Gary R. Hepp

Ecological, evolutionary, and conservation implications of incubation temperature-dependent phenotypes in birds.

Incubation is a vital component of reproduction and parental care in birds. Maintaining temperatures within a narrow range is necessary for embryonic development and hatching of young, and exposure to both high and low temperatures can be lethal to embryos. Although it is widely recognized that temperature is important for hatching success, little is known about how variation in incubation temperature influences the post‐hatching phenotypes of avian offspring. However, among reptiles it is well known that incubation temperature affects many phenotypic traits of offspring with implications for their future survival and reproduction. Although most birds, unlike reptiles, physically incubate their eggs, and thus behaviourally control nest temperatures, variation in temperature that influences embryonic development still occurs among nests within a population. Recent research in birds has primarily been limited to populations of megapodes and waterfowl; in each group, incubation temperature has substantial effects on hatchling phenotypic traits important for future development, survival, and reproduction. Such observations suggest that incubation temperature (and incubation behaviours of parents) is an important but underappreciated parental effect in birds and may represent a selective force instrumental in shaping avian reproductive ecology and life‐history traits. However, much more research is needed to understand how pervasive phenotypic effects of incubation temperature are among birds, the sources of variation in incubation temperature, and how effects on phenotype arise. Such insights will not only provide foundational information regarding avian evolution and ecology, but also contribute to avian conservation.

Slight differences in incubation temperature affect early growth and stress endocrinology of wood duck (Aix sponsa) ducklings

SUMMARY Early developmental experiences, such as incubation conditions, can have important consequences for post-hatching fitness in birds. Although the effects of incubation temperature on phenotype of avian hatchlings are poorly understood, recent research suggests that subtle changes in incubation conditions can influence hatchling characteristics, including body size and condition. We designed an experiment to explore the effects of incubation temperature on hatching success, survival to 9 days post hatch, growth and the hypothalamo–pituitary–adrenal (HPA) axis in wood ducks (Aix sponsa). Wood duck eggs were collected from nest boxes and experimentally incubated at three temperatures (35.0, 35.9 and 37.0°C), each falling within the range of temperatures of naturally incubated wood duck nests. Survival and growth were monitored in ducklings fed ad libitum for 9 days post hatch. In addition, baseline and stress-induced plasma corticosterone concentrations were measured in 2 and 9 day old ducklings. Hatching success and survival to 9 days was greatest in ducks incubated at the intermediate temperature. Ducklings incubated at 35.9°C and 37.0°C had 43% higher growth rates than ducklings incubated at 35.0°C. In addition, ducklings incubated at 35.0°C had higher baseline (17–50%) and stress-induced (32–84%) corticosterone concentrations than ducklings incubated at 35.9°C and 37.0°C at 2 and 9 days post hatch. We also found a significant negative correlation between body size and plasma corticosterone concentrations (baseline and stress-induced) in 9 day old ducklings. To our knowledge, this is the first study to demonstrate that thermal conditions experienced during embryonic development can influence the HPA axis of young birds. Our results illustrate that subtle changes (<1.0°C) in the incubation environment can have important consequences for physiological traits important to fitness.

