Ecology Article Summary And Critique

Journal of the Tennessee Academy of Science 89(2): 51-58 August 2014

The Giant Water Bug, Belostoma lutarium (Stal): An Ideal System for Studies of Ecology, Evolution, and Behavior

Hope Klug* and Patrick Hicks

Department o f Biological and Environmental Sciences, University o f Tennessee at Chattanooga, 215 Holt Hall, Dept 2653 615 McCallie Avenue, Chattanooga, T N 37403 USA

Abstract— Parental care, sexual selection, and life history are major areas of research in evolutionary ecology. Recent theoretical work has suggested that parental care, sexually-selected traits, and life-history characteristics are expected to co-evolve with one another, and such research has highlighted a need for more studies that focus on the interactions among these traits. We begin by identifying and reviewing key directions in the field o f evolutionary ecology in relation to parental care, sexual selection, and life history. We then describe a newly-documented southeastern Tennessee population o f the giant water bug, Belostoma lutarium (Stal), that is ideal for addressing timely questions related to parental care, sexual selection, and life history. Belostoma lutarium is one o f a relatively few species that provides exclusive paternal care, which makes it particularly ideal for studies focused on the evolution o f male care. Surprisingly, the behavior o f this species has not previously been studied. We describe mating and parental care in this species and provide details of adult body size and laboratory housing conditions. We then outline how B. lutarium can be used to address specific questions related to evolution, ecology and behavior.

Introduction Understanding diversity in parental care behavior and

patterns of sexual selection is a major focus in current studies of evolutionary ecology (Clutton-Brock, 2007; Kokko and Jennions, 2008; Kokko et al., 2012; Royle et al., 2012). In particular, recent research has suggested that the evolution of parental care is influenced by mate competition and choice (Alonzo, 2012; Kokko and Jennions, 2012), mate availability (Kokko and Jennions, 2008, 2012), and general life-history traits (Klug and Bonsall, 2010; Klug et al., 2013 a, b). Likewise, sex-specific patterns of parental investment are expected to affect the strength and direction of sexual selection (Emlen and Oring, 1977; Ahnesjo et al., 2001; Shuster and Wade, 2003; Kokko and Jennions, 2008, 2012; Jennions and Kokko, 2010). As such, understanding the evolution of parental care and sexual selection requires that we examine the relationship between mate choice, mate competition, and parental care in organisms that exhibit care and are likely to experience sexual selection.

In the present work, we identify and review key directions of research that are critical for broadening our understanding of the evolution of parental care and sexual selection. We then describe a newly-documented population of the giant water bug Belostoma lutarium (Stal) (Insecta: Hemiptera) in Tennes­ see, and outline several ways in which B. lutarium could be used to address timely questions in evolutionary ecology related to parental care and sexual selection.

* Corresponding author: H. Klug, hope-klug@utc.edu

Key Directions in the Study o f Parental Care and Sexual Selection

Parental care and sexual selection are intimately linked and expected to co-evolve with one another (Kokko and Jennions, 2008; Alonzo, 2012; Kokko et al., 2012; Royle et al., 2012; Kokko and Jennions, 2012). From an evolutionary perspective, parental care is only expected to evolve and be maintained if the fitness benefits to the caring parent outweigh the costs of care (reviewed in Klug et al., 2012 and Klug and Bonsall, 2014). Parental care is typically associated with increased offspring survival and/or quality (e.g. size). However, care is also costly to parents when it decreases survival and/or reduces future reproductive opportunities (Klug et al., 2012). In particular, parental care often decreases time and energy that individuals can invest into future mating (Royle et al., 2012). The benefits and costs of parental care can be affected by basic life-history characteristics such as offspring need, stage-specific mortality, and maturation rates (Klug and Bonsall, 2010; Klug et al., 2013 a, b). For example, if adults have relatively high mortality, and hence reduced future reproductive opportunities, the fitness benefits of care are expected to be relatively high (Klug and Bonsall, 2010). Likewise, the benefits of care are expected to be greatest when offspring need care the most (Klug and Bonsall, 2010; Klug et al., 2013 a, b).

When males and females differ in the potential costs of parental care, we expect sex differences in parental care to evolve (reviewed in Kokko and Jennions, 2012), which can, in turn, affect mating dynamics and sexual selection (Kokko and Jennions, 2008; Kokko and Jennions, 2012). Likewise, when males and females differ in the sexual selection that they experience, this can affect the evolution of parental care

52 Journal o f the Tennessee Academy o f Science vol. 89, no. 2

TABLE 1. Key questions in the field of evolutionary ecology and examples of specific related questions that could be addressed in B. lutarium to enhance our general understanding o f the evolution of parental care, sexual selection, and life-history evolution.

