Ethology

Brood Pumping Modulation and the Benets of Paternal Care in Abedus breviceps (Hemiptera: Belostomatidae)
n ez* a-Steyer*, Mario E. Favila & Rogelio Mac as-Ordo Roberto Mungu
a, A.C., Departamento de Biolog a Evolutiva, Km. 2.5 Carretera Antigua a Coatepec # 351., Xalapa, Veracruz, Mexico * Instituto de Ecolog a, A.C., Departamento de Biodiversidad y Ecolog a Animal, Km. 2.5 Carretera Antigua a Coatepec # 351., Xalapa, Veracruz, Instituto de Ecolog Mexico

Correspondence a-Steyer, Instituto de Ecolog a, A.C., R. Mungu a Evolutiva, Km. 2.5 Departamento de Biolog Carretera Antigua a Coatepec # 351., 91070 Xalapa, Veracruz, Mexico. E-mail: robermunguia@gmail.com

Abstract Males of the subfamily Belostomatinae, within the giant waterbugs (Hemiptera: Belostomatidae), brood eggs on their backs from oviposition until egg-hatching. The eggs in the clutch must be kept moistened and exposed to enough oxygen ow for them to develop properly and maximize hatching success. When submerged, males regularly perform different behavioral patterns that promote oxygen ow to the eggs. One of these patterns, brood pumping, consists of push-up like movements using their hind legs. In this study, we assessed if temperature, oxygen dissolved in the water and the developmental stage of the clutch inuence brood pumping rate in Abedus breviceps. In the wild, we found that males covered with bigger eggs showed a higher brood pumping rate than that of males with smaller eggs. An analysis of egg growth curves under laboratory conditions demonstrated that males that did not perform brood pumping were carrying broods that were in the rst third of their developmental period. We also found that non-brooded clutches had a much lower hatching success than those brooded by males, even when exposed to controlled and favorable environmental conditions. We discuss the persistence and modulation of paternal care intensity in belostomatines as an aptative character conditioned by environmental and anatomical features.

Received: September 5, 2007 Initial acceptance: November 28, 2007 Final acceptance: March 5, 2008 (S. K. Sakaluk)
doi: 10.1111/j.1439-0310.2008.01507.x

Introduction Parental care has been dened as any behavior performed by one or both parents that increases offspring survival (Clutton-Brock 1991). Parental care in belostomatid giant waterbugs (Hemiptera: Belostomatidae) is performed only by the male (Smith 1997), and is thus exclusive paternal care. In the subfamily Belostomatinae, females oviposit up to one-hundred eggs on the dorsal surface of the male. The eggs remain glued on the male throughout development by means of a mucous substance secreted by the females (Smith 1976a, 1997; Venkatesan 1983).
Ethology 114 (2008) 693700 2008 The Authors Journal compilation 2008 Blackwell Verlag, Berlin

