Semi-precocial Species Research Articles

Baseline and stress-induced prolactin and corticosterone concentrations in a species with female offspring desertion – The case of Whiskered Tern Chlidonias hybrida

To understand the proximate mechanisms regulating brood desertion, we studied hormonal and behavioural stress responses during the chick-rearing period in adult Whiskered Terns (Chlidonias hybrida), a socially monogamous, semi-precocial species with prolonged post-fledging parental care. In contrast to males, almost all females of this species desert during the chick-rearing and post-fledging periods. Because of the expected link between corticosterone, prolactin and parental investment, we hypothesized that males and females should differ in circulating prolactin and corticosterone concentrations. Baseline hormone concentrations did not differ between males and females. In both sexes, prolactin and corticosterone concentrations decreased and increased in response to acute stress (30 min after capture), respectively. Baseline and stress-induced prolactin concentrations decreased significantly in both sexes with advancing brood age. As expected, males had significantly higher stress-induced prolactin concentrations than females. None of the nine males released after being held in captivity for 24 h deserted, whereas four (29%) of the 14 females kept in captivity for 24 h did so. Altogether, these results suggest that higher prolactin concentrations may be involved in the maintenance of parental care under stress. However, there was no statistically significant difference in stress-induced hormone levels between males, females that deserted and those that returned to the nest after prolonged stress (24 h). Our data indicate that males are probably more resistant to stress as regards the continuation of parental care. The pattern of male and female behavioural and hormonal responses to stress partially predicts their behaviour in terms of natural desertion.

Development of the Visual System in a Burrow-Nesting Seabird: Leach's Storm Petrel

Little is known about the development of vision in wild birds. It is unknown, for example, whether the ability to see can be predicted by the level of prenatal growth or whether the eyes are open at hatching in a particular species. In this study, we investigated the growth of eyes, the formation of retinal ganglion cell topography, and the appearance of simple, visually guided behaviours in chicks of a small procellariiform seabird, Leach's storm petrel (Oceanodroma leucorhoa). This semi-precocial species, which has a well-developed sense of smell, nests in underground burrows where adults provision chicks for 6-8 weeks in the dark before fledging. Retinal ganglion cell topographic maps revealed that fine-tuning of cell distribution does not happen early in development, but rather that the ganglion cell layer continues to mature throughout provisioning and probably even after fledging. While the olfactory bulbs reached adult size around 7 weeks after hatching, the eyes and telencephalon continued to grow. Optokinetic head response and artificial burrow finding experiments indicated that chicks in the 2nd week after hatching lack even the most basic visually guided behaviours and are probably blind. Thus, vision in Leach's storm petrel chicks starts to function sometime around the 3rd week after hatching, well after the eyes have opened and the olfactory system is functional.

An Effective Method for Trapping Both Parents and Chicks of Whiskered Terns (Chlidonias hybrida) and Its Impact on Breeding Success

Abstract. A method for trapping both parents of Whiskered Terns (Chlidonias hybrida), a semi-precocial species, using enclosures that allow access to the chicks until they fledge is described. The approach combines the gradual installation of enclosures with their subsequent, temporary conversion into traps used to capture adult birds. The success rate for trapping both mates on the target nests (n = 83) was 77%. Nest desertions after the erection of the enclosure and after trapping were 1% and 3%, respectively. A high effectiveness of trapping both parents and a low percentage of losses can be achieved with the gradual installation of the enclosure and the birds' habituation to it. This trapping technique is safe and efficient, enabling researchers to collect samples from all family members with ease.

Effect of rapid modulation of circulating plasma testosterone concentration on begging, aggressive behavior and competition for food in black-headed gull (Larus ridibundus) chicks

Sibling competition mediated by begging behavior is extremely common in avian species and recent studies have highlighted the role of endogenous testosterone in regulating such phenomenon. However, current literature depicts an inconsistent pattern in altricial vs. semi-precocial species, with stimulating versus inhibitory effects of the hormone respectively. This is possibly due to a difference in the methodology of hormone treatment (short-term moderate dose versus a long-term stronger elevation, respectively) between the studies performed so far. In this study, we induced short-term moderate peaks in plasma testosterone levels, as applied in altricial bird species, and assessed the effects of our manipulation on begging, competitive and aggressive behavior in black-headed gull (Larus ridibundus) chicks, a semi-precocial species. Our results suggest that, unlike in altricial songbirds, temporary increase of plasma testosterone concentration suppresses begging and enhances aggressiveness towards intruders. However, it also increases aggression and the chances of getting priority while scrambling with nest mates to gain access to food. Thus, the inconsistencies in the hormonal control of begging behavior observed between altricial vs. semi-precocial birds seem real and perhaps related to species differences in complexity of the display and the nature of competition. These may be elucidated by future comparative studies.