General question: Example o f questions that B. lutarium is ideal for answering:

What are the costs and benefits of parental care, and how do these costs and benefits influence the evolution of parental care and mating dynamics?

Which sex, if any, experiences sexual selection, and if so, which traits are under sexual selection?

Which general life-history characteristics are associated with parental care?

Is there a relationship between male care behavior and future reproductive success? Is there a relationship between female parental investment (egg size and number) and future reproductive success? Does care duration influence offspring hatching success, future survival, future reproductive success, and/or size? How long are males unavailable to mate while providing parental care? Do females experience a mating ‘time-out’ period after producing eggs? What is the relative abundance of males and females that are available to mate at a given time? Does female investment in eggs (i.e., egg size and number) influence male care behavior and offspring abandonment? Are male traits, such as size and backspace area, correlated with mating success? Are female traits, such as size, correlated with mating success? Do males and females differ in the strength of sexual selection experienced? Does sexual selection change over the course of the breeding season? Are males that exhibit relatively high levels of parental care more likely to get mates in the future? How well do offspring survive in the absence of care (i.e., what is offspring need)? What is the average male and female survival during various life-history stages and how is survival influenced by care and mating? How long do individuals spend in various life-history stages?

(K okko and Jennions, 2008; Alonzo, 2010; K okko and Jennions, 2012). Indeed, there is expected to be co-evolutionary feedback between parental care and sexual selection, and, in part, this feedback is related to mate availability (reviewed in Kokko and Jennions, 2008).

If one sex provides parental care, that sex is often unavailable to mate for some period o f time due to time spent caring and/or time spent recouping resources that are required for mating (reviewed in Kokko and Jennions, 2008). If one sex is excluded from the mating pool due to this ‘time-out’ cost of parental care, the other sex will potentially have reduced mating opportunities because of the lack of opposite-sex individuals currently ready to mate. This lack o f potential mates, in turn, can lead to strong mate competition and sexual selection on the sex that does not provide parental care (Kokko and Jennions, 2008). Alternatively, a lack o f potential opposite-sex mates can select for the sex that is more common in the mating pool to provide parental care (Kokko and Jennions, 2008).

Understanding the complex link between parental care an d sexual selection requires th a t we have a detailed understanding of 1) the costs and benefits of parental care and investment by both males and females, 2) which sex (if any) experiences sexual selection, 3) which traits (if any) are under sexual selection, and 4) basic life-history characteristics such as offspring need (e.g., survival in the absence of parental care) and stage-specific m ortality and m aturation (Table 1). While many studies have focused on parental care (reviewed in Clutton-Brock, 1991 and Royle et ah, 2012), sexual selection (reviewed in Andersson, 1994), or life history (reviewed in

Stearns, 1992), relatively few studies focus on quantifying components of all three within the context o f a single species and/or a single study. As such, there is a need for more empirical studies that simultaneously focus on parental care, sexual selection, and basic life-history characteristics (Clutton- Brock, 1991; Alonso-Alvarez and Velando, 2012; Klug et ah, 2012; Klug and Bonsall, 2014). In particular, paternal care has received substantially less empirical and theoretical attention than m aternal care and has been more difficult to explain theoretically (e.g., Kokko and Jennions, 2008). As a result, more empirical studies are needed in systems in which males alone provide parental care to enhance our understanding of parental care and sexual selection (see e.g., discussion in Kokko and Jennions, 2008 and Alonzo, 2010).

We recently discovered a population of the giant water bug, Belostoma lutarium, in southeastern Tennessee. Based on our initial behavioral and population-level measurements of B. lutarium, we believe that this population could serve as an ideal study system for biologists interested in the evolution of parental care, sexual selection, and life history. Below we outline why B. lutarium is ideal for such studies in evolutionary ecology and provide suggestions for future avenues o f research in this system.