Parental males maintain oxygen and humidity conditions of the clutch that allow proper egg development and hatching (Smith 1976a,b, 1997). They may either remain in the airwater interface, where they are more exposed to predation (Smith 1997), or perform different underwater movements that promote oxygen ow. Such behaviors are energetically costly due to muscular activity (Smith 1976b, 1997). Two subaquatic parental behaviors have been described in belostomatine males: (1) egg stroking: males alternately use their hind legs to brush the clutch, thus generating water ow over the eggs (Smith 1976a,b, 1997) and (2) brood pumping: males perform a series of push-up movements
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using their hind legs, while holding on with their front legs, also promoting water ow and oxygen diffusion through the egg membrane (Smith 1976a, 1997; Venkatesan 1983). Given that brood pumping implies energetic costs derived from muscular activity (Smith 1976b), we suggest that this behavior may be modulated by the parental male, and may be a plastic behavioral trait (Schlichting & Pigliucci 1998). Brood pumping rate may be the target of optimizing selection in terms of its (energetic) cost benet (offspring survival) relationship (Parker & Maynard Smith 1990). Environmental factors such as oxygen concentration and water temperature may inuence brood pumping rates in the giant waterbug Abedus breviceps. For example, when oxygen concentrations are high, active oxygen diffusion may be less relevant for egg viability and development, as in the common goby sh Pomatoschistus microps (Jones & Reynolds 1999a; Green & McCormick 2004). Likewise, insect metabolic rates increase at higher temperatures thus augmenting the embryos oxygen demands. An increase in water ow promoting behaviors in response to an increase in temperature has been found in sh (Green & McCormick 2004) and crustaceans (Dick et al. 1998). Males may also modulate brood pumping rates depending on the developmental stage of the egg. Egg size increases with development, thus reducing the ratio of oxygen diffusion area to volume while the metabolic rate increases (Smith 1997). The rate of behaviors that promote active oxygen diffusion is expected to increase as the oxygen demand per volume unit also increases as has been reported ndez 2002) and sh in crustaceans (Baeza & Ferna (Green & McCormick 2004). Thus, bigger eggs could receive a higher brood pumping rate. Egg-laden males are capable of dislodging (aborting) the clutch (Smith 1976b, 1980; Kight & Kruse 1992; Kight et al. 2000; Roberto Mungu a-Steyer, pers. obs.) either actively (using their legs) or passively (staying out of the water until the mucous substance dries out). Based on laboratory studies, it has been suggested that males may abort clutches as a strategy that increases male lifetime reproductive success when the present clutch is small and or less developed (Kight & Kruse 1992; Kight et al. 2000). However, this interpretation should be considered with caution as laboratory conditions may promote male abortions due to stress and overcrowding (Smith 1976b, 1980; Roberto Mungu a-Steyer, pers. obs.). It has been demonstrated that parental males are less mobile (Smith 1976a; Kight et al. 1995) and forage less efciently (Crowl & Alexander 1989), but
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do not experience higher mortality (Mungu a-Steyer n & Mac as-Ordo ez 2007) relative to non-parental males. As males have costs derived from paternal care and are capable of aborting, it is important to assess the actual benets of paternal care in terms of egg survival to understand the stability of this behavior. In this study, we explored the variation in brood pumping, an energetically costly behavioral character, associated with environmental and developmental conditions as well as the benets of paternal care in terms of egg viability. Methods
Brood Pumping

Brood pumping rate was assessed in a eld population in Texala creek in the state of Tlaxcala, Mexico (N 192121, W 982232, 2295 m asl; see Munn gu a-Steyer & Mac as-Ordo ez 2007), in six eld surveys conducted between May 1st and 17th, 2005. Focal observations of brooding males were carried out between 10:00 and 15:00 hours, and the number of push-ups performed by each male was recorded during a 3-min period. If a male ceased brood pumping (no push-ups for more than a minute) before the 3-min period completion, the observation was discarded and the procedure repeated when he began to brood pump again. Males were assigned a brood pumping score of 0 if they did not perform the behavior after 50 min of focal observation. Once the observation was completed, the male was captured and two eggs from the edge of the clutch were removed using a dissection needle. Egg length was measured using a digital caliper (0.02 mm; DSE, Inc, Australia) and averaged for the two eggs. The clutch was classied as full or partial depending on whether it covered the entire male dorsum. Water temperature and dissolved oxygen in the water were recorded immediately after each observation using an oxymeter (Model YSI 55; Yellow Spring Instruments, Inc., Yellow Springs, OH, USA). Coefcients of variation were estimated for both these variables and egg size. These three variables and their interactions were used as independent variables in a multiple regression, using brood pumping rate as the dependent variable (push-ups per minute). Model selection was performed using the Akaike information criterion corrected for small samples (AICc) (Burnham & Anderson 2002). The best supported model had the lowest AIC and its relative support (weight) with respect to other
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models was estimated (Burnham & Anderson 2002; Johnson & Omland 2004).
Egg Growth Curves