Incubation as a Reproductive Cost in Female Wood Ducks

-We investigated the effects of body mass of incubating female Wood Ducks (Aix sponsa) on aspects of their current and future reproduction, and we examined factors that affect length of the incubation period. During three breeding seasons, body mass of female Wood Ducks averaged 578.0 g early and 553.3 g late in the incubation period. Body mass at the start of incubation was not related to either hatching success or length of the incubation period. In one of three years, females that were heavy at the end of incubation survived better to the next breeding season than those that were light. Reduced survival of light females in one year coincided with a greater loss of body mass in that year relative to other years, which indicates that incubation can be an important reproductive cost to female Wood Ducks. There were no relationships between body mass at the end of incubation and date of nesting or clutch size in the next breeding season. Partial correlations between clutch mass and length of incubation that controlled for date of nesting indicated a positive association between clutch mass and incubation length in every year. This relationship was evident only for parasitic nests (i.e. nests in which more than one female was laying eggs). Increased length of the incubation period associated with larger clutch mass represents a potential cost of intraspecific nest parasitism not previously recognized. Received 26 December 1989, accepted 17 June 1990. INCUBATING birds must provide the proper thermal environment for embryonic development. Simultaneously they must maintain their body condition so that survival and subsequent reproduction are not affected adversely. Time for feeding is restricted during incubation, which often makes it difficult for incubating individuals to meet daily metabolic costs (see Drent et al. 1985). Some avian species have adjusted to the demands of incubation by having biparental incubation (Eisner 1960, Feare 1984). In other species, males provide incubating females with food (Lyon and Montgomerie 1985, Nilsson and Smith 1988). In waterfowl (Anatidae), females of large-bodied species generally begin incubation with large energy reserves and are more attentive during incubation than females of small-bodied species, because largebodied females spend less time feeding (review in Afton and Paulus 1990). Small anatids depend on exogenous foods to meet most metabolic demands during incubation and take two 2 Present address: Maryland Department of Natural Resources, P.O. Box. 68, Wye Mills, Maryland 21679 USA. to three recesses each day to forage (Afton 1980, Hohman 1986). Successful development of bird eggs occurs within a relatively narrow range of incubation temperatures (White and Kinney 1974). Cooling of eggs increases as ambient temperature decreases, and as time away from the nest by incubating individuals increases (Caldwell and Cornwell 1975, Afton 1979). Short-term declines in egg temperature, however, apparently have little effect on hatching success (Vleck 1981, Haftorn 1988). Nevertheless, a decrease in average egg temperature may lengthen the incubation period, which exposes the nest to greater risk of predation and increases the energy expended by developing embryos (Vleck et al. 1980, Booth 1987). Greater amounts of energy used by embryos of precocial species before hatching may decrease the size of residual yolk reserves that are important to newly hatched chicks for maintenance and growth (Peach and Thomas 1986). Many species of birds modify activity patterns during incubation in response to variation in weather and food availability (Caldwell and Cornwell 1975, Cartar and Montgomerie 1985, 756 The Auk 107: 756-764. October 1990 This content downloaded from 157.55.39.124 on Mon, 16 Jan 2017 18:11:55 UTC All use subject to http://about.jstor.org/terms October 1990] Incubation Costs of Wood Ducks 757 Drent et al. 1985). Large-bodied species are affected less by environmental factors than smallbodied species (Afton 1980). Flexibility of incubation patterns within and among species suggests there is a tradeoff between maintaining body condition during incubation and providing eggs with a suitable environment for development. If time and energy constraints are important during incubation, then attentiveness at the nest should increase as body condition or food availability increases, assuming that greater attentiveness shortens the incubation period and increases hatching success (Martin 1987). Several studies support this idea. Aldrich and Raveling (1983) reported that female Canada Geese (Branta canadensis moffitti) that began incubation in good condition spent more time on the nest and had shorter incubation periods than females in poor condition. In years when food was abundant, European Starlings (Sturnus vulgaris) spent less time feeding, and some females were able to incubate without assistance from their mates (Drent et al. 1985). Female Blue Tits (Parus caeruleus) that were given a food supplement during incubation had shorter incubation periods and greater hatching success than females that were not provisioned (Nilsson and Smith 1988). Loss of body mass during incubation may reflect the need to provide constant care for developing embryos (Sherry et al. 1980), or it may enable females to reduce wingloading and to conserve energy during brood rearing (Freed 1981). However, a critical body mass certainly exists for individuals during incubation. Below that threshold, birds either spend more time feeding (Aldrich and Raveling 1983) or they abandon the nest (Drent 1975, Ankney and MacInnes 1978, Jones 1987). Body mass of female waterfowl during the annual cycle typically is lowest at the end of incubation (Afton and Paulus 1990). Ability of individuals to balance the conflicting demands of incubation may influence current and future reproductive suc-

Recruitment and Natal Philopatry of Wood Ducks

We tested whether hatch date and body mass at hatching affected recruitment of female Wood Ducks (Aix sponsa) to a breeding population in South Carolina. During six breeding seasons, day—old ducklings (n = 2945) were individually marked before leaving the nest. Females were recaptured later while nesting, and recruitment averaged 5.2% with no yearly differences. Most (82%) of the returning females nested as yearlings, but drought conditions in one year postponed the breeding of some females until they were 2 and 3 yr old. Most (60%) females did not return to nest on natal areas, but dispersed to sites a short distance away (mean = 1.6 km). Probability of dispersal was not related to competition for nesting space, and dispersing females did not begin nesting later than females that remained on natal areas. There was no evidence that early—hatched females had greater probabilities of being recruited than late—hatched females. In fact, late—hatched females had greater recruitment in two of six years than females that hatched early in the season. There also was no relationship between hatch date and the time that female Wood Ducks initiated their first nests. Heavy ducklings at hatching had higher probabilities of being recruited in one of six years, but composite statistics showed no overall relationship. We suggest that hatch date affects recruitment more at northern latitudes where time for producing and rearing offspring is short. Individuals hatching late at high latitudes may have insufficient time to mature before they must begin autumn migration.