Belostoma lutarium: Ideal fo r Studies o f Parental Care and Sexual Selection

The giant water bug, Belostoma lutarium, is a small insect in which males alone provide parental care o f eggs. After mating, females adhere their eggs to the back o f their mate,

August 2014 Klug and Hicks—G iant W ater Bug: Ideal for Studies o f Evolution & Ecology 53

an d m ales are left to care for eggs fo r approxim ately tw o weeks (described in detail below). B oth m ales a n d females have the p o te n tia l to m a te m u ltip le tim es b o th d u rin g a given reproductive b o u t an d th ro u g h o u t th e breeding season. M ale m atin g success in giant w ater bugs is p o tentially lim ited by female egg p ro d u ctio n , a n d female m atin g success is p o te n ­ tially lim ited by the availability o f m ale back space (K ruse, 1990). A s such, b o th m ale a n d female traits in this species have the p o ten tial to be u n d e r sexual selection. Because B. lutarium provides p a re n ta l care a n d likely experiences m ate lim itation, it is an ideal organism for em pirical studies o f paren tal care and sexual selection. Surprisingly, B. lutarium has never previously been used in studies o f p a re n ta l care a n d sexual selection.

Below we describe characteristics o f B. lutarium th a t m ake it well-suited to studies in evolution, ecology, a n d behavior, p artic u la rly th o se focused on p a re n ta l care a n d m atin g behavior. We begin by p roviding an overview o f previous descriptive w ork on this species a n d som e relevant inform ation on closely related species. W e th e n describe th e newly docum ented p o p u la tio n o f B. lutarium fo u n d in southeastern Tennessee. W e describe the collection, behavior, a n d m o r­ p h ology o f individuals in this p o p ulation.

Overview o f Previous Inform ation on B. lu tarium

Distribution and morphology!appearance— Belostoma lutar­ ium is pred o m in an tly fo u n d in the so u th eastern U n ited States, b u t has been fo u n d as far n o rth as M ichigan a n d is fairly co m m o n in n o rth e rn states alo n g the A tlan tic seab o ard (L u ack , 1964). I t is a m edium -sized b e lo sto m a tid , w ith previous research suggesting th a t m ale lengths range from 18.5-27.5 m m a n d fem ale lengths range fro m 19.5-26.0 m m (L uack, 1964). W idths ranged from 9.4—13.5 m m fo r males, an d 10.3-13.0 m m for females (L uack, 1964). T he ovate shape o f th eir bodies an d their b row n co lo ratio n give them the ap p earan ce o f decaying leaves a n d can m ake th em difficult to distinguish from litter resting on th e substrate. T heir ventral sides, including th eir legs, are often a lighter shade o f brow n. T heir legs are ch aracterized by distinct a n d regular d a rk spots an d bands; the m iddle an d hind lim bs are b ro ad en ed and h irsute to facilitate sw im m ing (Sm ith, 1997). T hey have pow erful ra p to ria l forelim bs used for grasping prey during cap tu re a n d while feeding.

P redatory habits and diet— B elostom a lutarium is an am b u sh p re d a to r. It grasps o n to vegetation using its hind- lim bs, w hich leaves its ra p to ria l forelim bs available to seize passing prey (personal o b servation in a la b o ra to ry setting). N o studies have focused on determ ining th e com plete diet o f B. lutarium; how ever, it is assum ed to be a generalist p red ato r. Sm ith (1997) states th a t th e genus Belostom a is a know n p re d a to r o f snails, crustaceans, insects, fish, a n d larval and ad u lt am phibians. In a study on p red ato r-p rey relationships, Sw art an d T ay lo r (2004) show ed th a t B. lutarium will readily feed u p o n tadpoles o f th e frog A naxyrus fow leri.

Parental care— Like all know n m em bers o f the subfam ily B elostom atinae, B. lutarium provides p a ren tal care o f eggs. W hile p a re n ta l care in closely re la te d species has been described, a n d is likely to be fairly sim ilar to th a t o f B. lutarium, p a ren tal care beh av io r in B. lutarium has n o t been previously described in detail, an d is a p rim ary goal o f this study. Some species o f the subfam ily B elostom atinae, includ­ ing m em bers o f the genus Lethocerus, b ro o d th eir eggs on

FIG. 1. Study site, a m arsh adjacent to M o u n ta in C reek R d, C h attan o o g a, T N , an d h a b ita t o f Belostom a lutarium.

em ergent vegetation. In co n trast, males o f th e genus Belostoma b ro o d th eir eggs on their backs, w hich are deposited there by a female after several b o u ts o f co p u latio n (see Sm ith, 1979 for details o f repeated co p u latio n in a related species an d its role in p atern ity assurance). W hile encum bered w ith eggs, Belostoma m ales are assum ed to a d o p t several care behaviors w hich are th o u g h t to prim arily provide oxygen to their eggs.