Effect of Paternal Care on Egg Viability

The relationship between egg developmental stage and egg length was assessed through modeling of growth curves obtained from ve males. Males mated and received eggs from females in aquaria maintained in the laboratory, allowing us to know the date of oviposition. Males were kept in an environmentally controlled room at 21 1C, 60 10% RH and 10L:14D photoperiod. Each egg-laden male was placed in a 3.92-l aquarium (23.5 cm length, 11.5 cm width, 14.5 cm height). The mean temperature of the water was 21.2C, SD = 0.7 (monitored with a submersible data logger Stowaway Tidbit TB132; Onset Computers. Corp., Bourne, MA, USA). The water was changed twice every week using inverse-osmosis treated water, and bubbled 10 min per day. Twice a week, males were fed laboratory-reared crickets. For each male, time in days between oviposition and hatching was recorded. Hatching time was recorded as the day when the rst egg of the pad hatched. Growth curves were estimated measuring egg length from serial samples of eggs from the same clutch over time. One egg was removed from each male every 2 d using a dissecting needle until the rst egg in the clutch hatched. Egg length was obtained from a digital photograph taken with a camera (Coolpix E4500; Nikon Corp. 4 megapixels, Japan) mounted on a dissecting microscope (SM2800; Nikon Corp., Japan), and measured using ImageJ v1.36 software (Abramoff et al. 2004). Given that initial egg length, environmental conditions (e.g. paternal effects) and growth rate from eggs belonging to the same clutch are not independent, non-linear mixed models were constructed to obtain the growth curves (Pinheiro & Bates 2000). These models allowed an assessment of curve variation between-individuals and population parameter estimation. A four parameter mixed logistic model was used to t the data (Pinheiro & Bates 2000). The equation of this logistic curve was A + (B ) A) (1 + exp((xmid ) x) scal)). The rst two parameters represent the asymptotes of those values related to egg length at the time of oviposition (A) and near hatching (B); the third parameter (xmid) represents the inection point, and the fourth (scal) is a scaling parameter. The use of this model was much better supported (AIC = )51.752) than a linear (AIC = 2.132) or quadratic (AIC = )12.118) model; the three parameter model using a logistic curve did not reach convergence.
Ethology 114 (2008) 693700 2008 The Authors Journal compilation 2008 Blackwell Verlag, Berlin

We randomly assigned 30 males collected in our eld site to two treatments: with parental care (PC, n = 15) and without parental care (WOPC, n = 15). For WOPC, we carefully removed each egg-pad from the males back and placed it on a 2-cm high polystyrene foam piece submerged in a sufcient volume of water, so that the base of the eggs were in contact with the water, but not their tip, resembling the behavior frequently performed by belostomatine males in which they oat and keep the egg-pad as described (Smith 1997). Each WOPC egg-pad was placed in polystyrene foam container (base diameter 12 cm, height 24.5 cm). Preliminary data (not shown) showed that all eggs failed to develop when they were not in contact with water (n = 5), or when they were totally submerged (20-cm deep, n = 5). Encumbered males of the PC treatment were held in the same type of containers, with a water depth of 12 cm. Water used in both treatments was puried using inverse osmosis, and changed every 2 d. Environmental conditions and the feeding regime were the same as described above. Egg survival was analyzed using a generalized mixed linear model with a binomial distribution, because each egg was aggregated in a clutch, thus the fate of each egg was not independent (Pinheiro & Bates 2000). A log-likelihood ratio test was used to assess the effect of paternal care between the model that included this factor, and the one that did not. The number of eggs per clutch in each treatment was compared using a Wilcoxon rank test to account for potential effects of brood size on egg viability. Statistical tests and graphics were carried out using R 2.3 statistical software (R Development Core Team 2006). Results
Brood Pumping

Brood pumping rate in the eld was in the range of 024 push-ups per minute, with a median of 11.3. The ranges for the independent variables were: temperature = 17.222.6C, dissolved oxygen = 4.46.0 mg l and egg length = 2.154.45 mm (Fig. 1). The respective coefcients of variation were: temperature = 8.61%, dissolved oxygen = 9.33% and egg length = 19.83%. Out of the 40 observed males, nine did not show brood pumping, out of which four (44%) carried partial
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Fig. 1: Variation in distribution of dissolved oxygen, temperature and length of eggs brooded by Abedus breviceps males in the Texala creek, Tlaxcala, Mexico, during ve eld surveys between May 1st and 17th, 2005. Boxplots represent the median (horizontal line), quartiles (boxes) and extreme values (whiskers).

