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Reproduction increases an individual's fitness directly; however, the act of copulation can incur fitness costs. In many animals, males mate-guard females before and after copulation (Bradbury and Vehrencamp, 2011) while in insects females often carry or drag males during prolonged copulation (Fairbairn, 1993; Ercit et al., 2014). This could result in substantial costs if it decreases a pair's ability to move around the environment. Through this mechanism, copulation could lead to increased energetic costs to locomotion and thermoregulation as well as to increased mortality via predation (Lima and Dill, 1990; Magnhagen, 1991; Fairbairn, 1993).

Predation is a major selective force for all but a few species (Curio, 2012). Predation risk increases during copulation, especially when pairs stay in copula for extended periods (Magnhagen, 1991; Han et al., 2015). Empirical work has found that, in odonates, copulating pairs are more vulnerable to predation than are single males (Fincke, 1982), and in a semiaquatic bug, Microvelia austrina, the proportion found in copulation is lower when there is a predator present (Sih, 1988). In locusts, copulation increases the risk of parasitoid-mediated mortality by 10% (Kemp, 2011). Experimental work in water striders (Aquarius remigis) has shown that weight bearing associated with copulation leads to higher predation risk by frogs (Fairbairn, 1993). Copulating pairs presumably present a more lucrative meal for a predator than would unpaired individuals, and they are potentially less wary of predators. Extended copulation could also affect the ability of a copulating pair to escape from predators, but this has not been directly established (but see Fairbairn, 1993; Jersabek et al., 2007).

In addition to increasing predation risk, copulation has energetic costs. Individuals decrease foraging and thermoregulating behaviors when in copula, though this can be alleviated through nuptial gifts (Watson et al., 1998). Nonetheless, energetic costs of mating can be higher for females (Franklin et al., 2012). In some insects, females have increased energy expenditure during locomotion because they carry or drag the smaller male while in copula (Fairbairn, 1993; Watson et al., 1998). This increased energy expenditure could manifest itself in lower movement speeds.

The potential costs to copulation have been established relatively well. However, the mechanisms by which these costs operate are less clear. It is uncertain whether copulation decreases mobility across species and whether the size ratio of female:male affects mobility. Presumably, costs to the female vary depending on male size; we expect higher costs for females paired with larger males than for females paired with smaller males. Here, I studied the mobility cost to copulation in common squash bugs (Anasa tristis, Coreidae). The objectives of the study were to determine (a) whether copulation decreases movement speed, and (b) whether the degree to which movement speed is impaired is a function of the ratio of female:male size.

Common squash bugs are sap-sucking hemipterans (Borror and White, 1998) commonly found on cucurbit leaves (Marah species). In this sexually dimorphic species, the larger female drags the smaller male during copulations that can last several hours (H. Schraft, pers. observ.). They often fall prey to birds, spiders, and other predators despite rapid escape behaviors and secretion of an unpleasant odor from glands on the thorax (Borror et al., 1989). The proportion of time that squash bugs spend mating is unknown but is likely high. A study of seed bugs (Neacoryphus bicrucis) found that marked females were copulating during 83% of resightings (McLain, 1989).

I collected single squash bugs (n = 43; 19 males, 24 females) and copulating pairs (n = 65 pairs) from cucurbit plants at the Bodega Marine Reserve on the California coast (38[degrees]19'N, 123[degrees]04'W) between 21 March and 23 March 2016. Specimens were housed individually or as copulating pairs with a cucurbit leaf in 2-oz and 6-oz plastic containers for the duration of the study. Pairs in copula typically aborted copulation shortly after collection but often resumed at sporadic intervals over the 3-d study period (30/65 pairs). I measured pronotum width of all individuals to the nearest tenth of a millimeter using calipers.

To determine whether copulation affects mobility, I placed copulating pairs (n = 30) and single bugs (n = 43) in an arena and measured average movement speed. Each individual or pair was placed in a white, 1-gal plastic bucket (diameter = 15.5 cm) with sides coated with silicone lubricant to prevent wall climbing. Contact with silicone did not appear to impair subsequent movement. Bugs were then filmed for 90 s using an overhead digital camera Sony DSC-HX7V (Sony Corporation, Minato, Tokyo, Japan) or Canon xs200is (Canon Inc., Ota, Tokyo, Japan). I measured total movement distance using automated image-based tracking software (Ctrax v0.5.5, Branson et al., 2009) and divided this distance by the trial duration to obtain average movement speed. The open environment of the arena provided sufficient stimulus for all animals to move immediately and continuously for the full 90-s period.

I fitted a linear model of speed as a function of pairing status to compare movement speed between copulating pairs and unpaired individuals. For copulating pairs, I tested whether the size disparity between sexes influenced movement speed by fitting a linear model of speed as a function of the ratio of female:male body size (pronotum width). This approach allowed me to control for variability in female size. I used Bayesian Markov-chain Monte Carlo model fitting methods with weakly regularizing priors. I report the effect sizes as means of the posterior distribution with highest posterior density intervals (HPDI; McElreath, 2016). All statistical analyses were performed in R v3.2.3 (R Core Team, Vienna, Austria, using the 'rethinking' package (McElreath, 2015).