Sex-specific vulnerability to breeding conditions in chicks of the sexually monomorphic Gull-billed Tern

Environmental conditions during early development may differentially affect male and female offspring, and the effects of this sex–environment interaction in chick performance may be exaggerated under harsh conditions. In birds, most of the currently available evidence on sex-biased environmental sensitivity in nestlings is derived from species that display sexual size dimorphism, while studies on monomorphic or slightly dimorphic species are less abundant and have produced inconsistent results. We have evaluated sex-specific vulnerability to breeding conditions in chicks of the Gull-billed Tern (Gelochelidon nilotica), a semiprecocial species with only low sexual size dimorphism. We compared male and female mass growth and fledgling physiological condition (measured through plasma metabolite levels) in several colonies that differed in reproductive parameters. Chicks of both sexes grew more slowly and fledged with lower mass and poorer nutritional state in the colony with the worst breeding conditions, i.e., with later phenology and lower clutch size and reproductive success. Contrary to our expectations, chick vulnerability to rearing conditions was more pronounced for female than male fledglings. While males grew faster than females during the middle phase of growth regardless of colony, this difference disappeared later in the fledging period in all but the worst colony, where females maintained a lower mass and worse nutritional condition than males. These results add to the evidence that, even in monomorphic species, the environmental sensitivity of nestlings during development may vary in a sex-specific way that may select for sex-biased allocation of parental resources and sex ratio adjustments under specific breeding conditions.

Do Large Eggs Favor the Growth of Chicks? An Experimental Study on a Semi-Precocial Seabird: Rhinoceros AukletCerorhinca monocerata

Avian egg size varies widely within populations and larger egg sizes reflect greater investment by the female parent. Whether, and how, the extent of egg size variation affects postnatal development, are important questions affecting our understanding of optimal resource allocation between pre- and post-hatching parental investment in altricial and semi-precocial species. Though much research has been carried out in the hope of answering these questions, the feeding ability of parents confounds the results. To verify a possible advantage of hatching from a large egg on chick growth, without the confounding effect of parental feeding ability, an artificial feeding experiment was carried out on the Rhinoceros Auklet Cerorhinca monocerata, a semi-precocial alcid species. Hatchlings from various sized eggs were reared with the same amount of food in separate cages. To verify the advantage of larger eggs, I tested whether the wing lengths of chicks from large eggs grew faster than those from smaller eggs; such growth is critical to chick survival at fledging. The hatchlings from large eggs were found to have greater mass, longer wings and better body condition than those from small eggs. The chicks from large eggs had greater growth only in their wings during the initial postnatal development. This accelerated growth resulted in them having longer wings at fledging. These results indicate that large egg size in the Rhinoceros Auklet provides a guarantee of chick growth and fledging success despite an unpredictable environment during the chick rearing period.

Mathematical modeling of appendicular bone growth in glaucous‐winged gulls

Development of locomotor activity is crucial in tetrapods. In birds, this development leads to different functions for hindlimbs and forelimbs. The emergence of walking and flying as very different complex behavior patterns only weeks after hatching provides an interesting case study in animal development. We measured the diaphyseal lengths and midshaft diameters of three wing bones (humerus, ulna, and carpometacarpus) and three leg bones (femur, tibiotarsus, and tarsometatarsus) of 79 juvenile (ages 0-42 days) and 13 adult glaucous-winged gulls (Larus glaucescens), a semiprecocial species. From a suite of nine alternative mathematical models, we used information-theoretic criteria to determine the best model(s) for length and diameter of each bone as a function of age; that is, we determined the model(s) that obtained the best tradeoff between the minimized sum of squared residuals and the number of parameters used to fit the model. The Janoschek and Holling III models best described bone growth, with at least one of these models yielding an R(2) > or = 0.94 for every dimension except tarsometatarsus diameter (R(2) = 0.87). We used the best growth models to construct accurate allometric comparisons of the bones. Early maximal absolute growth rates characterize the humerus, femur, and tarsometatarsus, bones that assume adult-type support functions relatively early during juvenile development. Leg bone lengths exhibit more rapid but less sustained relative growth than wing bone lengths. Wing bone diameters are initially smaller than leg bone diameters, although this relationship is reversed by fledging. Wing bones and the femur approach adult length by fledging but continue to increase in diameter past fledging; the tibiotarsus and tarsometatarsus approach both adult length and diameter by fledging. In short, the pattern of bone growth in this semiprecocial species reflects the changing behavioral needs of the developing organism.

