. Although A. remigis follows the temperature-size rule over this temperature range, this is likely due to a constraint on growth and development rather than being adaptive plasticity.

The effect of ambient humidity and metabolic rate on the gas-exchange pattern of the semi-aquatic insectAquarius remigis

We have examined the effects of temperature on metabolic rate and respiratory pattern in the water strider Aquarius remigis. As temperature was increased from 10 to 30°C, the metabolic rate of the insects increased and the respiratory pattern transitioned from discontinuous, to cyclic, to continuous. The discontinuous gas-exchange cycle (DGC) was observed even in insects standing on water when the respirometry chamber was being perfused with humid (>95% relative humidity) air. Comparisons of insects at 20°C in humid and dry air showed no statistically significant differences in metabolic rate or respiratory pattern (P>0.05). The proportion of time that the spiracles were closed was greater at 10°C than at 20°C (P<0.01), and greater at 20°C than at 30°C (P<0.05). These results are compatible with the hypothesis that the respiratory patterns of insects are determined by the relationship between oxygen supply and oxygen demand. There was no evidence in this insect that humidity had any effect on the respiratory pattern. The results are discussed in the context of the ongoing discussion in the literature of the origin, maintenance and adaptive significance of the DGC in insects.

Assembly of the fluorescent acrosomal matrix and its fate in fertilization in the water strider, Aquarius remigis

Animal sperm show remarkable diversity in both morphology and molecular composition. Here we provide the first report of intense intrinsic fluorescence in an animal sperm. The sperm from a semi-aquatic insect, the water strider, Aquarius remigis, contains an intrinsically fluorescent molecule with properties consistent with those of flavin adenine dinucleotide (FAD), which appears first in the acrosomal vesicle of round spermatids and persists in the acrosome throughout spermiogenesis. Fluorescence recovery after photobleaching reveals that the fluorescent molecule exhibits unrestricted mobility in the acrosomal vesicle of round spermatids but is completely immobile in the acrosome of mature sperm. Fluorescence polarization microscopy shows a net alignment of the fluorescent molecules in the acrosome of the mature sperm but not in the acrosomal vesicle of round spermatids. These results suggest that acrosomal molecules are rearranged in the elongating acrosome and FAD is incorporated into the acrosomal matrix during its formation. Further, we followed the fate of the acrosomal matrix in fertilization utilizing the intrinsic fluorescence. The fluorescent acrosomal matrix was observed inside the fertilized egg and remained structurally intact even after gastrulation started. This observation suggests that FAD is not released from the acrosomal matrix during the fertilization process or early development and supports an idea that FAD is involved in the formation of the acrosomal matrix. The intrinsic fluorescence of the A. remigis acrosome will be a useful marker for following spermatogenesis and fertilization.

Altitudinal differentiation of reproductive tactic plasticity despite the close proximity of two Aquarius remigis populations

AbstractIn the water strider (Aquarius remigis), direct and delayed reproductive tactics are largely canalized in southern and northern areas of North America, respectively. A transition zone occurs in upstate New York, defined as the area where lowland striders plastically express either tactic based on photoperiod and food abundance cues. We tested whether these cues similarly influence tactics among higher altitude transition zone populations. We compared the proportion of direct reproducers from a high altitude stream (HAS) and a low altitude stream (LAS) reared under low and high food abundance, as well as a normal and late-solstice photoperiod. With sexes combined, higher proportions of direct reproducers were found among LAS striders, and among striders reared in the late solstice photoperiod and high food abundance treatments. Among males, a food abundance × stream interaction was significant, suggesting greater canalization of reproductive tactics among HAS males. Among females, photoperiod was a significant factor, but did not interact with stream of origin. Field measurements showed that water surface temperatures and food abundance were lower in HAS compared to LAS. These conditions, as well as shorter season lengths, likely select against direct reproduction among HAS striders, possibly resulting in the observed canalization of reproductive tactics.

