Evidence for olfactory learning in procellariiform seabird chicks

Burrow nesting procellariiform seabirds use olfactory cues for both foraging and nest recognition. As chicks, burrow nesters develop in the dark, but are exposed to both prey‐related and individual‐specific scents through contact with their parents. This exposure suggests that chicks may have the opportunity to learn odours while still in the nest. In this study, we examined whether exposure to odourants during development might influence olfactory search behaviour expressed later in life. To test this idea, we exposed eggs of thin‐billed prions Pachyptila belcheri to a rosy‐scented novel odour (phenyl ethyl alcohol, PEA) or a control (water) just before hatching; chicks were then tested with these odours in a simple wind tunnel. Prior to fledging, subjects who had received pre‐exposure to PEA displayed head sweeps nearly twice as frequently as control birds did when presented with PEA. This study demonstrates that under natural rearing conditions, procellariiforms learn odour characteristics of their rearing environment in the nest.     

Parent-offspring recognition in bank swallows (Riparia riparia): II. Development and acoustic basis

In study 1, bank swallow (Riparia riparia) chicks were exchanged with like-aged chicks from other broods. Parents accepted chicks that were transferred into their nests at age 15 days or younger; rejection began to occur at 16 to 17 days. In study 2, chicks' vocalizations were recorded in the burrow. We found that an immature begging call given by young chicks is replaced by a ‘signature’ call at 15 to 17 days of age. An acoustic analysis suggested that these calls are individually distinctive. Study 3 was a playback experiment designed to test whether the chicks' signature calls are a sufficient cue for parental recognition. We found that parents would approach a speaker broadcasting the calls of their chicks in preference to one simultaneously broadcasting the calls of alien chicks. The pattern of results suggests that parental recognition is based on the chicks' signature calls and that development of recognition is dependent on the development of the call.     

Parent-offspring recognition in the barn swallow (Hirundo rustica)

Past research has shown that in the colonial bank swallow and cliff swallow, parents and offspring recognize one another by calls, enabling parents to locate and feed only their own chicks. To test the hypothesis that recognition traits are adaptations to coloniality, we examined parent-offspring recognition in the related but non-colonial species, the barn swallow. To allow cross-species comparisons, we used the same methods that had been used in the previous swallow studies. We carried out four studies. (1) Cross-fostering experiments done immediately before fledging gave no evidence of recognition. (2) In a playback experiment, parents gave no indication that they recognized the calls of their offspring. (3) In another playback experiment, chicks responded more strongly to the calls of their parents than to the calls of unrelated adults. The degree of recognition, however, was somewhat weaker than that seen in the two colonial swallow species. (4) Newly fledged young did not creche after fledging. Rather, family groups generally stayed apart from one another for almost 2 weeks, while parental care was still being given. The comparative data suggest that parent-offspring recognition via individually distinctive cues evolved in response to the intermingling of young associated with colonial living, and it thus weakly expressed in barn swallows compared to cliff swallows and bank swallows.     

The role of parent–offspring interactions during and after fledging in the Black-legged Kittiwake

Most bird species endure a high mortality at fledging, and selection should favour parental behaviour diminishing these costs. Post-fledging parental care varies greatly among species and is often linked to parent–offspring recognition. In the Black-legged Kittiwake (Rissa tridactyla), fledglings need to return to the natal nest to be fed by their parents until independence. Rejections of fledglings by non-parent adults may be fairly violent, and parents are expected to recognize and help their chicks at the time of first return. However, previous cross-fostering experiments pointed out that parents are not able to recognize their chicks up to 15 days before fledging. In this paper, we study the behaviour of both parents and juveniles at fledging. We found that parents answered significantly more to their fledgling's calls than to those of others. Compared to silent juveniles, juveniles that called before landing were more likely to be accepted by their parents. No such pattern was observed with foreign juveniles, indicating that fledglings’ voice may carry individual identity. Furthermore, fledglings found their way back to the natal nest faster when parents attended the natal nest and reacted to their offspring's calls than when they were absent or inactive. Such interactions may therefore diminish juvenile mortality at fledging.     

