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1993 The Relationship between Lifespan and Reproduction in the Giant Waterbug ( flumineum) Wendy Nixdorf This research is a product of the graduate program in Zoology at Eastern Illinois University. Find out more about the program.

Recommended Citation Nixdorf, Wendy, "The Relationship between Lifespan and Reproduction in the Giant Waterbug ()" (1993). Masters Theses. 2139. https://thekeep.eiu.edu/theses/2139

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Date Author

m The relationship between lifespan and reproduction in the giant waterbug (Belostoma flumineum). (TITLE)

BY

Wendy Nixdorf

THESIS

SUBMITIED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF

Master of Science

IN THE GRADUATE SCHOOL, EASTERN ILLINOIS UNIVERSITY CHARLESTON, ILLINOIS

1993 YEAR

I HEREBY RECOMMEND THIS THESIS BE ACCEPTED AS FULFILLING THIS PART OF THE GRADUATE DEGREE CITED ABOVE

DATE ABSTRACT

The evolutionary significance of senescence and death is poorly understood. Life history theory suggests that the allocation of energy to growth or reproduction is necessarily associated with a decrease in energy available for maintenance of the soma. This study attempted to determine if an investment in reproduction would decrease longevity in the giant waterbug (Belostoma flumineum). Male and female waterbugs were collected from the field as last instar stage nymphs and maintained under controlled laboratory conditions. Individuals were randomly assigned to mating effort treatments, (virgins or breeders with breeding efforts ranging from 1 to >5 times). Following breeding, one half of the males had their egg pads artificially removed whereas the other half were allowed to brood eggs pads through hatching. Female waterbugs lived, on average, longer than males; though when considered by level of mating effort the difference was statistically indistinguishable. Neither breeding nor number of breeding efforts had a detrimental effect on lifespan; virgins and breeders lived for approximately the same length of time. There was no significant difference between the lifespan of brooding and non-brooding males. Both male and female waterbugs that were paired with the opposite sex, yet

i yet failed to breed, died significantly sooner than either virgins or breeders; casual factors for this decreased longevity are uncertain. There was a significant positive relationship between age at first reproduction and age at death in both male and female waterbugs; those bugs that bred early in life died sooner than those that bred for the first time late in life. These results suggest that male and female waterbugs pay a longevity cost by reproducing early in life.

ii ACKNOWLEDGMENTS

I would first like to thank Dr. Kipp Kruse for serving as my graduate advisor. I could always count on him for help when problems developed, advice when I needed it, motivation when I got lazy and, most importantly, a good laugh when things got boring. I would like to thank Dr. Eric Bollinger and Dr. Michael Goodrich for comments on the thesis and for serving on my graduate committee. Thanks also go to Dr. Charles Costa for the use of his computer and for help with the figures. I have to thank Colin Smith for sweating it out with me in the "bug house"; I couldn't have done it without his help. Thanks also to Jimmie Griffiths, Nancy Johnson, Lori Davis and Roger Jansen for wading into the mud to collect bugs with me. Thanks to my friends and especially to my family for supporting me. No matter where I go, I always have a great place to go home to (even if I don't have a bed to sleep in!).

iii TABLE OF CONTENTS

Cover Page Abstract i Acknowledgments iii Table of Contents iv Introduction 1 Materials and Methods 7 Results 11 Discussion 15 Literature Cited 22

Table 1 29 Table 2A&B 30 Figure lA,B,C,D Legend 31 Figure 2A,B,C,D Legend 32

Figure 3 Legend 33

Figure 4A,B,C,D Legend 34

Figure 5 Legend 35

Figure 6A,B,C Legend 36

iv INTRODUCTION

No organism survives indefinitely even when maintained under "ideal conditions" where resources are readily available and the threat of predation, competition and disease are removed. In this situation, individuals continue to experience a persistent decline in age-specific fitness components due to some internal physiological decline (Rose 1991). The decrease in the likelihood of survival with increasing chronological age has been termed senescence (Comfort 1954; Medewar 1955). The evolutionary explanation of senescence has been ascribed to the decline in the force of natural selection with age (Rose 1984, 1991; Finch 1991). Prior to the onset of sexual maturity, lethal mutations are selected against because affected individuals do not bear offspring. Lethal or deleterious alleles that do not exert their effects until late in life may not be selected against and could persist within the population (Medewar 1955). Williams (1957) was the first to speculate how pleiotropic genes may play a role in senescence by suggesting that alleles with detrimental effects occurring, after reproduction, could actually be selected for if they also carried effects that improved fitness early in life. This theory, known as "antagonistic pleiotropy," is considered a likely candidate for explaining senescence (Charlesworth 1980;