THE ROLE OF MULTILEVEL SELECTION IN THE EVOLUTION OF SEXUAL CONFLICT IN THE WATER STRIDER AQUARIUS REMIGIS

In evolution, exploitative strategies often create a paradox in which the most successful individual strategy "within" the group is also the most detrimental strategy "for" the group, potentially resulting in extinction. With regard to sexual conflict, the overexploitation of females by harmful males can yield similar consequences. Despite these evolutionary implications, little research has addressed why sexual conflict does not ultimately drive populations to extinction. One possibility is that groups experiencing less sexual conflict are more productive than groups with greater conflict. However, most studies of sexual conflict are conducted in a single isolated group, disregarding the potential for selection among groups. We observed Aquarius remigis water striders in a naturalistic multigroup pool in which individuals could freely disperse among groups. The free movement of individuals generated variation in aggression and sex-ratio among groups, thereby increasing the importance of between-group selection compared to within-group selection. Females dispersed away from local aggression, creating more favorable mating environments for less-aggressive males. Furthermore, the use of contextual analysis revealed that individual male aggression positively predicted fitness whereas aggression at the group level negatively predicted fitness, empirically demonstrating the conflict between levels of selection acting on mating aggression.

Aggressive mating as a tragedy of the commons in the water strider Aquarius remigis

The tragedy of the commons usually refers to the overexploitation of resources such as food or water. Here, we show in a laboratory study that competition among males for females can also result in a tragedy of the commons’ situation. Male water striders (Aquarius remigis) vary widely in their aggressiveness toward pursuing females. The most aggressive males prevent females from feeding and cause them to leave the water surface, where they are unavailable to all males. Groups of nonaggressive males are collectively three times more fit than groups of hyperaggressive males, but hyperaggressive males are more successful than nonaggressive males within mixed groups. This is the classic tragedy of the commons’ situation, and it is likely to occur in many species that exhibit sexual conflict. We have also shown that individual differences in male aggression are stable across time and are not influenced by food or light regime, although all individuals become nonaggressive in the presence of fish predators.

Why do Californian striders fly?

Discerning the adaptive significance of migratory strategies poses significant challenges, not the least of which is measuring migratory capability in natural populations. We take advantage of a visible migratory dimorphism to study variation in migratory capability in the stream-dwelling water strider, Aquarius remigis. Theory predicts loss of migratory capability in this species because streams have been viewed as stable and persistent habitats. As expected, A. remigis lack wings throughout most of North America. However, Californian populations are noted for unexpectedly high frequencies of winged, migratory morphs. To deduce the adaptive significance of this anomalous regional variation, we compare proportion winged among 37 Californian populations. We discover a strong, positive correlation with altitude, but no correlations with latitude, rainfall or stream size. A common garden experiment reveals that both proportion winged and its reaction norm to temperature differ genetically among populations, and a half-sibling experiment demonstrates that wing morph has high heritability, moderate genetic correlations across environments and a significant genotype by environment interaction. These results support the hypothesis that proportion winged and its reaction norm to temperature have diverged genetically in California. We conclude that high migratory capability is an evolutionary adaptation to the unusual harshness and instability of Californian stream habitats, and particularly to the high elevational gradients and extreme seasonal variation characteristic of montane streams.

An elemental and stable isotope assessment of water strider feeding ecology and lipid dynamics: synthesis of laboratory and field studies