Pronotum width was 4.93 [+ or -] 0.17 mm (mean [+ or -] SD) for males and 5.55 [+ or -] 0.20 mm for females. Mated individuals did not differ in size from unpaired individuals. Singletons moved 44% faster than did copulating pairs (Fig. 1a): singletons moved at an average speed of 1.08 cm/s (0.99-1.16 HPDI); this decreased to 0.61 cm/s (0.51-0.71 HPDI) for pairs in copula. For singletons, average movement speed did not differ between males and females (data not shown). Size disparity had no effect on movement speed (Fig. 1b). A linear model fitted to speed as a function of the female:male size ratio had a slightly negative slope; however, the 89% HDPI overlapped zero widely (Table 1).

Copulating pairs moved slower than unpaired individuals. However, there was no relationship between the size ratio of the members of copulating pair and movement speed. I conclude that copulation comes with a marked mobility cost in this species, but it is improbable that this imposes a selection pressure for smaller male size.

There was no indication that the difference in size between male and female affected mobility. It therefore seems unlikely that there is a selective pressure causing females to prefer smaller males during precopulatory mate choice in this species (Fairbairn, 1990, 1993), assuming that the range of body sizes in this study accurately represents the range found in natural populations. Presumably, carrying larger loads should lead to greater costs; in crickets (Oecanthus nigricornis), females carrying larger egg loads have decreased mobility and are more susceptible to predation (Ercit et al., 2014). Likewise, work in water striders (A. remigis) has demonstrated that females are able to bear loads much greater than the average male weight, but increased weight bearing leads to lower mobility and higher predation (Fairbairn, 1993). If the initial struggle to reject undesired mates has energetic costs that exceed the benefits of choosiness, then females may accept males of any size, especially if male size does not affect female mobility during mating. Alternatively, large male size could be indicative of good genes and could lead females to preferentially accept larger males.

The current study design did not permit distinction between the hypotheses that weight bearing slows down females and that slower-moving females are more likely to be found in copula because they are less able to escape from males. Nevertheless, the results agree with the finding of other studies that show that weight bearing may represent a physical handicap to females and increase the predation risk (e.g., Fairbairn, 1993; Ercit et al., 2014). In water striders (A. remigis) mating duration and frequency decreases in the presence of predators (Sih et al. 1990), suggesting that mating increases predation risk. A conclusive test of the hypothesis that copulation does increase predation risk in A. tristis would involve measuring actual predation events on copulating and unpaired individuals. It is possible that decreased mobility is offset by other mechanisms that lower predation risk such as decreased conspicuousness due to decreased movement or dilution of predation risk if only one individual of the mating pair gets killed by the predator (Magnhagen, 1991).

Copulation can incur costs other than predation. Several studies have found that prolonged mating interferes with foraging (Robinson and Doyle, 1985; Stone, 1995; but see Fairbairn, 1993). Robinson and Doyle (1995) found that in amphipods, amplexus decreases male growth by as much as 45%, indicating that individuals face a trade-off between present reproduction and future size. Females are also likely to incur significant energetic costs during copulation because the larger female typically carries or drags the smaller male. Watson et al. (1998) found that the energy consumption in copulating female water striders was 24% higher when cruising and 43% higher when escaping, but they did not measure movement speed. Additionally, decreased mobility could present an obstacle to optimal behavioral thermoregulation in insects (Heinrich, 2013) if copulation prevents the pair from seeking out ideal microhabitats. Interestingly, if ideal microhabitats differ for males and females, then this cost is likely mainly borne by males because females control all movement and seek out microhabitats ideal for themselves.

This study demonstrated that copulating presents a considerable cost to mobility for A. tristis, but the degree to which mobility is impaired is not a function of the female:male size ratio. Future studies should attempt to elucidate the various selection pressures that lead to sexual size dimorphism in insects. It would be valuable to measure actual predation rates on copulating pairs and quantify the effects of copulation on growth, thermoregulation, and energy intake for both sexes.

R. Karban, E. LoPresti, P. Grof-Tisza, J. Borba, B. Reynolds, J. Weeks, and N. Booster aided in study design. R. Karban, E. LoPresti, and S. Whelan commented on an earlier draft. UC Davis-Bodega Marine Lab (Bodega Bay, California) provided the facilities where this research was carried out.

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Submitted 2 April 2017. Accepted 16 May 2017.

Associate Editor was Jerry Cook.

Hannes A. Schraft

Graduate Group in Ecology, Department of Neurobiology, Physiology, and Behavior, University of California, Davis, CA 95616

Present address: Department of Biology, San Diego State University, San Diego, CA 92182


Caption: Fig. 1-Common squash bugs (Anasa tristis) were collected at Bodega Marine Reserve on the California coast between 21 March and 23 March 2016. (a) Mean movement speed of unpaired squash bugs and pairs in copula. Boxplots show median, quartiles, and highest value within the 1.5 interquartile range. (b) Mean movement speed shows no clear relationship with the size disparity between copulating males and females. Speed was measured over 90 s in an empty arena. The line represents the mean posterior probability of a Bayesian linear model; shading represents 89% highest posterior density intervals.
Table 1--Results of a Bayesian linear model of movement
speed as a function of size disparity between copulating females
and males (n = 30 pairs) of common squash bugs (Anasa tristis
collected at Bodega Marine Reserve on the California coast
between 21 March and 23 March 2016.

Parameter   Posterior mean    89% HDPI

Intercept        1.69        -0.07-3.49
Slope           -0.96        -2.41-0.74
Sigma            0.27         0.22-0.33
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Title Annotation:common squash bug; Notes
Author:Schraft, Hannes A.
Publication:Southwestern Naturalist
Geographic Code:1U9CA
Date:Jun 1, 2017

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