Incubation temperature affects multiple measures of immunocompetence in young wood ducks (Aix Sponsa)

Parental effects play a vital role in shaping offspring phenotype. In birds, incubation behaviour is a critical parental effect because it influences the early developmental environment and can therefore have lifelong consequences for offspring phenotype. Recent studies that manipulated incubation temperature found effects on hatchling body composition, condition and growth, suggesting that incubation temperature could also affect energetically costly physiological processes of young birds that are important to survival (e.g. immune responses). We artificially incubated wood duck (Aix sponsa) eggs at three biologically relevant temperatures. Following incubation, we used two immunoassays to measure acquired immune responses of ducklings. Ducklings incubated at the lowest temperature had reduced growth, body condition and responses to both of our immune challenges, compared with those from the higher temperatures. Our results show that incubation temperatures can be an important driver of phenotypic variation in avian populations.

Characteristics and consequences of nest-site fidelity in wood ducks

-We used nine years of nesting data from a population of Wood Ducks (Aix sponsa) using nest boxes to test predictions regarding proximate controls of nest-site fidelity and the consequences of returning to the same nest site. Overall, 41.9% of females returned to the same nest box in year t + 1, 37.5% nested in a different box on the same wetland, and 20.5% of females moved to a different wetland to nest. There were no yearly differences in the degree of nest-site fidelity, and females using different wetlands between years travelled a median of two wetlands and moved an average distance of 1.3 km. Females nesting successfully used the same nest box to a greater extent in year t + 1 than females that were not successful. The positive association between nest success and nest-site fidelity also occurred within breeding seasons. Degree of nest-site fidelity exhibited by females was similar within and between breeding seasons. After controlling for variation in nest success, nest-site fidelity of yearlings did not differ from that of adults. Proportion of females returning to the same box in year t + 1 was not correlated with estimated population size of breeding females in that year. Females returning to the same box nested earlier than females using different boxes, but clutch size did not differ. Overall, females nesting in the same box did not have greater nest success in year t + 1, were not more likely to have nests parasitized, and did not survive better to year t + 2 than females nesting in different boxes. However, females that nested unsuccessfully tended to improve nest success by moving to a different nest box. Received 1 August 1991, accepted 18 February 1992. MANY SPECIES of migratory birds show a high degree of fidelity to previous breeding sites both within and between seasons (Greenwood and Harvey 1982). Males of most species have greater breeding-site fidelity than do females (Greenwood 1980). In waterfowl, however, female-biased natal philopatry and nest-site fidelity is the rule (Rohwer and Anderson 1988). Pair bonds are formed on winter areas or during spring migration, and the pair returns to the females natal area or previous nesting location (Dow and Fredga 1983, Hepp et al. 1989, Gauthier 1990). Widespread occurrence of breeding-site fidelity in birds suggests that the behavior is beneficial. Familiarity with an area may increase foraging efficiency, predator avoidance, dominance status, and the likelihood of pairing with a familiar partner, all of which may enhance reproductive success (Greenwood and Harvey 1982). Common Goldeneyes (Bucephala clangula), for example, that changed nest boxes nested later, produced smaller clutches, and had lower nesting success than females that did not change nest sites (Dow and Fredga 1983). Female Willow Ptarmigans (Lagopus lagopus) pairing with previous mates nested earlier and produced heavier chicks than females that switched partners (Schieck and Hannon 1989). The decision to return to a previous breeding site may involve several factors. Competition for nest sites may influence whether individuals return and may be especially important in cavity-nesting species (Dow and Fredga 1983). Previous experience is another factor influencing nest-site fidelity in birds. Individuals nesting successfully are more likely to return to the same nest site than individuals that are not successful (Gavin and Bollinger 1988, Gauthier 1990, Beletsky and Orians 1991; but see Haig and Oring 1988). Site quality may interact with nest success to influence subsequent nesting decisions (Weatherhead and Boak 1986, Bollinger and Gavin 1989). Nest-site fidelity also may be influenced by age, with yearlings having a greater probability of changing nest sites than adults (Newton and Marquiss 1982). Causes for age-specific differences in fidelity are unclear (Greenwood and Harvey 1982). It is possible that young individuals use poor-quality sites during initial nest attempts and move to betterquality sites when these sites become available.