1 Rose and Charlesworth 1980; Rose 1984, 1991; Finch 1991). Senescence may play an important role in the evolution of life history characteristics. According to the "principle of allocation," natural selection optimally allocates resources among growth, maintenance and reproduction (Gadgill and Bossert 1970; Pianka 1988). When resources become limited, competition occurs for the allocation of these resources; resources allocated to one area is thought to be associated with a decrease in resources available to other areas (Bell 1984; Reznick 1985). If, for example, environmental hazards (e.g., predation, disease) are likely to kill an individual early in its life, natural selection should favor individuals who invest more energy in reproduction than in maintenance. In contrast, species that are likely to survive longer should divert relatively more energy into maintenance. Known as the "disposable soma" theory, this suggests that energy should be invested to maintain the soma for only the expected period of vigor whereas the remainder should be used for reproduction (Kirkwood 1985, 1987). It is generally assumed that there is a inverse relationship between reproduction and longevity (Bell 1984; Reznick 1985). organisms that reproduce are faced with costs that may decrease their longevity. For example, individuals may encounter ecological costs

2 which include exposure to predators during oviposition or while guarding eggs or young (Bell 1984; Tallamy 1984). Physiological costs may also be incurred when energy used for egg production or other reproductive activities is not available for maintenance. Furthermore, the increases in the size of reproductive organs that occur during breeding may constrict and reduce the effectiveness of other organs that are essential for normal maintenance. (Calow 1954; Tallamy and Denno 1982). Some research has shown that individuals that breed die sooner than their virgin counterparts (Tinkle 1969; Snell and King 1977; Law 1979; Tallamy and Denno 1982; Feifarek, Wyngaard and Allen 1983; Partridge, Green and Fowler 1987; Fowler and Partridge 1989; Reznick 1992); there has, however, been evidence to the contrary (Haukioja and Hakala 1978; Dean 1981; svard and Wiklund 1988). Most research dealing with the relationship between longevity and reproduction has been devoted to females, since they generally have the greater parental investment than males (Trivers 1972). The cost of reproduction to males has generally been thought to be minimal (Partridge and Andrew 1985;

Hayashi 1993). Recently, work with the nematode~ elegans suggested that males may also pay a longevity cost associated with sperm production (VanVoorhies 1992) • have been utilized extensively in aging

3 research for several reasons: (1) the lifespan of insects is relatively short so several generations can be investigated in a relatively short period of time; (2) insects are often available in large numbers, and can be generally easily maintained and will breed in captivity; and (3) though physiology can be complex, it is well known for several species (Lints 1985). There has not been any work investigating the cost of parental investment and reproduction in a relatively short-lived iteroparous species in which both males and females contribute significantly to each brood. This is primarily due to the fact that there are very few species in which the male exclusively provides postcopulatory care to the eggs. One group in which this occurs is the giant water bugs (: ). The subfamily Belostomatinae contains nearly 100 species, in which males provide exclusive postcopulatory parental care. In the giant waterbug, (Belostoma flumineum) both males and females participate in courtship, but successful courtships depend on the male's performance of a precopulatory display called "brood pumping" (Smith 1979). This behavior is similar to that used by egg­ laden males to aerate developing eggs and could help females assess paternal ability (Smith 1979; Thornhill and Alcock 1983). Mating consists of alternating bouts

4 of copulation and oviposition that are controlled by the male (Smith 1979). The female deposits her eggs on the male's back in a pad of mucilaginous cement with size of egg pads ranging from 60-195 (Menke 1960; Smith 1976a, Kruse 1990). Encumbered males stroke the eggs and stay near the water's surface to keep the eggs exposed to air. These brooding behaviors keep the eggs clean, aerated and free from parasites (Smith 1976a; Kraus, Gonzalese and Vehrencamp 1989). When egg pads are removed and placed in either standing water or air, all eggs fail to hatch (Smith 1976a). This suggests that male brooding behaviors are vital to egg survival and hatching. After brooding 6-12 days the eggs hatch and the egg pad is discarded (Torre Bueno 1906, Kruse 1990). Brooding is not without cost to males. As eggs develop they increase in length and may increase the cross-sectional thickness of a male by more than 60% (Smith 1976b) . These encumbered males have slower swimming speeds and are less efficient at capturing active prey (Smith 1976b; Crowl and Alexander 1989). Encumbered males have also been found to be more vulnerable to predators (Kruse, personal communication). More importantly, males are unable to breed again until their current brood hatches and the pad is discarded. After oviposition, females contribute no more to the care of the eggs or young. If prey are available, they are able to quickly synthesize additional eggs and

5 will deposit partial clutches when they encounter a second available male (Kruse 1990). If males are unavailable, females continue to produce eggs and will lay them on available vegetation or even other females (Smith 1979; Kruse and Leffler 1984; personal observ.). Since both males and females invest heavily in each brood and breeding opportunities can be manipulated, this species makes an interesting subject for a study investigating the trade-off between reproduction and longevity. This study was designed to investigate how reproductive effort affects longevity in both male and female waterbugs maintained under controlled laboratory conditions.