Summary1. Despite the ubiquity and abundance of water striders (Hemiptera: Gerridae) in temperate streams and rivers and their potential usefulness as sentinels in contaminant studies, little is known about their feeding ecology and lipid dynamics.2. In this study we used stable isotopes of carbon (δ13C) and nitrogen (δ15N) and elemental carbon to nitrogen ratios (C/N) to assess dietary habits and lipid content, respectively, for water striders.3. To determine diet‐tissue fractionation factors, nymphs of the most common species in New Brunswick, Canada, Aquarius remigis were reared in the laboratory for 73 days and exhibited rapid isotopic turnover in response to a switch in diet (C half‐life = 1.5 days, N half‐life = 7.8 days). Their lipid content increased towards the end of the growing season and resulted in lower δ13C values. Diet‐tissue fractionation factors were established after correction of δ13C data for the confounding effect of de novo lipid synthesis (strider δ13Cadj– diet δ13Cadj = 0.1‰, strider δ15N – diet δ15N = 2.7‰).4. Water striders from the majority of 45 stream sites (83%) in New Brunswick had less than 50% contribution of aquatic carbon to their diets but showed a gradual increase in the contribution of this carbon source to their diet with increasing stream size.5. These data indicate that striders exhibit a strong connection to terrestrial carbon sources, making them important users of energy subsidies to streams from the surrounding catchment. However, this dependence on terrestrial organic matter may limit their utility as indicators of contamination of aquatic systems by heavy metals and other pollutants.

Trophic interception: how a boundary‐foraging organism influences cross‐ecosystem fluxes

The rate at which subsidies move between habitats is a function not only of those factors that facilitate such transfers, but also of factors that limit or restrict the movement of subsidies. The interruption or redirection of subsidies by organisms foraging at the boundary between habitats, or trophic interception, has the potential to substantially restructure the food webs of recipient habitats. In this study we describe how a waterstrider, Aquarius remigis, limits the transfer of a subsidy across the land‐water boundary. Prey interception varied with the type of stream habitat; on average, waterstriders in isolated pools intercepted 71.8% of experimental prey inputs of all sizes compared with 21.5% in connected pools and 0.8% in riffles. Across all stream habitat types, waterstriders consumed 43.2% of the experimental inputs of the smallest prey used, the prey size class most similar to natural inputs in our study area. We estimate that foraging waterstriders may intercept 0.3–1.2 kg of terrestrial prey subsidy for every 100 m of stream channel during three summer months, resources that could otherwise support 13–58 young‐of‐the‐year salmonids. In controlled trials, waterstriders significantly altered the amount of terrestrial prey directly consumed by fish, while fish also altered waterstrider interception of those prey. Interestingly, when waterstriders and fish were present together, more terrestrial prey were lost to the streambed than when either or both of these consumers were absent, making this resource available to benthic detritivores, and facilitating the direct incorporation of terrestrial nutrients into stream detrital webs. Overall, we demonstrate that organisms that forage at habitat boundaries can control the quantity and quality of subsidies arriving in recipient habitats, potentially altering food web structures within those habitats.

THE FORM OF SEXUAL SELECTION ON MALE GENITALIA CANNOT BE INFERRED FROM WITHIN-POPULATION VARIANCE AND ALLOMETRY?A CASE STUDY IN AQUARIUS REMIGIS

Male genital morphology in insects and arachnids is characterized by static hypoallometry and low intrapopulational levels of phenotypic variation relative to other male traits. The one-size-fits-all model of genital evolution attributes these patterns to stabilizing sexual selection. This model relies on the assumption that the observed patterns of variation and allometry reflect the form of sexual selection acting these traits. We test this by examining the patterns of scaling and trait variation for a set of genitalic and somatic morphological traits in male water striders (Aquarius remigis). This suite of traits is of particular interest because previous work has shown that the genitalic traits are under strong directional selection whereas the somatic traits are under either weak directional or stabilizing selection. Because the selection regime for these traits is known, we can, for the first time, test the purported relationship between trait variation, scaling, and the form of sexual selection. We show that the patterns of variation and scaling of these traits differ sharply from those predicted for traits experiencing strong directional sexual selection. Specifically, the male genital structures show static hypoallometry and low intrapopulational levels of phenotypic variation relative to other male traits, in spite of consistent, strong, directional sexual selection. These scaling relationships and levels of variation are typical of genital traits in other insect species, where they have been presumed to reflect stabilizing sexual selection. Our data clearly refute the assumption of the one-size-fits-all hypothesis that hypoallometric scaling of genitalic traits implies stabilizing selection. We discuss the implications of this finding and propose future directions for improving our current understanding of genital evolution in arthropods.