Sibling Recognition in Bank Swallows (Riparia riparia)

Observations of the behavior of newly-fledged bank swallows suggest that sibling recognition may be a mechanism promoting location of the home burrow in their large, dense colonies and of cohesion of family groups following departure from the burrow. We tested for sibling recognition in the field by comparing the antiphonal response of sibling groups to the recorded calls of own vs. unrelated sibling groups. Birds responded more to the calls of their own groups. In a laboratory experiment we raised chicks in isolation from 8–10 to 20 days of age and exposed them to a call of an unrelated chick. When tested in a choice situation at 15–20 days, chicks approached the familiar call in preference to a different call which they had not previously heard. We suggest that sibling recognition is based on familiarity, i.e., that it requires a period in which the calls of siblings are learned.     

On the responses of laughing gull chicks (Larus atricilla) to the calls of adults II. Age changes and responses to different types of call

Three age-groups of laughing gull chicks were tested with playback of recordings of calls of their parents and calls of neighbouring adults. The chicks in each group showed response to the playback calls, and recognition of the voices of their parents. The chicks in the early group (1 to 3 days post-hatching) showed the least evidence of parent recognition: the chicks of the late group (12 to 28 days post-hatching) showed the lowest levels of response in general.Evidence of relationships between variation in the behaviour in the tests and variation in the test recordings was found from correlation analysis, the type of call initiating positive response, and analysis of temporal association. This evidence, and the results of tests which allowed responses to the parents' crooning and responses to the parents' ke-hah calls to be compared for chicks in the late group, indicate that whereas the filial approach behaviour of very young chicks is stimulated by crooning but suppressed by ke-hah and long-calls, this behaviour in older chicks requires the occurrence of ke-hah calls or long-calls for its elicitation. However the ke-hah calls and long-calls of adults other than the parents continue to have negative effects on the behaviour of older chicks.It is argued that this progression in discrimination of the voices of the parents and the changes in responsiveness to the different types of adult calls are consistent with functional requirements, both from the point of view of changes in a growing chick's social situation and from the point of view of the characteristics of the calls. The changes are also discussed from a developmental point of view.     

Why does the herring gull lay three eggs?

Food supplements placed daily beside the nests of herring gulls, Larus argentatus, for the first 5 days after the first chick hatched produced improved weight gains over this initial period and higher fledging success, particularly in the third chick. The fledging success of the fed group appears to be due to increased weight gain and not to increased parental protection in the supplemented period. Since there is indirect evidence that food is available this suggests that the parents are putting less effort into foraging for their chicks than they are able to, and less than is in the interests of the third chick, in the first days after hatching. On a separate colony we found that having three chicks in the brood for more than 5 days resulted in lower weight gains for the second chick, but not the first. We suggest that fledging three chicks rather than one or two greatly increases the parents' reproductive effort, and consequently interpret the third egg as primarily insurance against the loss of the first or second.     

Taming parent‐reared orange‐winged Amazon parrots by neonatal handling

Tameness in parrots is often achieved by artificial rearing, in which chicks are typically removed from parents, fed a liquified or semi‐liquified diet by oral gavage and maintained in thermally controlled brooders until they are grown. As an alternate means of rearing birds, we tested whether occasional neonatal human handling of parent‐reared chicks might produce tameness while reducing the risk of sexual imprinting on humans. Orange‐winged Amazon chicks (Amazona amazonica) were incubated and hatched by wild‐caught parents, then were temporarily removed from the nest box, and handled at various times during the nestling period. In Trial 1, handled chicks (n = 6) were handled from days 10 to 39 of age for 10–20 min/day and from 40 days to fledging (days 56–/57) for 20–30 min/day. Nonhandled chicks (n = 4) were handled only to record body weight and provide medication, as needed. After fledging, chicks were evaluated for tameness, e.g., by their willingness to approach the handler, perch on a finger, be touched on the head, and by their respiratory rate in the presence of the handler. Handled birds differed significantly in all indices of tameness. In Trial 2, handled chicks were handled for 30 min, four times/week either from days 15 to 36 (n = 3) or 35 to 56 (n = 3); results were similar to Trial 1. Chicks handled later tended to be slightly tamer than those handled earlier. In both trials, the amount of time that handled chicks were in contact with humans was less than 2% of the time they spent with conspecifics. It is therefore unlikely that these chicks imprinted either filially or sexually on humans, although this has not been experimentally tested. While continued handling is likely necessary to maintain tameness, these results support the concept that neonatal handling of parent‐raised parrots provides a low‐labor and low‐technology alternative to artificial rearing as a means of initially taming birds, thereby improving their adaptation to life in captivity. Zoo Biol 18:177–187, 1999. © 1999 Wiley‐Liss, Inc.     