6 MATERIALS AND METHODS

Giant waterbugs were collected as last instar nymphs from ponds in Coles County, IL, USA in July and August 1992 using aquatic dip nets. Nymphs were transported to the laboratory in plastic coolers containing pond water and aquatic vegetation. Once in the lab, nymphs were placed in 40-1 aquaria filled with approximately 20 cm of deionized water along with plastic aquarium plants which served as perching sites. All waterbugs were maintained at a temperature between 25-30 c under 14L:lOD and fed crickets fill libitum. Adults used for matings were also collected and maintained as described above. Nymphs were checked every 24 hours and were placed in individual 1-1 plastic circular containers with plastic perching materials the day they emerged as adults. Day of emergence was recorded and considered to be day one of adult life. Within five days of emerging, gender was determined and all bugs were individually marked. Sex is determined by examining the genital plate; females posses two apical tufts, whereas males lack these structures (Menke 1960). Marking involved placing a number on the pronotum with a fountain pen using liquid paper, which was then covered with a thin layer of cyanoacrylate glue and allowed to dry. Water in both containers and aquaria was changed

7 weekly. Twice a week each waterbug was given one live cricket. The containers were covered with a glass plate to prevent the crickets from escaping. After 48 hours, all dead crickets were removed. Experiment I This experiment was designed to investigate the effect of reproduction on longevity in male waterbugs. Ten males were randomly designated to remain virgins and were maintained individually in containers from emergence until death. The remaining males were randomly divided into four groups of ten individuals; each group was randomly assigned a specific number of mating efforts (1, 3, 5, or greater than 5). A mating effort was defined as becoming egg-laden, brooding until the eggs hatch, then discarding the egg pad. Beginning on day 14 of adult life, I placed each male in an aquarium with gravid females. Tanks were checked daily and all encumbered males removed and placed in individual containers and allowed to brood eggs to hatching. I collected all discarded egg pads and ruptured egg cases were counted on each pad. After discarding the egg pad, males remained in individual containers for 14 days before being returned to the aquaria with females. After completing the assigned number of mating efforts, males were kept in individual containers until their death.

8 Experiment II In this experiment, I assessed the longevity costs of brooding eggs by males. Males were randomly divided into the same mating effort categories as Experiment I. In order to determine costs of brooding, egg pads were gently scraped from the males back and counted within 24 hours of being deposited. once egg pads were removed, males were placed in individual containers for 14 days before being returned to the aquaria with females. As in Experiment I, after the assigned number of mating efforts was completed, males remained in individual containers until day of death. Experiment III This experiment involved investigating the longevity costs of reproduction in female waterbugs. Females were randomly divided into the same mating effort categories as males in Experiments I and II. As with males, virgins were kept in individual containers from emergence until death. Each breeding female was kept in a individual container until being placed in a aquarium with 7-10 unencumbered males for 24 hours. Males were then checked and any eggs that had been laid were attributed to that female. I collected and counted all egg pads. If breeding occurred, females were kept in individual containers for 14 days before being returned to a aquarium containing males. If no breeding occurred, females were continually placed with males

9 every 5-7 days for 24 hours until breeding occurred. Any eggs found on the plastic vegetation or sides of the container were counted and removed. After completing the assigned number of mating efforts, females remained in individual containers until death. Waterbug longevity (day until death) was monitored and recorded for each individual waterbug. All waterbugs living less than 100 days were not considered in the data analysis (8 males were excluded while only one female failed to live at least 100 days). Age at death was analyzed with either an independent t-test or a one-way ANOVA. Unless otherwise specified, a Newman­ Keul 's Means Comparison Test was used to reveal any significant differences between means. Comparisons of percent of life spent with opposite sex were completed after the data were transformed using the arcsine transformation (Zar 1984). Pearson Product Moment Correlation was used to determine potential relationships among several variables. An alpha value of less than 0.05 were used to determine the significant difference in all hypothesis testing procedures.