Genital morphology and taxonomy of the water strider Aquarius remigis (Say) (Insecta, Hemiptera-Heteroptera: Gerridae)

Received 12 J anuary 2005; accepted for publication 16 Marc h 2006The shape of the dorsal vesical plate w as used to determine the extent of morphological differentiation amongpopulations of the w ater strider Aquarius remigis (Sa y) (Hemiptera-Heteroptera: Gerridae), and between speciesassigned to the A. remigis species group . P opulations were sampled throughout North America and Mesoamerica,and inc luded paratypes of A. remigoides Gallant & F airbairn, and material collected from the type localities ofA. amplus (Drake & Harris) and A. nyctalis (Drake & Hottes). If taxonomy is to be inferred from the shape of the dor -sal vesical plate , as suggested by previous authors , several taxonomic issues need to be reconsidered. F irst, there w a sone species distributed widely across North America and deep into Mexico that is very likely to represent A. remigis ,meaning that populations from the western USA previously assigned to OA. nyctalis O should be synonymized with thisspecies . Second, A. remigoides as currently deÞned also inc ludes some populations of A. remigis , and is probablymuc h less widely distributed in the south-eastern USA than previously thought. A hybridization zone in P ennsyl-vania between A. remigis and A. remigoides , as inferred from measurements of body size and allozyme electrophore-sis , is not congruent with data from the male genitalia, whic h indicated a transition zone between the two forms inV irginia muc h further to the south. F inally , A. amplus w as widespread in Mexico , reac hing into Guatemala to thesouth and into Arizona to the north. © 2007 The Linnean Society of London, Biological J ournal of the Linnean Soci-ety , 2007, 90 , 381Ð398.

Divergent juvenile growth and development mediated by food limitation and foraging in the water strider Aquarius remigis (Heteroptera: Gerridae)

AbstractThe factors leading to variation in growth, development and body size are of central importance for the study of life histories. I investigated the effect of food limitation on patterns of growth and development in the water strider Aquarius remigis (Heteroptera: Gerridae). Groups of 10 juveniles were allowed to develop under field conditions at three different food levels. Food limitation prolonged juvenile development, reduced growth rates and led to smaller adult body size and weight, the most common life‐history response in ectotherms; it also increased the variance among individuals in these traits, demonstrating variance accumulation suggesting divergent growth. Evidence that this resulted from competition among individuals for limited food was equivocal. On the one hand, direct observation of foraging nymphs showed that larger instar individuals were more likely to obtain monopolizable prey items than expected by chance, independent of food level. On the other hand, there was only a trend for the variance in moulting dates to increase when striders were raised in groups as opposed to singly at various temperatures in a controlled laboratory experiment. When food limitation prolongs juvenile development, variance accumulation with age can result from food limitation per se, as well as from random or heritable variation in growth trajectories. Foraging competition may amplify this effect, but not necessarily so. Therefore, it must not be assumed that divergent growth is necessarily caused by food competition.

Allometry for Sexual Size Dimorphism: Testing Two Hypotheses for Rensch’s Rule in the Water StriderAquarius remigis

Within any given clade, male size and female size typically covary, but male size often varies more than female size. This generates a pattern of allometry for sexual size dimorphism (SSD) known as Rensch's rule. I use allometry for SSD among populations of the water strider Aquarius remigis (Hemiptera, Gerridae) to test the hypothesis that Rensch's rule evolves in response to sexual selection on male secondary sexual traits and an alternative hypothesis that it is caused by greater phenotypic plasticity of body size in males. Comparisons of three populations reared under two temperature regimes are combined with an analysis of allometry for genital and somatic components of body size among 25 field populations. Contrary to the sexual-selection hypothesis, genital length, the target of sexual selection, shows the lowest allometric slope of all the assayed traits. Instead, the results support a novel interpretation of the differential-plasticity hypothesis: that the traits most closely associated with reproductive fitness (abdomen length in females and genital length in males) are "adaptively canalized." While this hypothesis is unlikely to explain Rensch's rule among species or higher clades, it may explain widespread patterns of intraspecific variation in SSD recently documented for many insect species.