PATTERNS OF NEST ATTENDANCE IN FEMALE WOOD DUCKS

Abstract We examined sources of variation in incubation patterns among female Wood Ducks (Aix sponsa), and investigated the effect of female nest attentiveness on incubation period. Data were collected from 44 females (n = 911 days) using temperature data loggers to monitor nest attendance throughout incubation. Mean (± SE) incubation constancy was 86.9 ± 0.6% and incubation period averaged 30.9 ± 0.2 days. Females took an average of two bimodally-distributed recesses per day. Duration of recesses averaged 98.6 ± 3.4 min, but were shorter in the morning than in mid-day or late afternoon. Body mass of incubating females declined 0.68 ± 0.2 g day−1, but there was no relationship between constancy and early incubation body mass or weight change of females. Incubation constancy was not correlated with length of the incubation period. For most females, incubation constancy and recess frequency did not change as incubation progressed. The fact that incubating females only lost an average of 3% of body mass, and constancy was not related to either body mass or length of the incubation period, suggests that females were not constrained energetically. Finally, we propose that the combination of reduced predation risk and the need of neonates to be more functionally mature at hatching has selected for longer incubation periods in Wood Ducks and other cavity-nesting waterfowl.

Population parameters and philopatry of breeding female wood ducks

Capture-recapture methods were used to estimate population size, survival rate, and recruitment to a breeding population of female wood ducks (Aix sponsa) in 1979-86. A total of 181 females was captured in nest boxes and banded during the 8-year period. Population size averaged 44 individuals. Mean annual survival rate was 0.55, and annual recruitment averaged 22 females. Data were used to illustrate the philopatric behavior of female wood ducks during the breeding season. J. WILDL. MANAGE. 51(2):401-404 Estimation of waterfowl survival rates has been improved by developing and using a series of models for analyzing band-recovery data (Brownie et al. 1978). Studies using these analytical methods have examined the relationship between survival and harvest rate (reviewed in Nichols et al. [1985]), population density (Anderson 1975, Conroy and Eberhardt 1983), and habitat conditions on breeding (Nichols et al. 1982) and wintering (Nichols and Hines, in press) areas. Capture-recapture methods allow estimation of population size and recruitment as well as survival, but are used infrequently to study avian population dynamics (Nichols et al. 1981, Pollock 1981). Open population models that allow gains and/or losses to occur between sampling periods seem particularly well-suited for long-term studies of waterfowl populations (Anderson and Sterling 1974, Sulzbach and Cooke 1979). In this paper we use 8 years of capture-recapture data from a breeding population of female wood ducks to estimate population size, recruitment, and survival and to determine whether wood duck hens are philopatric. We thank J. D. Nichols and J. E. Hines for helping with data analysis. J. D. Nichols provided an especially helpful review of an early draft of the paper. We also are grateful to the many people who helped in various ways durIPresent address: Indiana Department of Natural Resources, R.R. 4, Box 47, Peru, IN 46970. This content downloaded from 157.55.39.238 on Sat, 02 Jul 2016 05:33:15 UTC All use subject to http://about.jstor.org/terms 402 WOOD DUCK HEN SURVIVAL * Hepp et al. J. Wildl. Manage. 51(2):1987 ing the study, particularly L. D. Vangilder. This study was supported by a U.S. Dep. Energy Contract, DE-AC09-76SR00-819, with the Univ. Georgia (SREL).