10 RESULTS

Longevity (age at death) was determined for a total of 49 female and 81 male waterbugs; individuals lived an average of 205.9 days (sd=57.3, n=130), irrespective of gender or lifetime mating effort. Though not quantified

in this study, waterbugs ~ithin 3-4 days of death from senescence are easily discernable. Both male and females become a deep brown, almost black color, become extremely lethargic and their swimming ability is highly diminished. Females, on average, lived longer than male waterbugs (tcal=-2.5899, df=128, P=0.0048; Fig. lA). However, when separated into mating effort categories, the difference between the sexes becomes statistically indistinguishable. For example, virgin females lived, on average, only 12 days longer than virgin males (tca1=0.4497, df=27, P=0.3282; Fig. lB). Male waterbugs designated to be "virgins" in both the brooding and non­ brooding experiments were found to not differ significantly in age at death (tcal=-0.1728, df=17, P=0.4324) and were pooled into a "virgin male" category. Males in both experiments that were paired with females yet failed to breed, were also found to not differ in mean age at death (tcal=.9024, df=30, P=0.1870) and were also subsequently considered collectively as males that did not bred. Similar to virgins, females waterbugs

11 that were paired with males but did not breed lived only 10 days, on average, longer than males who were paired with females but failed to breed (tcal=-0.6020, df=38, P=0.2754; Fig. lC). There was also no difference in age at death between breeding females and brooding and non­ brooding males (F2 , 58=1.0l63, P=0.3683; Fig. 10). There was a significant difference in the mean age at death among virgin females; those individuals who· were exposed to males yet failed to breed (zero) and breeders (F2 , 46=3.25, P=0.0476; Fig. 2A). A means comparison procedure revealed that non-breeders died sooner than virgins or breeders, whereas the two latter categories were statistically indistinguishable. There was a significant difference in mean age at death for females that bred one, two or more than two times (F2 , 28=3.502, P=0.0439, Fig. 2B). A means comparison test showed that female waterbugs that bred more than two times lived significantly longer than those that bred one time. However, there was no difference between those females that bred one or two times and those that bred two or more times. Similarly, there was a significant difference in age at death among virgin males, those that were paired with females yet failed to breed (zero), brooders and non-brooders (F3 , 77=4.818, P=0.004; Fig. 2C). A means comparison procedure revealed that there was no significant difference between virgins, brooders and

12 non-brooders, whereas males that bred zero times died significantly sooner than the other three categories. Descriptive statistics for days and percent of life spent paired with the opposite sex can be found in Table 1. There was no significant difference in percent of life spent with males between breeding females and those females that were paired with males but failed to breed (tca1=0.1126, df=38, P=0.4515). There was also no difference in percent of life spent with females between brooding males and non-brooding males (tcal=0.6330, df=28, P=0.2659) so they were pooled together as breeder males. There was, however, a significant difference in percent of life spent with females between breeder males and those males that failed to breed (tca1=5.6672, df=60, P<0.0001); males that failed to breed spent, on average, 10 percent more of their life with females. In males that bred but did not brood, the number of breedings had no effect on age at death. Individuals that bred one time lived approximately the same length of time as males that bred more then once (tca1=-0.9187, df=16, P=0.1859; Fig. 2D). Descriptive statistics for egg production in females as well as egg pad size and brooding times in males can be found in Table 2A & B. Age at first reproduction appears to affect longevity in both males and females. There was a significant positive correlation between age at first

13 DISCUSSION

The principal objective of this research was to determine if an investment of time and/or energy in reproduction is associated with a concomitant decrease in longevity (age at death) in both male and female giant waterbugs, (Belostoma flumineum). If there is a trade-off between reproduction and maintenance as the "principle of allocation" suggests (Pianka 1988), I would expect mated waterbugs to die significantly sooner than their virgin counterparts and lifespan to decrease as parental investment increases. Similarly, if the parental care that male waterbugs provide to their eggs is energetically demanding, then males that have their egg pads artificially removed should live longer then males that brood their egg pads until hatching. There is evidence to suggest that a negative relationship between reproduction and longevity does, in fact, exist. In rotifers (Snell and King 1979), fruitflies (Partridge et al. 1989), lace bugs (Tallamy and Denno 1982), blue tits (Nur 1984), meadow grass (Law

1979) and the nematode ~ eleqans (VanVoorhies 1992) mated individuals have lower survival rates than their unmated counterparts. The observed decreases in mated female lifespan may be related to egg production. When ovarian activity or egg production in flour beetles (Tribolium confusum) and fruitflies (Drosophila