One tool, many uses: precopulatory sexual selection on genital morphology inAquarius remigis

While congruent evidence indicates that sexual selection is the most likely selective force explaining the rapid divergence of male genital morphology in insects, the mechanisms involved in this process remain unclear. In particular, little attention has been paid to precopulatory sexual selection. We examine sexual selection for mating success on male genital components in six populations of Aquarius remigis, a water strider characterized by unique genital morphology. Multivariate selection analysis confirms previous findings that precopulatory sexual selection favours longer external genitalia, and provides new evidence that this selection acts independently on external genital components. In contrast, the size of the major internal genital sclerite is not correlated with mating success. Thus, precopulatory sexual selection acts strongly on the size of the external genitalia, but not on the intromittent organ itself. These results highlight the multiple functions of genital organs and the importance of both precopulatory and post-copulatory sexual selection in shaping the remarkable diversity of male genitalia in insects.

The mix matters: behavioural types and group dynamics in water striders

Summary The effect of an individual’s behavioral type (e.g., its boldness or aggressiveness) on fitness likely depends on the environmental context. In many species, an important component of an individual’s environment is its social environment — the mix of individuals in its social group. Accordingly, much of game theory assumes that the mix of behavioral types (BTs) in a social group influences individual fitness and group dynamics. Few experimental studies, however, have directly investigated how the group’s mix of BTs influences individual and group outcomes. Here we manipulated social group composition in the water strider Aquarius remigis and evaluated the effects of our manipulation on individual behavior and various group outcomes (overall group activity, aggression, mating success). We formed 12 groups that differed substantially in average male BT (activity and aggression level), each with a low variance in BT. That is, one group had only the most active and aggressive males, a second group was made up of the next most active and aggressive males, and on down to a group of all very inactive and unaggressive males. All groups also had females. We found that, on average, groups made up of more active-aggressive males continued to be more active than other groups, but that contrary to predictions, these groups did not tend to enjoy higher mating success. Instead, a major factor affecting group mating activity was the presence of hyper-aggressive males. Hyper-aggressive males drove females out of the group and thereby decreased the group’s overall mating activity. We discuss these findings in terms of their importance to the study of behavioral plasticity in social groups and the potential role of keystone individuals in determining group dynamics.

Water-repellent legs of water striders

Water striders (Gerris remigis) have remarkable non-wetting legs that enable them to stand effortlessly and move quickly on water, a feature believed to be due to a surface-tension effect caused by secreted wax. We show here, however, that it is the special hierarchical structure of the legs, which are covered by large numbers of oriented tiny hairs (microsetae) with fine nanogrooves, that is more important in inducing this water resistance.

Sources of character conflict in a clade of water striders (Heteroptera: Gerridae).