clutches (i.e. they were not completely covered by eggs). The percentage of partial clutches among brood pumping males was 29% (nine males). The best supported model maintained only egg length as an explanatory variable of brood pumping rate (Table 1). The regression equation was y = )19.12 + 87.29x (r2 = 0.698, F1,38 = 87.78, p < 0.001, Fig. 2). Non-brood pumping males carried eggs between 2.15 and 2.85 mm in length, whereas brood pumping males carried eggs between 2.60 and 4.45 mm in length.
Table 1: Model selection explaining brood pumping rate in Abedus breviceps
Models L L+O L+O L+O L+O L+O L+O Null AICc 226.22 228.23 230.14 232.80 234.58 236.93 240.07 271.75 DAICc 0.00 2.01 3.92 6.58 8.36 10.71 13.85 45.54 Weight 0.64 0.23 0.09 0.02 0.01 <0.01 <0.01 <0.01

Egg Growth Curves

The growth curve of the mixed model showed that the highest between-male variation was found around the inection point, that is, the time period between oviposition and the highest growth rate (Table 2). The other parameters were similar among males as shown by the random effect row of Table 2. The logistic model equation was 2.53 + 2.134 (1 + exp((11.651 ) x) 2.967)) (Fig. 3). The logistic curve of the mixed model was used to estimate the development stage of the eggs brooded by those males that did not perform brood pumping, using size as an explanatory variable. The largest eggs of these males would be on the seventh day of the 21 d in the brooding period (Fig. 2). This estimation suggests that non-brood pumping males were carrying eggs in the rst third of the developmental period.
Effect of Paternal Care on Egg Viability

+ + + + +

T T T T T

+ + + +

L:O L:O + L:T L:O + L:T + O:T L:O + L:T + O:T + L:O:T

L, egg length; O, dissolved oxygen; T, water temperature.

Eggs in the WOPC treatment had lower viability than eggs of the PC treatment (Fig. 4). PC eggs had between 65% and 100% hatching success with a median of 93%, while WOPC eggs had between 0%
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Fig. 2: Relationship between brood pumping rate of Abedus breviceps males and egg length of brooded eggs.

Fig. 3: Egg growth curves of egg-pads brooded by Abedus breviceps males. Broken lines represent the t of the logistic curve per individual and the continuous line represents the t for the population.

Table 2: Egg growth rate parameters for clutches brooded by ve Abedus breviceps males, obtained using a non-linear mixed model t with a four parameter logistic curve
Random effects Parameters A B xmid scal Residual SD 0.052 0.098 1.141 0.178 0.009 Coefcients 2.530 4.664 11.651 2.967 Fixed effects SE 0.039 0.099 0.620 0.273 t 65.018 47.136 18.795 10.872 p-value <0.001 <0.001 <0.001 <0.001

and 81% hatching success with a median of 46%. The log-likelihood ratio test between the null model and the one including the effect of male-back brooding showed a signicant effect (v2 = 82.22, df = 1, p < 0.001), thus strongly suggesting the relevance of paternal care on egg viability. The variation (SD) associated with random effects (different clutches) was 1.59. The differences in viability were not related to the number of eggs maintained on the egg pad (W = 107, p = 0.947). Discussion There are several reported cases in which parents modulate the intensity of parental care in terms of behaviors that promote oxygen ow to their progeny (Jones & Reynolds 1999a; Neff & Gross 2001). Females of the crustacean Crangonyx pseudogracilis increase fanning as temperature rises or dissolved
Ethology 114 (2008) 693700 2008 The Authors Journal compilation 2008 Blackwell Verlag, Berlin

Fig. 4: Boxplot comparing egg viability between parental care (PC) and no parental care (WOPC) treatments in Abedus breviceps. Median (horizontal line), quartiles (boxes) and extreme values (whiskers) are represented.