Life-history stages— G ia n t w ater bugs have distinct life- history stages w hich m akes them ideal to test predictions o f basic life-history theory. Belostoma lutarium develops from an egg th ro u g h five n y m p h a l in sta rs (see M c P h e rso n an d Packauskas, 1986 fo r a description o f each instar), before m olting to an adult.

A s stated above, o u r goal is to provide m ore inform ation on the behavior an d possible utility o f B. lutarium fo r studies o f ecology, evolution, and behavior. Below, we provide basic behav io ral a n d population-level in fo rm a tio n fo r a newly described p o p u la tio n in south eastern Tennessee. Specifically, we focused on identifying th e breeding season o f B. lutarium in the p o p u latio n , quantifying the a b u n d an ce an d sex ra tio o f B. lutarium in the wild, an d providing details o f la b o rato ry housing an d rearing, behavioral observations o f m atin g a n d p a re n ta l care, a n d m o rp h o lo g ic a l m easu rem en ts o f this p o p ulation.

M aterials a n d m eth o d s

Beginning in June 2012, we identified a p o p u la tio n o f B. lutarium in a m arsh connected to M o u n ta in C reek located to th e west o f M o u n ta in C reek R o a d in C h a tta n o o g a , T N . This perm an en t m arsh, roughly th e size o f a football field, is fed by M o u n ta in C reek (Figure 1). T he m arsh is characterized by rich vegetation w ithin and a ro u n d th e w ater du rin g spring and sum m er. T he edge o f the m arsh is p o p u lated w ith large grasses, a n d the w ater bugs were typically observed a n d cap tu red w ithin 1 m o f these grasses in w ater less th a n 1 m deep. T he shallows are inh ab ited by poten tial prey species such as m innow s, tadpoles, a n d m acroinvertebrates.

W e sam pled this m arsh fo r B. lutarium betw een June 17 an d July 15, 2012 an d from M arch 19 to July 26, 2013. We m oved dip nets th ro u g h the vegetation a n d along th e su bstrate

54 Journal o f the Tennessee Academy o f Science vol. 89, no. 2

FIG. 2 a -b . G eneral ap p earan ce o f th e giant w ater bug, Belostoma lutarium (dorsal view) (2a) an d (ventral view) (2b).

to cap tu re adult w ater bugs. Each sam pling p eriod lasted for approxim ately 90 min. A d u lt bugs were stored in plastic bottles a n d transferred to a lab o ra to ry a t the University o f Tennessee a t C h attan o o g a. C annibalism w as never observed am ong adu lts during transfer. W e recorded the ab u n d an ce o f adult m ales a n d females an d the n u m b er o f cap tu red males th a t h ad eggs on their backs during each collecting trip.

In the lab o rato ry , w ater bugs were housed in aerated 10- 20 gal a q u a ria a n d /o r approxim ately 450-m L plastic cups filled w ith aged ta p w ater. A q u aria were o u tfitted w ith artificial p lan ts and an air stone. C om plete o r p a rtial w ater changes were im plem ented approxim ately every two weeks. A fter com pletion o f the study, bugs were used in o th er behavioral studies in the laboratory.

U sing dial calipers, we m easured the w idth a n d length o f the back for a sam ple o f male an d female adults collected in

2013. M easurem ents tak en include the back length from the m ost a n terio r po in t o f th e scutellum to th e m ost p o sterio r po in t o f th o rax , and the w idth o f the back at its w idest point. D escription an d diagram s o f h em ipteran anatom y, including Belostoma, can be found in M erritt an d C um m ins (1995), an d the general appearance o f B. lutarium is provided in Figs. 2a an d b. T o determ ine w hether males an d females were sexually dim orphic in size, we used a tw o-tailed stu d e n t’s f-test to determ ine w hether there were significant differences between m ales an d females in back w idth a n d /o r back length.

W e recorded the sex ratio (males/females) o f a sam ple o f a d u lt w a te r bugs c a p tu re d each m o n th in b o th years. Specimens were sexed using a dissecting m icroscope (Fisher Scientific Stereoscope M odel 1256214). T h e genital plate, found on the m ost p o sterio r p o rtio n o f the abd o m en , has a few distinct differences am ong males (Figure 3a) an d females

FIG. 3 a-3 b . G en ital p late o f a male Belostom a lutarium (3a). N o te the lack o f setal tufts. G enital plate o f a fem ale Belostoma lutarium (3b).