Alarm responses are maintained during captive rearing in chicks of endangered kaki

The maintenance of species-specific behavioural repertoires and traditions is an important but often implicit goal of conservation efforts. When captive rearing is used as a conservation practice, it becomes critical to address its possible implications for the social and behavioural traits of developing individuals. In particular, animals must retain or acquire many of their behavioural abilities to increase the likelihood of survival upon release into the wild. This study investigated the behavioural development of critically endangered kaki (black stilt: Himantopus novaezelandiae ) chicks reared without live adult conspecifics. The captive rearing programme included playbacks of adult kaki alarm calls during cleaning and handling of precocial chicks housed as groups. We used videotaped observations and playback experiments to address the following questions: do kaki chicks respond differentially to (1) familiar versus unfamiliar adult kaki alarm calls and (2) conspecific alarm versus heterospecific control vocalizations. Adult-naïve kaki chicks exhibited a varied behavioural repertoire over their early development. In multivariate analyses, when age was statistically controlled, chicks showed responses to familiar and unfamiliar alarm calls that were similar in magnitude. In contrast, following conspecific alarm calls chicks had longer average latencies to resume pre-playback activities than following heterospecific vocalizations. Although the generality of these conclusions is limited by experimental constraints stemming from working with an endangered species, the findings suggest that current management techniques produce captive-reared kaki for release into the wild that possess many of the behavioural and auditory recognition skills that are required for survival.     

Acoustic systems are adapted to breeding ecologies: individual recognition in nesting penguins

In all species of penguins studied to date, the display call, or parental call, has been demonstrated experimentally to facilitate identification between mates and between chicks and parents. We investigated parent-chick recognition in two nesting species, the Adélie penguin, Pygoscelis adeliae, and the gentoo penguin, P. papua. Through playback experiments, we tested the capacity of chicks to recognize the parental call at varying levels of background noise. By using modified calls, we found that chicks of neither species used temporal characteristics of the parental call (variations in frequency or amplitude with time) for individual recognition, but that both species used a simpler parameter, the pitch of the call. This finding contrasts with the more sophisticated use of acoustic cues by chicks of two non-nesting species, identified in earlier work. These differences in auditory processing of parental calls may have evolved because of different ecological constraints, particularly whether recognition of a nest site supports mutual identification of parent and offspring. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Chick Begging Calls Reflect Degree of Hunger in Three Auk Species (Charadriiformes: Alcidae)

Begging behaviour is an important element in the parent-offspring conflict; it has been studied in many avian species. However, the majority of the studies have been entirely based on the call counts, and they agreed that vocal activity was a good indicator of chick’s nutritional need and/or condition. Fewer researches were dedicated to the temporal-frequency variables of the begging calls themselves and they showed contrary results. Here begging behaviour in three burrow nested, uniparous species of auks (Alcidae) was studied. These objects provide an opportunity to study the signalling value of begging calls in the absence of important confounding factors such as nestling competition and predation pressure. I recorded calls of individual chicks in two conditions: during natural feeding and after experimental four-hour food deprivation. I found that almost all measured acoustic variables contain information about the chick’s state in all studied species. The hungry chicks produced calls higher in fundamental frequency and power variables and at higher calling rate compared to naturally feeding chicks. The effect of food deprivation on most acoustic variables exceeded both the effects of individuality and species. In all studied species, the frequency variables were stronger affected by hunger than the calling rate and call durations. I suppose that such strong change of acoustic variables after food deprivation can be explained by absence of vocal individual identification in these birds. As parents do not need to check individuality of the chick in the burrow, which they find visually during the day time, the chicks could use all of the acoustic variables to communicate about their nutritional needs.     

Fledging success of little auks in the high Arctic: do provisioning rates and the quality of foraging grounds matter?