15 subobscura) is experimentally reduced by either radiation or high temperatures, longevity was increased (Cork 1957; Maynard Smith 1958; Lamb 1964; Ducoff 1986). In direct contrast, Fowler and Partridge (1989), found that the lifespan of female Drosophila melanogaster with high mating frequencies was shorter than that of females with low mating frequencies, while egg production between the two was not significantly different. This suggests that the physical act of mating was itself detrimental to female fruitfly longevity. There have, however, also been reports that demonstrate no relationship between reproduction and longevity in mussels (Andonta) (Haukioja and Hakala 1978), grasshoppers (Melanoplus) (Dean 1981), and butterflies (Danaus) (Svard and Wiklund 1988). My results indicate that mating, as well as the number of matings, had no effect on waterbug lifespan in either males or females. However, age at first reproduction did influence future survival in this species. Breeding waterbugs, regardless of sex, lived for approximately the same length of time as virgins suggesting that mating itself does not decrease lifespan in waterbugs. This is further corroborated by the fact that increasing number of mating efforts did not negatively affect lifespan. In fact, I found that increasing number of mating efforts seemed to increase longevity. This result may be explained by the fact

16 that long life is accompanied by in an increase in the number of opportunities to breed. All bugs were fed ad libitum throughout all experimentation and it is possible that mating does not incur a longevity cost under these conditions. Female waterbugs that never come in contact with males continue to produce eggs and will deposit them on any available structure (Smith 1979; person. observ.). Consequently, virgin females in this study were still producing eggs which could have associated longevity costs. It would be valuable to compare the lifespans of female waterbugs that had either ovarian activity or egg production halted to virgin females and breeders who produced eggs to determine if egg production affects lifespan. I expected to see an increase in longevity in male waterbugs that had their egg pads removed when compared to males that brooded egg pads through hatching. It is known that egg pads increase the cross-sectional thickness of males by 60 percent which makes swimming more difficult (Smith 1976a; Crowl and Alexander 1989). Encumbered males also perform a series of brooding behaviors that could potentially raise their metabolic rates (Smith 1976a; Kraus et al. 1989). I found, however, there was no difference in the lifespan between brooders and non-brooders, but sample sizes were small (brooders n = 12, non-brooders n = 18).

17 The lifespan of male and female waterbugs that failed to breed, though paired with the opposite sex, was significantly shorter than those of both virgins and breeders. In my study, time spent with the opposite sex included being placed in a large aquarium where movement was unrestricted, as well as being exposed to the opposite sex. Work done by Ragland and Sohal (1973) with houseflies (Musca domestica) showed that individuals kept in small containers where flying is restricted lived significantly longer than flies kept in large cages where movement was unrestricted. When houseflies of the opposite sex are housed together a considerable amount of mating-related interactions occur, enough so that manipulations of the sex ratio in experimental cages affected lifespan (Ragland and Sohal 1973; Sohal 1986). Male waterbugs who failed to breed spent significantly more time with females than breeding males. Females, on the other hand, showed no difference in time spent with males. The explanation for the differences observed in female lifespan may lie in the protocol of the experiments. Females were placed in a scheduled rotation, spending 24 hours with males approximately every 3-4 days. once breeding occurred females were removed from this rotation for 14 days. It appears that females given this "rest period" live longer than those females who did not receive it. Similar to Ragland and Sohals' (1973) experiments with

18 houseflies, it is impossible to determine whether physical activities or mating-related activities are responsible for the observed declines in lifespans (Lints 1985). The fact the mating itself does not reduce lifespan in breeding bugs may imply that physical activity might be an important factor influencing aging. Another possible explanation for the decreased lifespan in individuals that did not breed, although given the opportunity, was that they were "less healthy" than other individuals and consequently did not breed and died sooner. I found that overall, female waterbugs live statistically longer than males. Although not statistically significant at any single level of mating effort, females consistently lived longer on average than did males. These results agree with other findings concerning sex differences in longevity. For example, in 13 species of Lepidoptera, Musca domestica and several other insects, males die sooner than females (MacArthur and Ballie 1932; Rockstein and Lieberman 1959). There are, however, several exceptions to this trend; Tribolium castaneum females lived longer than males in only 4 of 20 cases (Soliman and Lints 1982). Lints (1985) reported the results of a systematic examination of published data of longevity in Drosophila; males outlived females in over one half of the cases examined. There seems to be no real