August 2014 Klug and Hicks—Giant Water Bug: Ideal for Studies of Evolution & Ecology 55

TABLE 2. Abundance of male and female B. lutariwn collected in the M ountain Creek m arsh June 17-July 15, 2012. The num ber o f males found with eggs on their back(s) is shown in parentheses.

Date Total number of males

(number with eggs) Total number of

females

June 17 8 (2) 2 June 27 1 (1) 3 June 30 1 (0) 9 July 4 2 (1 ) 6 July 10 2 (0 ) 1 July 15 1 (0) 11

Total 15(4) 32

(Figure 3b). The most conspicuous difference is the numerous setae present on the female genital plate, especially along the posterior tip of the plate (Fig. 3a and 3b). The setae may appear in two small patches on either side o f the midline. Males usually lack setae in this area or may display a few setae. The tip of the genital plate in males is rounded, whereas females may have a notched or split tip. To determine whether sex ratio o f captured individual was significantly biased, we calculated sex ratio (males/females) for each m onth and categorized each month as male-biased, female-biased, or unbiased. We then used a one-sample t-test to determine if sex ratio was on average biased across months.

To observe m ating and parental care behavior, various male-female combinations were each placed in a 10-gallon aquarium and observed for 20 min per day for five days. These included pairs (N = 5), two male and four female com­ binations (N = 5), and four male and two female combinations (N = 5). We describe mating and parental care behavior below.

TABLE 3. Abundance of male and female B. lutarium collected in the M ountain Creek m arsh M arch 19-July 26, 2013. The number of males found with eggs on their back(s) is shown in parentheses.

Total number of males Total number of Date (number with eggs) females

March 19 0 0 April 12 1 (0) 1 April 30 5(?) 7 May 2 0 0 May 7 2(1) 0 May 20 3(3 ) 0 May 24 0 0 May 31 1 (1) 1 June 8 4 (1 ) 6 June 28 1(0) 4 July 13 3(2) 5 July 26 KD 1

Total 21(9) 25

TABLE 4. Adult sex ratio (males/females) of collected B. lutarium during June and July o f 2012 and A pril-July 2013.

Year Month Sex ratio

(males/females) Bias

2012 June 0.71 Female July 0.28 Female

2013 April 0.75 Female May 6 Male June 0.5 Female July 0.67 Female

Results

Abundance and sex ratio o f adult B. lutarium in 2012 and 2013—We first identified the M ountain Creek population of B. lutarium on June 17, 2012. Adults and nymphs were captured regularly until July 15, 2012 (Table 2), after which no B. lutarium individuals were found in 2012. In 2013, adults of B. lutarium were first observed on April 12, 2013 (Table 3) and captured regularly until July 26, 2013, after which no adults were observed. Nymphs were first observed in early May 2013. Thus, the breeding season of this B. lutarium population appears to span April through July. During four out o f the six m onths that B. lutarium individuals were found in the marsh, the sex-ratio was female biased (Table 4). Indeed, across months, the sex ratio was significantly female-biased (two- tailed student’s t-test, t = 7.0, d f = 5, P = 0.001).

Morphological measurements—Males captured in 2013 had back widths o f 11.32 ± 0.34 mm (mean ± SD) and back lengths o f 16.21 ± 0.73 mm (mean ± SD). Females had back widths of 11.44 ± 0.51 mm (mean ± SD) and back lengths of 16.35 ± 0.82 mm (mean ± SD). There was no significant difference between male and female back widths (FJ22 — 0.49, P = 0.49) or between male and female back lengths ( F , 32 = 0.29, P = 0.59), suggesting no sexual dimorphism in back size in this population.

Mating behavior—Adult B. lutarium readily bred in the laboratory in all male-female combinations described above. Prior to mating, males were often seen display-pumping at the surface, and we hypothesize that this pumping behavior might be used to attract female mates or function as a form of communication between individuals. Pumping involves a longitudinal up-and-down body movement, like a push-up (see also Smith, 1997). After courtship, multiple bouts o f ovipositing occurred over a span o f several hours (e.g., in Fig. 4 a female is depositing eggs on the back of a male shortly after copulating; for a description o f breeding behavior in a closely related species, see Smith, 1979). When breeding was successful and eggs were deposited on the back of a male in the laboratory, the number of eggs deposited ranged from 44 to 87. Egg-encumbered males in nature were never found with fewer than 83 eggs. If females were kept in isolation without males, a small number o f females deposited eggs on the artificial vegetation in the aquarium.