Long-lived birds often face a dilemma between self-maintenance and reproduction. In order to maximize fitness, some seabird parents alternate short trips to collect food for offspring with long trips for self-feeding (bimodal foraging strategy). In this study, we examined whether temporal and spatial variation in the quality of foraging grounds affect provisioning and fledging success of a long-lived, bimodal forager, the little auk (Alle alle), the most abundant seabird species in the Arctic ecosystem. We predicted that an increase in sea surface temperature (SST), with an associated decrease in the preferred Arctic zooplankton prey, would increase foraging trip durations, decrease chick provisioning rates and decrease chick fledging success. Chick provisioning and survival were observed during three consecutive years (2008–2010) at two colonies with variable foraging conditions in Spitsbergen: Isfjorden and Magdalenefjorden. We found that a change in SST (range 1.6–5.4 °C) did not influence trip durations or provisioning rates. SST was, however, negatively correlated with the number of prey items delivered to a chick. Furthermore, provisioning rates did not influence chick’s probability to fledge; instead, SST was also negatively correlated with fledging probability. This was likely related to the prey availability and quality in the little auk’s foraging grounds. Our findings suggest that predicted warmer climate in the Arctic will negatively influence the ability of parents to provide their chicks, and consequently, the fledging prospects of little auk chicks.     

Food Provisioning in Red-Necked Grebes (Podiceps Grisegena) at Common Carp (Cyprinus Carpio) Ponds

Parental feeding patterns were studied in red-necked grebe (Podiceps grisegena) broods throughout the entire period of parental care in a common carp (Cyprinus carpio) fish-pond area in SE Poland in 1993–2002. Fish formed a substantial part of prey provided to the flightless young from their second week of life. Although the numbers of large invertebrates and tadpoles, the alternative prey to fish, did not decrease during the chick rearing period, grebe parents gradually shifted from delivering predominately invertebrates to delivering fish, and the average size of fish fed to chicks increased with brood age. Broods with relatively high fledging success (at least two chicks fledged) had a larger proportion of fish in their diet than broods seriously reduced because of undernourishment. The dive duration of foraging grebe parents did not differ between carp, wild fish and non-fish prey, but carp prey required significantly more time for handling. The percentage of prey rejected by chicks increased over the prefledging period from 2 to 24%. Of the prey rejected, 82% were fish apparently too large for the young to swallow. Fish prevalence in the diet of red-necked grebe chicks at carp ponds contradicts the results of other studies on the feeding habits of the nominative subspecies during breeding season. However, the red-necked grebe is a gape-limited predator and the piscivory of the chicks is limited to small-bodied fish.     

Intraspecific kleptoparasitism improves chick growth and reproductive output in Common Terns Sterna hirundo

Kleptoparasitism is a well‐known foraging strategy used opportunistically by many seabirds. Here, we investigated the effect of intraspecific kleptoparasitism on chick growth and reproductive output in Common Terns Sterna hirundo. Effects were compared between two groups comprising (1) individuals using kleptoparasitism during the chick‐rearing period (kleptoparasitic group, n = 18), and (2) individuals in pairs that never performed kleptoparasitism throughout the season (‘honest’ group, n = 21). The null models best described variation in mass at day 3 and the pre‐fledging mass, indicating no significant effect of the explanatory variables. However, the best models describing the linear growth rate (days 3–13) and peak mass included the parents' foraging strategy (kleptoparasitic vs. honest parents) as an explanatory variable. These two growth parameters were higher in chicks of kleptoparasitic parents. Kleptoparasitic foraging strategy was also associated with higher pre‐fledging survival, as the reproductive performance (i.e. number of fledglings) was significantly higher in the kleptoparasitic than in the honest group. We suggest that by stealing food (and consequently feeding offspring more frequently with high‐quality prey), kleptoparasitic parents are able to produce higher quality chicks with enhanced survival.     

Parent-offspring recognition in bank swallows (Riparia riparia): I. Natural history

A field study of the highly colonial bank swallow (Riparia riparia) revealed several contexts in which parent-offspring recognition occurs. Parents find their young away from the bank when the young make spontaneous flights from the burrow, and also when the young, after such flights, have returned to incorrect burrows. The resident adult in the latter situation also shows recognition, by ‘evicting’ alien chicks. Resident adults also make mistakes, however, and feed alien chicks. An analysis of these mistakes revealed that (a) the majority of mistakes are made by the male parent, and (b) mistakes generally do not exceed 0.5% of the parent's total feeding bouts. Parents also feed young in a crèche away from the bank, both before and after the burrow is vacated.     