oxygen diminishes (Dick et al. 1998). A proportional increase in fanning related to embryo developmental stage has been described in the damselsh Amphiprion melanopus (Green & McCormick 2004) and in the crab ndez 2002). At low disCancer setosus (Baeza & Ferna solved oxygen concentrations, males of the gobid sh P. microps fanned for longer and at a higher rate,
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and lost more weight, than those at higher concentrations (Jones & Reynolds 1999a). In our study, parental behavior was not related to environmental variables but rather to egg developmental stage. This may be due to the fact that, unlike previously studied species, dissolved oxygen is not obtained underwater by means of gills in belostomatids, but rather as an air bubble at the airwater interface. When waterbugs submerge, this bubble is maintained by retractable airstraps (Eriksen et al. 1996; Smith 1997). The lack of tracheal gills in belostomatids may also imply that males may be unable to assess subtle changes in dissolved oxygen of around 1.5 mg l (as found in this study) and thus may be unable to modulate parental effort accordingly. There was less variability in dissolved oxygen and temperature than in egg developmental stages. The increase in egg size in belostomatids is caused by water intake by the embryo through the hydropyle (Madhavan 1974; Venkatesan & Rao 1980), thus increasing mass as well. Males might assess the size of the egg clutch using their posterior legs, or the weight of the clutch when they leave the water. Non-brood pumping males were found to carry eggs in the rst third of the developmental stage, according to predictions of the logistic mixed model. At this stage, males may be able to avoid any cost of brood pumping because less-developed eggs are smaller and have a higher surface volume ratio, which is probably sufcient for passive oxygen intake and embryo development (Hinton 1969; Gillooly & Dodson 2000). Larger eggs in subaquatic conditions and the difference in oxygen concentration in water (012 ppm) as compared to air (200 000 ppm) may promote the appearance of phenotypic characters that facilitate oxygenation of the eggs such as plastron horns (a supercial chorionic egg layer associated with oxygen exchange) in the Nepidae or aerating behaviors in Belotostomatidae (Eriksen et al. 1996; Smith 1997). It has been suggested that brood pumping performed by belostomatine males is important for egg development because eggs are frequently underwater and the plastron covers a reduced amount of the egg surface (Perez-Goodwyn et al. 2006). In contrast, Lethocerinae eggs are covered to a larger extent by plastron and have a greater oxygen supply available as they are oviposited on emergent vegetation (Smith 1997; Perez-Goodwyn et al. 2006). Thus, brood pumping rates in Belostomatinae could change not only within but also across species, depending on oxygen concentration in the water and their specic egg plastron surface area.
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Aside from increasing egg viability, paternal care could be used to attract females (Jones & Reynolds 1999b; Pampoulie et al. 2004). Push-up frequency may be an honest signal to females reecting male parental quality (Tallamy 2000). However, the fact that brood pumping is reduced or absent during the rst stages of egg development of partial clutches does not support this hypothesis. The logistic model showed an egg growth curve similar to that of Abedus indentatus (Kraus et al. 1989). In our study, the mixed model showed that the parameter associated with maximum growth rate presented the highest variation among males. This is important as variation in this parameter is likely to be related to the modulation in brood pumping rate, and males whose broods increase growth rate later may be paying lower energetic costs. This may be especially critical if food is scarce or temperatures are high (which would imply a shorter egg developmental time), because they may save resources in those few cases in which a second clutch is brooded (Mungu a-Steyer & Mac as-Ordn o ez 2007). Alternatively, males may be able to accelerate or delay the increase in egg growth rate by increasing or reducing brood pumping rate, and adjust to the above-mentioned environmental and ecological conditions. Egg survival to hatching was higher in the PC than in the WOPC treatment, even though the later included a combination of moisture and atmospheric oxygen. This result suggests much lower egg viability in the absence of paternal care in natural conditions, and highlights the importance of the constant change of micro-environmental conditions that results from brooding by a moving male. Males in the studied population change depth and even completely leave the water occasionally (Roberto Mungu a-Steyer, pers. obs.). Despite being able to dislodge their egg-pad, it seems unlikely that this may increase egg viability as eggs quickly dry out away from water, and may be infected by fungus when submerged (Kraus et al. 1989; Smith 1997). A previous study of an unidentied belostomatine in the genus Diplonychus showed that eggs in atmospheric conditions loose up to 50% of their mass in 24 h due to water loss (Venkatesan & Rao 1980). Similar differences in egg survival to those found between our treatments have been described in other belostomatines such as Diplonychus indicus (Venkatesan 1983), Abedus herberti (Smith 1976a), Belostoma umineum (Smith 1976b) and Belostoma malkini (Cullen 1969). However, Kraus et al. (1989), working with A. indentatus, found high egg viability
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for clutches with no parental care placed at the air water interface. In summary, we demonstrated that brood pumping is a plastic behavioral trait inuenced by development stage of the eggs carried by the males. In this way, we suggest paternal care is an aptative character that increases egg viability due the interplay of environmental conditions such as dissolved oxygen in the water and constraints such as egg size and chorionic structure of the eggs (Smith 1997; Merila & Bjo rklund 2004). Acknowledgements We want to express our gratitude to R. Guevara who provided the microscope employed to perform zquez who lent us the egg measurements, and G. Va eld oxymeter. This manuscript was improved by rez-Staples, G. Machado, A. Co rthe review of D. Pe doba-Aguilar, J. Rull, S. K. Sakaluk and two anonymous reviewers. Literature Cited
Abramoff, M. D., Magelhaes, P. J. & Ram, S. J. 2004: Image processing with ImageJ. Biophotonics Intl. 11, 3642. ndez, M. 2002: Active brood care in Baeza, J. A. & Ferna Cancer setosus (Crustacea: Decapoda): the relationship between female behaviour, embryo oxygen consumption and the cost of brooding. Funct. Ecol. 36, 241251. Burnham, K. P. & Anderson, D. R. 2002: Model Selection and Multimodel Inference. Springer-Verlag, New York. Clutton-Brock, T. H. 1991: The Evolution of Parental Care. Princeton Univ. Press, Princeton, NJ. Crowl, T. A. & Alexander, J. E. 1989: Parental care and foraging ability in male waterbugs (Belostoma umineum). Can. J. Zool. 67, 513515. Cullen, M. J. 1969: The biology of giant water bugs (Hemiptera: Belostomatidae) in Trinidad. Proc. R. Entomol. Soc. Lond. 44, 123137. Dick, J. T. A., Faloon, S. E. & Elwood, R. W. 1998: Active brood care in an amphipod: inuences of embryonic development, temperature and oxygen. Anim. Behav. 56, 663672. Eriksen, C. H., Lamberti, G. A. & Resh, V. H. 1996: Aquatic insect respiration. In: An Introduction to the Aquatic Insects of North America (Merritt, R. W. & Cummins, K. W., eds). Kendall Hunt Publishing, Duboque, IA, pp. 2940. Gillooly, J. F. & Dodson, S. I. 2000: The relationship of egg size and incubation temperature to embryonic
Ethology 114 (2008) 693700 2008 The Authors Journal compilation 2008 Blackwell Verlag, Berlin