19 explanation for the lifespan differences observed between the sexes, but chromosome number and structure as well as metabolic patterns have been offered as possible explanations (Rockstein and Miquel 1973; Lints 1985). Due to the contradictory nature of the information available, Lints suggested that more definitive studies are needed to truly answer the question of differences in lifespan between the sexes. Life history theory suggests that natural selection will push the age of first reproduction to the physiological minimum (Stearns 1976). Furthermore, any allocation of time or energy to reproduction is probably accompanied by a decrease in survivorship and future reproduction (Pianka and Parker 1975) . Organisms are thus faced with the task of striking a balance between the benefits of reproducing early and the cost to longevity and future reproductive potential (Pianka 1988). In rotifers, long lived individuals avoid high rates of reproduction early in life whereas short lived individuals reproduce early with high reproductive outputs (Snell and King 1977). Law (1979) found that annual meadow grass pays a price for early reproduction by sacrificing reproductive potential late in life. In a sib-analysis of adult life-history characters in Drosophila melanogaster, a negative relationship was found between early fecundity and lifespan (Rose and Charlesworth 1980). I found a significant positive

20 relationship between age at first reproduction and age at death in both male and female waterbugs. Those bugs that delayed reproduction, even though given the opportunity to breed, lived longer than those that bred early. In the terrestrial isopod, (Armadillidium vulgare), early breeders have a slower growth rate compared to individuals that breed later in life (Lawlor 1976). It would be interesting to monitor growth in waterbugs to see if a similar trend exists. In conclusion, there was no evidence to suggest that the amount of reproductive effort negatively affects lifespan in waterbugs; breeding waterbugs lived for approximately the same length of time as virgins. Age at first reproduction did affect future survivorship; individuals that bred early in life died sooner than individuals that first bred later in life. These experiments may be a valuable guide for future research. Larger initial sample sizes would be useful due to the fact that there was limited breeding, especially among the males, and several bugs that lived less than 100 days had to be excluded from the data analysis. Design of experiments should be such that the effects of physical activity can be separated from those of mating­ related activity. Changes in body characteristics such as weight or gonad size along with characteristics of egg production, such as egg weight, would be valuable in further investigating the costs of reproduction.

21 LITERATURE CITED

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22 Finch, c. 1991. Longevity, senescence and the genome. University of Chicago Press, Chicago. Fowler, K. and L. Partridge 1989. A cost of mating in female fruitflies. Nature 338:760-761. Gadgill, M. and W.H. Bossert 1970. Life historical consequences of natural selection. Amer. Nat. 104:1-24. Haukioja E. and T. Hakala 1978. Life-history evolution in Andonata piscinalis (Mollusca, Pelecypoda). Oecologia (Ber) 35:253-266. Hayashi, F. 1993. Male mating costs in two insect species (Protohermes, Megaloptera) that produce large spermatophores. Anim. Behav. 45:343-349. Kirkwood, T.B.L. 1985. Comparative and evolutionary aspects of longevity. In Handbook of the biology of aging. 2ed. Eds. C.E. Finch and E.L. Schneider Van Nostrand Reinhold Co., New York. pp 209-218. Kirkwood, T.B.L. 1987. Immortality of the germ-line versus disposability of the soma. In Evolution of longevity in . A comparative method. Eds. A.O. Woodhead and K.H. Thompson Plenum, New York. pp 27-44.

23 Kraus, W. F.; Gonzalese, M. J.; Vehrencamp, s. L. 1989. Egg development and an evaluation of some of the costs and benefits for paternal care in the Belostomatid, Abedus indentatus (Heteroptera: Belostomatidae). J. Kan. Entomol. Soc. 62 ( 4) : 548-562. Kruse, K.C. 1990. Male backspace availability in the giant water bug (Belostoma flumineum Say). Behav. Ecol. Sociobiol. 26:281-289. Kruse, K.C. and T.R. Leffler 1984. Females of the giant water bug Belostoma flumineum (Hemiptera: Belostomatidae), captured carrying eggs. Ann. Entomol. Soc. Amer. 77:20. Lamb, M.J. 1964. The effects of radiation on the longevity of females Drosophila subobscura. J. Insect. Physiol. 10:487-497. Law, R. 1979. The cost of reproduction in annual meadow grass. Amer. Nat. 113:3-16. Lawlor, L.R. 1976. Molting, growth and reproductive strategies in the terrestrial isopod, Armadillidium vulgare. Ecology 57:1179-1194. Lints, F.A. 1985. Insects. In Handbook of the biology of aging. Eds. C.E. Finch and E.L. Schneider. Van Nostrand Reinhold Co., New York. pp 146-172.