Parental care behavior— After egg deposition, several parental care behaviors were observed. First, males with eggs positioned themselves at the surface. While at the surface, the eggs are partially exposed to the air (Fig. 5). This likely allows

56 Journal o f the Tennessee Academy o f Science vol. 89, no. 2

FIG. 4. A pair of Belostoma lutarium mating. The female is seen ovipositing on the male’s back.

sufficient oxygen exchange while also keeping the eggs moist (Smith, 1997). Second, brood pumping was commonly observed. Brood pumping is similar to the display pumping described above except that it occurs frequently under the surface and at a slower rate than display pumping (Smith, 1997). Third, males were also observed engaging in a behavior which involved stroking their eggs using their hind legs. In B. flumineum, this behavior may aid nymphs in freeing themselves from their eggs (Smith, 1979). We hypothesize that egg stroking in B. lutarium might also function to clean the eggs of debris or other material and/or provide stimulation that could improve development. No egg predators were present in our laboratory set-up, but in the wild, males also likely protect their eggs from predators. Fish, which are a likely egg predator (Smith and Horton, 1998), were commonly observed near water bugs in the marsh.

Egg abandonment was also frequently observed. Egg pads were commonly scraped off by parental males; this typically occurred within the first day or two of care. Additionally, two cases of filial cannibalism (i.e., the consumption of one’s own offspring) were observed. After removing small egg pads from their backs, two males were seen cannibalizing their eggs. Similar behaviors were also observed in a study of B. flumineum (Smith, 1976). Hatching occurred roughly 17 days after deposition.

Discussion

Here, we have provided basic behavioral and population- level information for a newly-described population of Belo­ stoma lutarium in southeastern Tennessee. Specifically, we found that the breeding season of the Mountain Creek population of B. lutarium extends from April through July, the sex ratio is typically female-biased across months in the wild, and males and females were not sexually dimorphic with respect to back size. In a laboratory setting, B. lutarium mated in pairings that included one male and one female, two males and four females, and four females and two males, suggesting that individuals breed readily in aquaria. Behaviorally, prior to mating males exhibited display pumping, and after mating, their parental care behavior included brood pumping, remain­ ing at the surface such that eggs were exposed to the air, and

FIG. 5. Male Belostoma lutarium with eggs at water surface.

egg stroking behavior. Egg abandonment and filial cannibal­ ism by males were also observed.

Belostoma lutarium is ideal for studies of ecology, evolution, and behavior (outlined in Table 1). Adults are easily maintained and observed in a laboratory setting, which will allow for future experimental studies. Additionally, they exhibit exclusive paternal care, which is relatively uncommon (Clutton-Brock, 1991; Royle et al., 2012; Kokko and Jennions, 2008) and remains an evolutionary conundrum (reviewed in Kokko and Jennions, 2008, 2012). Recent reviews have highlighted the need for more studies that focus on under­ standing the evolution of paternal care (e.g. Kokko and Jennions, 2008; Alonzo, 2010; Klug et ah, 2012). Belostoma lutarium is well-suited for determining what selective factors play a role in maintaining paternal care (outlined in Table 1). Smith (1997) hypothesized that selection for larger body size, and hence, larger eggs, is the driving force maintaining paternal care within giant water bugs in general. Specifically, he argues that larger eggs require brooding because brooding provides sufficient 0 2 which allows larger eggs to survive and develop (Smith, 1997). In the future, it would be interesting to explicitly examine the costs and benefits of brooding behavior in relation to oxygen availability and size at hatching in B. lutarium (Table 1). Such a study would provide insight into whether brooding and oxygen availability influence body size, and whether larger body size is a likely driver of paternal care.

Sexual selection might also play a role in maintaining paternal care. The operational sex ratio (i.e., ratio of males and females that are prepared to mate at a given point in time, OSR; Emlen and Oring, 1977) likely shifts throughout the breeding season in giant water bugs. In a study on the related species B. flumineum in Illinois, Kruse (1990) found that male back space is limited only during early spring when animal density is low and the sex ratio is female biased. During this time period, one would expect females to compete for males, and as a result sexual selection will potentially favor female traits that improve their access to male mates. Similarly, in the giant water bug, Abedus indentatus, in California, male back space was found to limit female mating at certain points during the breeding season (Kraus, 1989). In our study, the adult sex ratio of B. lutarium was female biased, which might lead to male mate choice and female competition for mates in this population. In B. lutarium, it will be key for future studies to examine whether males or females are mate limited and identify potential traits (e.g., body size in males or females,

August 2014 Klug and Hicks—Giant Water Bug: Ideal for Studies of Evolution & Ecology 57

parental care in males) that are under sexual selection (Table 1). Additionally, examining any shift in the operational sex ratio throughout the breeding season is an ideal avenue of future research. Such work could provide insight into plasticity in sex roles and examine the link between paternal care, sexual selection, and OSR.