Avian brood patch temperature: Relationships with female body mass, incubation period, developmental maturity and phylogeny

Brood patch temperatures (BPT) of 76 species of birds were collated from the literature and compared with female body mass (FBM) and incubation period ( I p) of the species concerned. Correlations between BPT and FBM and I p were associated with phylogenetic relatedness at a high taxonomic level (Order). BPT was highest in species producing altricial hatchlings, intermediate for precocial species and lowest for semi-precocial species. BPT was higher than embryo and egg temperatures reported in the literature implying that the process of heat transfer during contact incubation is unable to raise embryo temperature to core body temperature.

Effects of early incubation constancy on embryonic development: An experimental study in the herring gull Larus argentatus

1. In many birds, parental nest attendance in early incubation is variable, with eggs incubated only intermittently. The effect of this on chick hatching success is unknown. 2. We allowed clutches of a semi-precocial species, the herring gull, to experience different levels of early incubation constancy and examined the effects on embryonic development and hatching. 3. We found evidence that high early incubation constancy enabled some eggs to develop and hatch faster. Chicks that experienced high thermal constancy during early incubation had heavier body mass at hatching. 4. We discuss the factors that might constrain parental attendance early in incubation.

Endocrine and behavioural plasticity in response to juvenile stress in the semi-precocial rodent Octodon degus

The present study in the South American rodent Octodon degus shows for the first time that the postnatal development of hypothalamic-pituitary-adrenal axis function in this semi-precocial species differs from that of altricial rodents, i.e. rats or mice, in several aspects. Our experiments revealed a particular pattern of hypothalamic-pituitary-adrenal axis activity during the first 3 weeks of life characterized by (i) a period of low plasma glucocorticoid concentrations, during which (ii) brief stress exposure (1 h parental separation) is able to elevate glucocorticoids significantly. In addition, (iii) repeated stress exposure (1 h parental separation daily) during the first 3 weeks of life resulted in females, but not in males, in an attenuated separation-induced increase of glucocorticoids, and a higher behavioural activity in both sexes at postnatal day 21. These data indicate that parental separation early in life acts as a 'strong' stressor in this species, which on the long run can alter endocrine stress response at the time of weaning in a sex-specific manner. These findings support the role of the hypothalamic-pituitary-adrenal axis as one of the key factors mediating the effects of early life stress on the neuronal network and behaviour in O. degus.

Analysis of heart rate in developing bird embryos: effects of developmental mode and mass

Bird embryos may be regarded as developing in their thermo-neutral zone, at rest, and stay in the egg for a fixed period of time until hatching. It is therefore interesting to investigate if they follow the same ‘rule’ set for adult homeotherms, which states that, within a taxonomically or functionally defined category such as mammals or birds, the number of heart beats throughout the life span ( s L) is more or less constant. This rule stems from the allometric relationships between heart rate ( f H) and body mass ( m B) and between s L and m B. As a step towards understanding the general allometric nature of avian embryonic physiology we analyzed the f H values of avian embryos in relation to their incubation span ( s I). Data from 30 species were selected from the scientific literature for the analyses. Values obtained from invasive methods which were judged to grossly alter natural incubation conditions, or from undefined or unmatched temperature conditions were not used. These include most values obtained below the first 30% of the incubation. Also, data obtained after internal pipping were discarded since hatching activity influences them. Values for s I and egg mass ( m E) as representatives of embryonic mass were also collected. Embryonic f H was normalized to 70.1–80% s I. At 20.1–30% s I it was only 85% of the value at 70.1–80% s I and increased to a plateau at about 50.1–60% s I. It was almost constant among species between 50.1 and 60% s I and pre-internal pipping (PIP) time and thus, the mean f H value between 50.1 and 60% s I and between 90.1 and 100% excluding pipped eggs ( f̄ H) was taken as a representative value for each given species. The f̄ H (min −1) and the corresponding s I (days) values for the 30 species, scaled with m E (g) as follows: f̄ H=371.1 · m E −0.112 and: s I=12.29 · m E +0.209. Both powers were significantly different from 0. The product of f̄ H and s I ( f̄ H · s I), representing the total number of heartbeats throughout the incubation, scaled with m E for the entire data set as follows: f̄ H · s I=6.565 · 10 +6 · m E +0.096, where the +0.096 power is significantly different from 0. Values for f̄ H · s I from embryos of altricial birds tended to concentrate at the low m E end of the plot while those of the precocial ones tended towards the high end. Separate analyses showed that the m E power for the combined altricial and semi-altricial species (ASA), and the combined precocial and semi precocial species (PSP), of log f̄ H · s I against log m E regressions, were both insignificantly different from 0. Thus, means of f̄ H · s I for ASA and PSP were calculated. The mean ASA value of 7.27 · 10 +6 heartbeats for f̄ H · s I, was significantly different from the mean PSP value of 10.93 · 10 +6. The difference of 3.66 · 10 +6 (33.5%) heartbeats can be attributed to either the more advanced stage of the PSP hatchlings at hatch, to the larger m E values of these hatchlings, to the difference in water fraction of the hatchlings or all. The result of a linear regression of f̄ H · s I against the rate of s I completion (the inverse of incubation span, f I; day −1) was: f̄ H · 10 −6=0.205+3.940 · s I −1. Thus, the faster is the average rate of development accomplished per day (shorter incubation) the higher is daily heart rate. Data tended to cluster such that large eggs, mostly of the PSP type with relatively low f̄ H, complete 2–4% of their incubation per day, while small, ASA type eggs with relatively high f̄ H, complete 6–8% of their incubation time per day. We conclude that, at this stage of knowledge, the data is insufficient to resolve whether the different modes of hatch stage alone can explain differences in the total number of heartbeats throughout embryonic life among all bird species, or egg mass and water content differences contribute variability. This should be investigated on a larger sample of species in more depth.