Incongruence among trees reconstructed with different data may stem from historical (gene tree-species tree conflict) or process (character change biases) phenomena. Regardless of the source, incongruent data, as determined with "global" measures of homoplasy, have often been excluded from parsimony analysis of the combined data. Recent studies suggest that these homoplasy measures do not predict the contribution of each character to overall tree structure. Branch support measures identify, on a character to node basis, sources of support and conflict resulting from a simultaneous analysis of the data. We implement these branch support measures to identify sources of character conflict in a clade of water striders consisting of Gerris Fabricius, Aquarius Schellenberg, and Limnoporus Stål species. Separate analyses of morphology, mitochondrial cytochrome oxidase I (COI), large mitochondrial ribosomal subunit (16SrRNA), and elongation factor-1α (EF-1α) data resulted in cladograms that varied in resolution and topological concordance. Simultaneous analysis of the data resulted in two trees that were unresolved for one node in a strict consensus. The topology agreed with current classification except for the placements of Aquarius chilensis and the Aquarius remigis species group closer to Gerris than to congeneric species. Branch support measures indicated that support derived from each data set varied among nodes, but COI had an overall negative effect on branch support. However, Spearman rank correlation of partitioned branch support values indicated no negative associations of branch support between any data sets and a positive association between EF-1α and 16SrRNA. Thus incongruence among data sets was not drastic and the gene-tree versus species tree phenomenon was not implicated. Biases in character change were a more likely reason for incongruence, although saturation curves and incongruence length difference for COI indicated little potential for homoplasy. However, a posteriori inspection of COI nucleotide change with reference to the simultaneous analysis tree revealed AT and codon biases. These biases were not associated with branch support measures. Therefore, it is difficult to predict incongruence or identify its cause. Exclusion of data is ill advised because every character is potentially parsimony informative.

Sources of character conflict in a clade of water striders (Heteroptera: Gerridae)

Incongruence among trees reconstructed with different data may stem from historical (gene tree-species tree conflict) or process (character change biases) phenomena. Regardless of the source, incongruent data, as determined with “global” measures of homoplasy, have often been excluded from parsimony analysis of the combined data. Recent studies suggest that these homoplasy measures do not predict the contribution of each character to overall tree structure. Branch support measures identify, on a character to node basis, sources of support and conflict resulting from a simultaneous analysis of the data. We implement these branch support measures to identify sources of character conflict in a clade of water striders consisting of Gerris Fabricius, Aquarius Schellenberg, and Limnoporus Stål species. Separate analyses of morphology, mitochondrial cytochrome oxidase I (COI), large mitochondrial ribosomal subunit (16SrRNA), and elongation factor-1α (EF-1α) data resulted in cladograms that varied in resolution and topological concordance. Simultaneous analysis of the data resulted in two trees that were unresolved for one node in a strict consensus. The topology agreed with current classification except for the placements of Aquarius chilensis and the Aquarius remigis species group closer to Gerris than to congeneric species. Branch support measures indicated that support derived from each data set varied among nodes, but COI had an overall negative effect on branch support. However, Spearman rank correlation of partitioned branch support values indicated no negative associations of branch support between any data sets and a positive association between EF-1α and 16SrRNA. Thus incongruence among data sets was not drastic and the gene-tree versus species tree phenomenon was not implicated. Biases in character change were a more likely reason for incongruence, although saturation curves and incongruence length difference for COI indicated little potential for homoplasy. However, a posteriori inspection of COI nucleotide change with reference to the simultaneous analysis tree revealed AT and codon biases. These biases were not associated with branch support measures. Therefore, it is difficult to predict incongruence or identify its cause. Exclusion of data is ill advised because every character is potentially parsimony informative.

Host age, but not host location within a stream, is correlated with the prevalence of gut parasites in water striders.

We tested for correlations between the geographic, demographic, and temporal distribution of an aquatic insect host and the prevalence of its gut parasites in southwestern Ohio. Trypanosomatids were present in Aquarius remigis collected from all 4 streams surveyed in the watershed. Prevalence declined dramatically from May to July and remained low through the fall. This pattern was consistent over all sites of our study, with no effect of stream, stream site (upstream vs. downstream), or host sex on prevalence. Stage, however, was strongly correlated with prevalence; adults were more likely to be infected than were nymphs. We argue that behavioral differences between the 2 age classes may account for the decline in prevalence; opportunities for transmission are highest in the spring, when mating activities increase adult host contact rates, and decline in the summer, when contact rates decrease.