24 Maynard Smith, J. 1958. The effect of temperature and of egg laying on the longevity of Drosophila subobscura. J. Exp. Biol. 35:832-842. MacArthur, J.W. and W.H.T. Ballie 1932. Sex differences of mortality in Abraras-type species. Quart. Rev. Biol. 7:313-325. Medawar, P.B. 1955. The definition and measurement of senescence. Ciba Found. Colloq. on Aging 1:4-15. Menke, A.S. 1960. Family Belostomatidae. In The Semi­ Aguatic and Aquatic Hemiptera of California. Ed. A.S. Menke Bull. Calf. Insect Suv. 21. pp 76-86. Nur, N. 1984. The consequences of brood size for breeding blue tits I. Adult survival, weight change and the cost of reproduction. J. Anim. Ecol. 53:479-496. Partridge, L. and R. Andrews 1985. The effect of reproductive activity on the longevity of male Drosophila melanoqaster is not caused by an acceleration of aging. J. Insect. Physiol. 31(5):393-395. Partridge, L.; Green, A. and K. Fowler 1987. Effects of egg-production and exposure to males on female survival in Drosophila melanogaster. J. Insect Physiol. 33:745-748. Pianka, E.R. 1988. Evolutionary Ecology 4th Ed. Harper & Row, New York.

25 Pianka, E.R. and w.s. Parker 1975. Age-specific reproductive tactics. Amer. Nat. 109:453-464. Ragland, S.S. and R.S. Sohal 1973. Mating behavior, physical activity and aging in the housefly, Musca domestica. Exp. Gerontol. 8:135-145. Renzick, D. 1985. Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257-267. Reznick, D. 1992. Measuring the costs of reproduction. Trends Ecol. Evol. 42-45. Rockstein, M. and H.M. Lieberman 1959. A life table for the common housefly, (Musca domestica). Gerontologia 3:23. Rockstein, M. and J. Miquel 1973. Aging in insects. In The physiology of Insecta. 2nd ed. Ed. M. Rockstein Academic Press, New York. pp 23-44. Rose, M.R. 1984. The evolution of senescence. Can. J. Zool. 62:1661-1667. Rose, M.R. 1991. Evolutionary biology of aging. Oxford University Press: New York. Rose, M. and B. Charlesworth 1980. A test of evolutionary theories of senescence. Nature 287:141-142. Smith, R. 1976a. Brooding behavior of a male water bug Belostoma flumineum. J. Kan. Entomol. 49(3):333- 343.

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28 Table 1. Days and percent of life spent with the opposite sex

Davs with the OQQOsite sex % life with OQQOsite sex x SD Range x SD Range n ------Females Zero 17.4 6.0 9-27 9.6 1.9 5.7-12.1 8 All Breeders 22.3 9.3 5-39 9.4 3.2 3.1-15.8 31 Bred lx 19.3 11.9 5-39 8.8 4.1 3.1-15.8 15 Bred 2x 26.7 5.8 19-33 11. 4 1.8 8.0-13.1 6

N Bred >2x 24.1 9.3 5-39 9.4 1.9 7. 1-11. 9 10 ID

Males Zero 134.2 36.0 88-212 79.l 4.1 72.1-91.6 32 All Brooders 152.2 47.6 105-222 70.8 8.9 57.7-90.6 12 All Nonbrooders 146.9 47.9 87-241 68.5 7.9 49. 3-81. 3 18 Table 2A. Number of egg laid on plastic, males and totals. Eggs Eggs Eggs Veg Total ------Males x SD x SD x SD n ------Virgins 68.7 48.4 68.7 48.4 10 Zero 8.3 14.0 0.0 o.o 8.2 14.0 8 Bred lx 18.6 18.1 57.1 23.1 75.6 28.1 15 Bred 2x 36.3 50.8 105.7 35.7 142.0 71.4 6 Bred 3x 25.3 16.4 217.5 42.9 242.7 65.6 6 Bred >3x 29.5 16.5 289.5 77.6 327.7 65.6 10

Table 2B. Number of eggs brooded and days spent brooding. # of Eggs Days broods on back Brooding

x SD x SD n ------Brooders 1 41.3 20.7 8.1 5 10 2 129.5 7.8 22.0 9 2 Nonbrooders 1 51.4 30.9 9 2 141.5 30.5 6 >3 216.7 14.2 3 ------

30 Fig. 1 Mean (+/-2 S.E.) age at death for female and male waterbugs used in experiments. A. All females (X = 222.3, sd = 56.1, n = 49) and all males (X = 196.0, sd = 55.9, n = 81). B. Virgin females (X = 228.0, sd = 67.9, n = 10) and virgin males (X = 216.5, sd = 64.0, n = 19). c. Females that were paired with males but failed to breed (X = 178.1, sd = 32.8, n = 8) and males that were paired with females but failed to breed (X = 168.8, sd = 40.7, n = 32). D. Females that bred {X = 231.8, sd = 52.8, n = 31); males that brooded their eggs {X = 213.0, sd = 49.6, n = 12); and males that had their egg pads removed {X = 211.6, sd = 58.7, n = 18).