Size-Selective Predation by a Specialist Forager, the Roseate Tern

Parent birds must be able to recognize and provide for the energetic demands of their chicks. In semiprecocial species, including many seabirds, the energy requirements of young birds reach a peak at some point before fledging, coinciding with the period of maximum growth (Dunn 1980, Ricklefs and White 1981). Thus, older chicks that are still growing require more food than they did at a younger age. During this time, the energy budgets of parent birds increase sharply, because they must maintain a positive energy balance as well as provide for the energy requirements of their chicks (Ricklefs 1983). Parents can adjust to this increased burden in three ways: (1) they can deliver a constant quantity of food to their young at an increasing rate, (2) they can maintain a constant feeding rate but deliver a larger quantity of food per trip, or (3) they can increase both food load and feeding rate. Terns appear to meet the increased demands of their chicks by delivering increasingly larger prey items rather than by increasing provisioning rate (Miller and Confer 1982, Wiggins and Morris 1987, Burger and Gochfeld 1991, Smith 1993, Shealer 1995) . The increases in prey size observed in terns suggest that they are capable of size-selective predation. Evidence in support of size-selective predation by adult seabirds has been weak, however, primarily because of confounding factors. First, terns and other seabirds feed primarily on small fish, usually youngof-the-year, or the 0 age class (Harris and Wanless 1991, Monaghan et al. 1992, Bertram and Kaiser 1993). Juvenile fish also are growing at this time, such that as seabird chicks grow larger, the average size of individuals in the prey base increases as well (Miller and Confer 1982). Therefore, studies that document an increase in the size of prey fed to chicks over time cannot infer size-selective predation without using other methods. For example, Burger and Gochfeld (1990) found that some Black Skimmers (Rhynchops niger) fed their mates consistently larger fish than were fed to chicks at similar times throughout the breeding season, suggesting that adults recognized and provided for the different needs of their dependents. Second, previous studies of piscivorous birds have demonstrated that size-selective predation differs with the structural complexity of the foraging habitat. In simple habitats without vegetative cover or shelter, predators showed a consistent preference for larger prey; however, when vegetation or cryptic substrates were added, this preference was less pro-

Thermal Responses of Late Embryos and Hatchlings of the Sooty Tern

Oxygen consumption (VO2) and body temperature (Tb) of young Sooty Terns (Sterna fuscata) were measured during late incubation and in the first 24 hr after hatching at ambient temperatures (Ta) between 28° and 38°C and between 15° and 43°C, respectively. Evaporative cooling by hatchlings at Ta of 36°-43°C was also measured. Significant increases in embryonic metabolic level occurred between external and internal pipping and between internal pipping and establishment of a pip hole. However, despite the improving access to oxygen produced by these events, VO2 and Tb both varied directly with Ta in an ectothermic pattern throughout the final stages of incubation. A capacity for sustained endothermy only became apparent in hatchlings. Their VO2 varied inversely with Ta between 27.5° and 36°C to an extent indicating a modest capacity for regulatory thermogenesis. This served to maintain Tb above 35°C in this range of Ta. The apparent abruptness of the appearance of this regulatory capacity after hatching suggests that emergence from the physical confinement of the egg could be an important proximate factor in the establishment of endothermy in this semi-precocial species. Hatchling Sooty Terns underwent a progressive fall in Tb with declining Ta below 27.5°C. On the other hand, they appeared quite proficient at evaporative cooling with increasing Ta between 36° and 43°C.