The distinct life-history stages of giant water bugs could be used to answer timely questions related to life-history evolution. For example, classic life-history theory predicts that an increase in predation risk should select for nymphs that have increased size at hatching. Whether there are differences in the size of offspring from a single pad or across egg pads, and whether such size differences influence predation risk is an interesting focus for future studies. If larger nymphs have a higher chance of survival, this could play a part in maintaining paternal care (see also Smith, 1997). In addition, recent studies have suggested that stage- specific maturation and mortality rates will influence the evolution of parental care (Klug and Bonsall, 2010; Klug et al., 2013 a, b). The fact that B. lutarium has distinct life- history stages makes this species well-suited for examining the link between life-history characteristics (e.g., maturation rate and egg, juvenile and adult mortality) and parental care. Characterizing stage-specific mortality and maturation rates would provide insight into the characteristics that are likely to be associated with paternal care (Table 1).

Belostoma lutarium is also ideal for studies of offspring abandonment. As mentioned above, egg pad removal by the encumbered males was common. Anecdotally, it appeared that the smaller egg pads were more commonly discarded than larger pads. This possibly allows the male to breed again and obtain a larger egg pad, potentially increasing his fitness. Consistent with this idea, Kight and Kruse (1992) found that B. flumineum males are more likely to discard smaller egg pads prior to hatching. However, they also determined that the likelihood of discarding eggs decreases as eggs age. In the future, it would be interesting to examine the relationship between egg pad size and discarding behavior in B. lutarium. In particular, if males discard pads in order to increase their chances of receiving a larger egg pad in the future, one might expect OSR to influence discarding. For example, males may be less likely to discard small egg pads during times when females are scarcer.

In summary, B. lutarium is an ideal system for ecological, evolutionary, and behavioral studies. There is limited research on B. lutarium and other giant water bugs. Paternal care is a key life-history trait and a major focus in studies of behavior of behavior and evolution. The fact that B. lutarium provides parental care, likely experiences sexual selection, and is easily housed and studied in the lab makes this species ideal for a range of future studies.

Acknowledgments

We are grateful for the assistance provided by S. Chatzimanolis (University of Tennessee at Chattanooga) in identifying and sexing B. lutarium. We are also appreciative of E. Reyes (University of Tennessee at Chattanooga) and P. Thrasher (University of Tennessee at Chattanooga) for their assistance in the laboratory and T. Gaudin (University of Tennessee at Chattanooga) for his help photographing the

water bugs. We also appreciate the detailed comments from the referees which greatly improved this manuscript.

Literature Cited

Ahnesjo, I., C. Kvamemo, and S. Merilaita. 2001. Using potential reproductive rates to predict mating competition among individuals prepared to mate. Behavioral Ecology, 12:397—401.

Alonzo, S. H. 2010. Social and coevolutionary feedbacks between mating and parental investment. Trends in Ecology and Evolution, 25:99-108.

Alonzo, S. H. 2012. Sexual selection favours male parental care, when females can choose. Proceedings o f the Royal Society o f London Series B-Biological Sciences, 279: 1784-90.

Alonso-Alvarez, C., and A. Velando. 2012. Benefits and costs of parental care. Pp. 40-61 in The Evolution o f Parental Care (N. J. Royle, P. T. Smiseth, and M. Kolliker, eds.). Oxford University Press, Oxford, United Kingdom.

Andersson, M. 1994. Sexual Selection. Princeton University Press, Princeton, New Jersey.

Clutton-Brock, T. H. 1991. The Evolution o f Parental Care. Princeton University Press, Princeton, New Jersey.

Clutton-Brock, T. H. 2007. Sexual selection in males and females. Science, 318:1882-1885.

Emlen, S. T., and L. W. Oring. 1977. Ecology, sexual selection, and the evolution of mating systems. Science, 197: 215-223.

Jennions, M. D., and H. Kokko. 2010. Sexual selection. Pp. 343-364 in Evolutionary Behavioral Ecology (D. F. Westneat, and C. W. Fox, eds.). Oxford University Press, New York, New York.