development time in univoltine and multivoltine aquatic insects. Freshw. Biol. 44, 595604. Green, B. S. & McCormick, M. I. 2004: O2 replenishment to sh nests: males adjust brood care to ambient conditions and brood development. Behav. Ecol. 16, 389397. Hinton, H. E. 1969: Respiratory systems of insect egg shells. Annu. Rev. Entomol. 14, 343368. Johnson, J. B. & Omland, K. S. 2004: Model selection in ecology and evolution. Trends Ecol. Evol. 19, 101108. Jones, J. C. & Reynolds, J. D. 1999a: Costs of egg ventilation for male common gobies breeding in conditions of low dissolved oxygen. Anim. Behav. 57, 181188. Jones, J. C. & Reynolds, J. D. 1999b: The inuence of oxygen stress on female choice for male nest structure in the common goby. Anim. Behav. 57, 189196. Kight, S. L. & Kruse, K. 1992: Factors affecting the allocation of paternal care in waterbugs (Belostoma umineum Say). Behav. Ecol. Sociobiol. 30, 409414. Kight, S. L., Sprague, J., Kruse, K. & Johnson, L. 1995: Are egg-bearing male water bugs, Belostoma umineum Say (Hemiptera: Belostomatidae), impaired swimmers? J. Kans. Entomol. Soc. 68, 468470. Kight, S. L., Batino, M. & Zhang, Z. 2000: Temperaturedependent parental investment in the giant waterbug Belostoma umineum (Heteroptera: Belostomatidae). Ann. Entomol. Soc. Am. 93, 340342. Kraus, W. F., Gonzalez, M. J. & Vehrencamp, S. L. 1989: Egg development and an evaluation of some of the costs and benets for paternal care in the belostomatid, Abedus indentatus (Heteroptera: Belostomatidae). J. Kans. Entomol. Soc. 62, 548562. Madhavan, M. M. 1974: Structure and function of the hydropyle of the egg of the bug, Sphaerodema molestum. J. Insect Physiol. 20, 13411349. Merila , J. & Bjo rklund, M. 2004: Phenotypic integration as a constraint and adaptation. In: Phenotypic Integration: Studying the Ecology and Evolution of Complex Phenotypes (Piggliucci, M. & Preston, K., eds). Oxford Univ. Press, Oxford, pp. 107129. n Mungu a-Steyer, R. & Mac as-Ordo ez, R. 2007: Is it risky to be a father? Survival assessment depending on sex and parental status in the waterbug Abedus breviceps using multistate modelling. Can. J. Zool. 85, 4955. Neff, B. D. & Gross, M. R. 2001: Dynamic adjustment of parental care in response to perceived paternity. Proc. R. Soc. Lond. B. 268, 15591565. Pampoulie, C., Lindstro m, K. & St. Mary, C. M. 2004: Have your cake and eat it too: male sand gobies show more parental care in the preference of female partners. Behav. Ecol. 15, 199204. Parker, G. A. & Maynard Smith, J. 1990: Optimality theory in evolutionary biology. Nature 348, 2733.