The influence of egg‐size, mass and composition upon hatching success in the short‐tailed shearwater Puffinus tenuirostris (Aves: Procellariiformes)

Short‐tailed shearwaters in Bass Strait, Australia, exhibited extreme synchronicity in laying during 1991. Egg dimensions and masses varied by approximately 40% between females and were related to the date of laying but not the fate of the egg at hatching. The composition of eggs was similar to other petrels, and typical of semiprecocial species. Larger egg‐size was attributable to relatively more albumen, but less yolk. Thus, hatching succcss may be proximately constrained by behavioural attributes of the patents.

Intraclutch Variation in Egg Weights of Pied-Billed Grebes

Much discussion has recently focused on the effects that quality of eggs, and hatching order of chicks, have on chick survival within avian broods. Chicks which hatch from larger eggs are heavier (e.g., Howe 1976), grow faster (e.g., Ankney 1980), and survive better (e.g., Lundberg and Viiis~inen 1979). Chicks which hatch later, however, generally have poorer survivorship (e.g., Parsons 1975). Thus there potentially exists either additive or opposing influences of egg quality and hatching order of chicks on chick survival. One rationale for examining whether or not such effects are additive has been an attempt to resolve controversy concerning the adaptiveness of hatching asynchrony (review by Clark and Wilson 1981). The only work on intraclutch variation in egg quality for grebes has been Fugle and Rothstein's (1979) examination of the effects of egg removal, from two clutches of Pied-billed Grebes (Podilymbus podiceps), on clutch size and egg-size determination. Grebe broods, however, show considerable hatching asynchrony (Cramp and Simmons 1977). For example, Forbes and Ankney (1987) found that broods of P. podiceps from clutches of five to eight eggs hatched over 3 to 7 days. Thus chicks within grebe broods may exhibit considerable differences in size at hatch completion due to hatching order (Nuechterlein 198 1, Forbes and Ankney 1987). Our objective was to determine whether or not variation in egg weights within clutches ofPied-billed Grebes was related to laying order of eggs. For both altricial (e.g., Richter 1984) and semiprecocial species (e.g., Horsfall 1984), laying order of eggs was a good predictor of hatching order of chicks and thus may be used for comparisons with egg quality (review by Slagsvold et al. 1984).

Intraclutch Variation in the Size, Mass and Composition of Ring-Billed Gull Eggs

In 1984, 94 complete three-egg clutches of Ring-billed Gull (Larus delawarensis) eggs were collected on Granite Island, northern Lake Superior. The fresh eggs (i.e., collected within 12 hr of being laid) were weighed, measured and frozen for later chemical analysis to determine if relationships existed between egg size, composition, and sequence. Egg size and mass decreased through the laying sequence. The average composition of fresh eggs was 35% yolk, 56% albumen, and 9% shell. Water accounted for 69% of fresh egg mass. Approximately 8% of fresh egg mass was yolk lipid. Dry yolk consisted of approximately 40% protein and 60% lipid. Caloric content averaged 1.55 kcal/g fresh egg mass. Within clutches, third-laid eggs contained absolutely less albumen and nutrients than earlier laid eggs. Albumen increased in proportion to the 1.2 power of egg mass, and the yolk in proportion slightly greater than the 0.66 power of egg mass. Results agreed well with egg composition studies of other semiprecocial species.

The Development of Endothermy and Existence Energy Expenditure in Herring Gull Chicks

The development of thermoregulation has been studied in a large number of altricial species (summarized in Dunn 1975a), but only for a few semi-precocial species (Behle and Goates 1957, Dawson et al. 1972, Palokangas and Hissa 1971, summary of others in Dunn 1976a). Of these few, only Drent (1965) and Palokangas and Hissa (1971) had any information for semi-precocial chicks older than about one week, and no one has investigated energetic costs of thermoregulation in the wild.