Kight, S. L., and K. C. Kruse. 1992. Factors affecting the allocation of paternal care in waterbugs (Belostoma flumineum Say). Behavioral Ecology and Sociobiology, 30:409-A14.

Klug, H., and M. B. Bonsall. 2010. Life history and the evolution of parental care. Evolution, 64:823-835.

Klug, H., M. B. Bonsall, and S. H. Alonzo. 2013 a. The origin of parental care in relation to male and female life-history. Ecology and Evolution, 3:779-791.

Klug, H., M. B. Bonsall, and S. H. Alonzo. 2013 b. Sex differences in life history drive transitions between maternal, paternal and bi-parental care. Ecology and Evolution, 3:792-806.

Klug, H., and M. B. Bonsall. 2014. The benefits of par­ ental care in relation to increased offspring survival and parental effects on developmental rate. Ecology and Evolution. Published online early: DOI: 10.1002/ ece3.1083

Klug, H., S. H. Alonzo, and M. B. Bonsall. 2012. Theoretical foundations of parental care. Pp. 21-39 in The Evolution o f Parental Care (N. J. Royle, P. T. Smiseth, and M. Kolliker, eds.). Oxford University Press, Oxford, United Kingdom.

Kokko, H., and M. D. Jennions. 2008. Parental investment, sexual selection and sex ratios. Journal of Evolutionary Biology, 21:919-948.

Kokko, H., and M. D. Jennions. 2012. Sex differences in parental care. Pp. 101-116 in The Evolution o f Parental Care (N. J. Royle, P. T. Smiseth, and M. Kolliker, eds.). Oxford University Press, Oxford, United Kingdom.

58 Journal o f the Tennessee Academy o f Science vol. 89, no. 2

Kokko, H., H. Klug, and M. D. Jennions. 2012. Unifying cornerstones of sexual selection: operational sex ratio, Bateman gradient, and the scope for competitive invest­ ment. Ecology Letters, 15:1340-1351.

Kraus, W. F. 1989. Is male back space limiting? An investigation into the reproductive demography of the giant water bug, Abedus indentatus (Heteroptera: Belosto- matidae). Journal o f Insect Behavior, 2:623-648.

Kruse, K. C. 1990. Male backspace availability in the giant waterbug (Belostoma flumineum Say). Behavioral Ecology and Sociobiology, 26:281-289.

Lauck, D. R. 1964. A monograph of the genus Belostoma (Hemiptera) Part III. Bulletin o f the Chicago Academy o f Sciences, 11 (5): 102-154.

McPherson, J. E., and R. J. Packauskas. 1986. Life history and laboratory rearing of Belostoma lutarium (Heteroptera: Belostomatidae) with descriptions of immature stages. Journal o f the New York Entomological Society, 94: 154-162.

Merritt, R. W., and K. W. Cummins. 1995. An Introduction to the Aquatic Insects o f North America, 3rd Edition. Kendall/ Hunt, Dubuque, Iowa.

Royle, N. J., P. T. Smiseth, and M. Kolliker. 2012. The Evolution o f Parental Care. Oxford University Press, Oxford, United Kingdom.

Shuster, S. M., and M. J. Wade. 2003. Mating Systems and Stra­ tegies. Princeton University Press, Princeton, New Jersey.

Smith, R. L. 1976. Brooding behavior of a male water bug Belostoma flumineum (Hemiptera: Belostomatidae). Jour­ nal o f the Kansas Entomological Society, 49:333-343.

Smith, R. L. 1979. Paternity assurance and altered roles in the mating behavior of a giant water bug Abedus herberti (Heteroptera: Belostomidae). Animal Behaviour, 27:716-725.

Smith, R. L. 1997. Evolution of paternal care in the giant water bugs (Heteroptera: Belostomatidae). Pp. 116-149 in Social Behavior in Insects and Arachnids (J. C. Choe, and B. J. Crespi, eds.). Cambridge University Press, London, United Kingdom.

Smith, R. L., and C. Horton. 1998. Fish predation on giant water bug (Heteroptera: Belostomatidae) eggs in an Arizona stream. Great Basin Naturalist, 58:292-293.

Stearns, S. 1992. The Evolution o f Life Histories. Oxford University Press, Oxford, United Kingdom.

Swart, C., and R. Taylor. 2004. Behavioral interactions between the Giant Water Bug (Belostoma lutarium) and tadpoles of Bufo woodhousii. Southeastern Naturalist, 3:13-24.

Manuscript received 9 October, 2013; Manuscript accepted 1 August, 2014.

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