31 300 300 ,- All A Virgins B

250 250 ~

200 200 ._

150 150 '"" n=lO n=19 n=49 n=81 ...c:: .j...I 1 00 1 0 0 '---_..._--'---...___..___ ro Females Males Females Males Cl) Q .j...I ro Cl) b.O 300 300 < Breeders D ~ Nonbreeders c ~ 250 250 ~ 200 200

150 150 n=31 n=12 n-18 n=8 n=3 100 .______.. ______1 0 0 '----'-----'---'--_.__.....___.____ Females Males Males Females Males Brooding Nonbrooding

Gender Fig. 2 Mean (+/-2 S.E.) age at death for female or male waterbugs. A. Virgin females (X = 228.0, sd = 42.9, n = 10), females that were paired with males but failed to breed (X = 178.1, sd = 23.2, n = 8) and females that did breed (X = 231.8, sd = 18.9, n = 31). B. Females that bred once (X = 209.8, sd = 52.7, n = 15), twice (X = 236.0, sd = 49.6, n = 6), or more than two times (X = 262.4, sd = 41.8, n = 10). c. Virgin males (X = 216.5, sd = 53.9, n = 19), males that were paired with females but failed to breed (Zero) (X = 168.8, sd = 40.7, n= 32), males that brooded their eggs (X = 213.0, sd = 49.6, n = 12) and males whose egg pads were removed (X = 211.6, sd = 58.7, n = 18). D. Non-brooding males that bred once (X = 198.8, sd = 54.7, n = 9), or more than one time (X = 224.3, sd = 63.0, n = 9).

32 300 Females A 300 Females B 250 250

200 200

150 150 =1 n=6 =1 =1 n= n=3 1 0 0 ._____...._____..__._...__._____._ 1 0 0 ,_____.____.__._____.__.____.__ Virgins Zero Breeders lx 2x >2x

D Males c 300 -Nonbrooding Males 250 ,_

200 200 - T 1

150 150 - n=9 n=9

100 100 '-----'-~-'--'-~_.._- Virgins Zero Brooders Non lx >lx Brooders

Breeding History Fig. 3 The relationship between age at first reproduction and age at death for all male and females waterbugs that bred (r = 0.5311, P < 0.0001, n = 61); open circles = females, closed circles = males.

33 Age at First Reproduction (days) Fig. 4 The relationship between age at first reproduction and age at death in female waterbugs. A. All females (r = 0.4104, P = 0.0105 n = 31). B. Females that bred once (r = 0.6276, P = 0.0053, n = 15). c. Females that bred twice (r = 0.8407, P = 0.0170, n = 6). D. Females that bred three or more times (r = 0.3688, P = 0.1529, n = 10).

34 300 A 300 0 B ~ o 'eo 0 '«:8 08 250 0 Oo 250 0 0

~ 0 0 200 80 200 0 00 °o 150 00o 0 150 0 0 ~ 0 0 0 0 ~ 100 100 ro 0 100 200 300 0 100 200 300 '"CS...._,,,, ...c:: .j...Jro Q) Q .j...J ro 300 300 0 c D Q) ~ 0 00 Oo 0 b.O 250 0 250 ~ 0 200 0 200

150 0 150 0

100 100 0 100 200 300 0 100 200 300

Age at First Reproduction (days) Fig. 5 The relationship between age at first reproduction and age at death in male waterbugs that brooded eggs to hatching (r = 0.9649, P < 0.0001, n =12).

35 300 A 300 B 00 0 0 0 250 0 250 0 0 0 00 0 200 0 200 r-... 0 0 a 0 0 0 ~ 150 0 150 "d 00 0 0 0 ~ 100 100 ...c:1-' 0 100 200 300 0 100 200 300 C'd (1.) Q 1-' C'd (1.) b.O 300 c 0 <: 0 0 250

0 200 0 0

150 0 0 100 0 100 200 300

Age at First Reproduction (days) Fig. 6 The relationship between age at first reproduction and age at death in male waterbugs that had egg pads removed. A. All males (r = 0.7128, P = 0.0003, n = 18). B. Males that bred once (r = 0.8211, P = 0.0022, n = 9). c. Males that bred two or more times (r = 0.7717, P = 0.0060, n = 9).

36 .300

0

0 0 ~

0

1 00 .._____.._____.______._ ____. _ __.._ ___. 0 50 1 00 150 200 250 .300

Age at First Reproduction (days)