699

Brood Pumping Modulation and Paternal Care Benets in A. breviceps

a-Steyer et al. R. Mungu

Perez-Goodwyn, P. J., Ohba, S. & Schnack, J. A. 2006: Chorion morphology of the eggs of Lethocerus delpontei, Kirkaldya deyrolli, and Horvathinia pelocoroides (Heteroptera: Belostomatidae). Russ. Entomol. J. 15, 151156. Pinheiro, J. C. & Bates, D. M. 2000: Mixed-Effect Models in S and S-Plus. Springer-Verlag, New York. R Development Core Team. 2006: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Viena, Austria. Schlichting, C. D. & Pigliucci, M. 1998: Phenotypic Evolution: A Reaction Norm Perspective. Sinauer Associates, Sunderland, MA. Smith, R. L. 1976a: Male brooding behavior of the water bug Abedus herberti (Heteroptera: Belostomatidae). Ann. Entomol. Soc. Am. 69, 740747. Smith, R. L. 1976b: Brooding behavior of a male water bug Belostoma umineum (Hemiptera: Belostomatidae). J. Kans. Entomol. Soc. 49, 333343.

Smith, R. L. 1980: Evolution of exclusive postcopulatory paternal care in the insects. Fla. Entomol. 63, 6578. Smith, R. L. 1997: Evolution of paternal care in the giant water bugs (Heteroptera: Belostomatidae). In: The Evolution of Social Behavior in Insects and Arachnids (Crespi, B. J. & Choe, J. C., eds). Cambridge Univ. Press, Cambridge, pp. 116149. Tallamy, D. W. 2000: Sexual selection and the evolution of exclusive paternal care in arthropods. Anim. Behav. 60, 559567. Venkatesan, P. 1983: Male brooding behaviour of Diplonychus indicus Venk. & Rao (Hemiptera: Belostomatidae). J. Kans. Entomol. Soc. 56, 8087. Venkatesan, P. & Rao, T. K. R. 1980: Water loss by eggs of Diplonychus sp. J. Kans. Entomol. Soc. 53, 587594.

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