Age-specific reproduction in three species of European ducks

-We tested the effects of female age on reproductive performance of Northern Shovelers (Anas clypeata), Tufted Ducks (Aythya fuligula), and Common Pochards (A. ferina) based on a long-term study (1958 to 1995) at Engure Marsh, Latvia. Yearling females initiated nests later than older (-2 years) females in each species, but female age explained little of the remaining variation in reproductive performance. Clutch size and brood size of all species declined seasonally. Age-specific increases in reproductive performance were most consistent between 1 and 2 years of age and were more apparent in the diving ducks than in Northern Shovelers. Clutch size, brood size, and duckling mass of yearling Tufted Ducks, and brood size and duckling mass of yearling Common Pochards, were smaller than those of older females. In Northern Shovelers, only duckling mass increased with age of the female. Nesting and hatching success did not vary by age for any species. Among 2-year-old females with and without previous breeding experience, experienced females nested five to six days earlier than inexperienced females in all species. Experienced, 2-year-old Tufted Ducks also had larger clutches and broods than inexperienced females. Effects of breeding experience generally lasted for only a single breeding season. Nesting date and duckling mass of yearling Northern Shovelers did not differ from that of inexperienced 2-year-olds. However, inexperienced 2-year-old Tufted Ducks and Common Pochards nested earlier and produced larger ducklings than did yearling females. Brood size of inexperienced, 2-year-old Common Pochards also was larger than that of yearlings. We found no evidence that age-specific increases in reproductive performance were related to differential survival of good breeders. Reproductive performance was constrained by past breeding experience in Northern Shovelers and by age and experience in Tufted Ducks and Common Pochards. Received 19 August 1996, accepted 22 May 1997. REPRODUCTIVE PERFORMANCE varies with parental age in many species of birds (Sather 1990). Young birds commonly nest later in the season, produce smaller clutches, and have lower fledging success than older conspecifics (Saether 1990, Forslund and Pirt 1995, Martin 1995). A better understanding of whether age influences reproduction is important for studies of demography and life-history evolution (Clutton-Brock 1988). Hypotheses proposed to explain age-specific variation in reproduction have focused on the concepts of constraint and restraint, which are not mutually exclusive (Curio 1983, Rohwer 1992). The constraint hypothesis proposes that young individuals lack some skill essential for high reproductive performance. Developmental or behavioral constraints, for example, may re3Present address: Gaylord Memorial Laboratory, School of Natural Resources, University of MissouriColumbia, Puxico, Missouri 63960, USA. E-mail: gaylord@sheltonbbs.com duce foraging success of young birds (Marchetti and Price 1989), thereby lowering reproductive performance (Desrochers 1992a). The restraint hypothesis suggests that the young are not less skilled than adults, but rather that they increase their probability of future reproduction by limiting current reproduction. This idea is based on life-history theory; i.e. residual reproductive value declines with age because of lower agespecific survival and reproduction (Curio 1983, Stearns 1992). In essence, reproductive events become more valuable with age; hence, older individuals invest more in reproduction than do younger individuals, causing age-specific differences in reproductive performance. Increased age-specific breeding performance also may result from differential survival of the more successful breeders (Clutton-Brock 1988, Rohwer 1992). We use data from a long-term study of breeding waterfowl on the Engure Marsh in Eastern Europe to examine age-specific (1 to 6 years old) differences in reproductive performance of

Potential effect of grass carp herbivory on waterfowl foods

Reservoirs in the southern United States provide important habitats for migrating and wintering waterfowl. Use of grass carp (Ctenopharyngodon idella) to control nuisance aquatic vegetation may reduce habitat quality for waterfowl because foods of grass carp and waterfowl overlap. In 1992-93 we used exclosures (1 m 2 ) to investigate effects of herbivory on introduced Eurasian watermilfoil (Myriophyllum spicatum; hereafter referred to as milfoil) and several other aquatic plant taxa in Guntersville Reservoir, Alabama. We compared exclosure and open plot treatments in milfoil and native plant areas in a large embayment. Milfoil within monospecific stands was not affected (P = 0.566) by herbivory in either year, but wet mass of milfoil at the edge of monospecific stands at 1 of 4 sites in 1993 was greater (P < 0.001) in exclosures than in open plots. Wet mass of native vegetation was greater (P < 0.001) in exclosures than in open plots in 1992-93. Taxa in native plant sites included muskgrass (Chara spp.), milfoil, southern naiad (Najas guadalupensis), slender spikerush (Eleocharis acicularis), pondweed (Potamogeton spp.), and spinyleaf naiad (N. minor; introduced exotic). In both years, milfoil and southern naiad dry mass was greater (P < 0.001 and P = 0.001, respectively) inside exclosures, while slender spikerush dry mass was greater (P = 0.043) outside exclosures. Dry mass of muskgrass and pondweed was greater (P < 0.001 and P = 0.002, respectively) inside exclosures than outside in 1992, but not different (P = 0.590 and P = 0.315, respectively) between inside and outside exclosures in 1993. Herbivory, predominately by grass carp, reduced native aquatic vegetation in some areas while milfoil remained unaffected. We discourage use of grass carp to control aquatic vegetation in areas dominated by plant species that are poorly consumed (i.e., milfoil) by grass carp without consideration of the potential effect on more palatable species.