Variation in faecal corticosterone metabolites in an Arctic seabird,the Little Auk (Alle alle) during the nesting period

Glucocorticoids participate in the control of whole body homoeostasis and an organism’s response to stress. Corticosterone, which is the principal glucocorticoid in birds, has been shown to increase in response to different energetic demands and perturbations that individuals have to cope with. In this study, a non-invasive method to examine the corticosterone secretion by measuring faecal corticosterone metabolites (FCM) has been established for an Arctic seabird, the Little Auk (Alle alle). A group-specific immunoassay was successfully validated for adults and chicks using an adrenocorticotropic challenge test. Then, FCM levels were investigated under different energetic and physiological demands, determined by weather conditions, week of chick rearing in adults, and age in chicks. The amount of rainfall had no effect on FCM levels in adults, whereas it negatively affected FCM levels in chicks. There was no variation in FCM concentrations among weeks of chick rearing in adults. In chicks, the FCM levels increased with age. Moreover, chicks with higher FCM levels had lower body mass and fledged later than chicks with lower FCM levels. This study demonstrates that environmental stress such as poor weather conditions can trigger significant changes in corticosterone levels in seabird chicks. Furthermore, the results indicate that corticosterone may be involved in the physiological and behavioural adjustments necessary for successful fledging and post-fledging survival.     

Lipid reserves,fasting capability and the evolution of nestling obesity in procellariiform seabirds

Several alternative explanations have been proposed to account for the evolution of nestling obesity in a variety of avian groups. These predict quite different patterns of fat accumulation, storage and use by chicks of different ages. Yet surprisingly few studies have measured changes in body composition during chick development. We tested the applicability of these hypotheses for fulmars, Fulmarus glacialis, by direct measurement of changes in water, lipid and lean dry mass in growing chicks. Lipid and lean dry mass increased until ca. 70% of the way through chick rearing, but then levelled off. Total body water also increased until the same stage, but gradually declined thereafter, and it was this change rather than fat metabolism that resulted in mass recession. The observed pattern of a continued increase in stored lipid, and most importantly, its maintenance all the way through the mass-recession phase until chicks reach fledging, is incompatible with many of the proposed hypotheses. We suggest that the most likely ultimate explanation for large fat deposits is to fuel chicks during the initial critical period away from the nest site while they learn to forage     

Seasonal changes in the provisioning behaviour and mass of male and female wandering albatrosses in relation to the growth of their chick

Procellariiform seabirds have a number of extreme life-history characteristics in common, in particular low reproductive rates and slow postnatal development, which are generally assumed to reflect the difficulty in acquiring energy in the marine environment. The wandering albatross (Diomedea exulans) is a sexually dimorphic species with the longest postnatal growth found in any bird, suggesting severe constraints on provisioning and possible sex-specific strategies of provisioning. We studied the provisioning behaviour and mass changes of male and female parent wandering albatross throughout the 9-months rearing period to examine how each sex adjusts its foraging effort in relation to the needs of the chicks and the seasonal changes in food availability. The study was carried out on the Crozet Islands, using an automated system recording continuously the attendance pattern of parents between March and December 1994. During the brooding period when energy requirements are highest, parents only perform trips of short duration to sea, and their body condition deteriorates. When the chick is old enough to be left alone, the parents mix short and long foraging trips. The proportion of short trips is very high until July, allowing high rate of food delivery and rapid growth, and at the same time the body condition of adults improves. From August this proportion declines until fledging in December. As a result, the feeding rate decreases from August and adult condition declines, suggesting that feeding conditions at sea are better during the first part of the chick-rearing period, i.e. in autumn and winter. Male parents perform more short trips of shorter duration and provide larger meals than females, delivering an estimated total after brooding of 110 kg of food, compared to 70–80 kg delivered by females. Meal size is inversely related to the body condition of male chicks but not to that of female chicks, suggesting that food delivery is regulated by the adults in response to the condition of the male chick. Male chicks received larger meals and more food every month than female chicks, and overall it was estimated that they receive, after brooding, 195 kg of food compared to 180 kg for the female. As a result, male chicks have a higher growth rate, attain a higher asymptotic mass, and are larger and heavier at fledging than female chicks. However, the differences are relatively small between the chicks of each sex and suggest that energy may be used differently between the sexes to maximise fitness. The results of the study suggest that provisioning effort of wandering albatrosses is adjusted by parents in relation to the availability of food, to the energetic needs of the chick and to the sex of the chick. The adult body mass is likely to play an important role in the long term for the regulation of provisioning, deficits in body mass probably providing the buffer in high power-requirement periods. Accepted: 20 March 2000     

Timing of fledging is influenced by glucocorticoid physiology in Laysan Albatross chicks

Fledging is a major life transition for birds, when juveniles move from the safety of a nest into an environment where they must find food and avoid predators. The timing of fledging within a season can have significant effects on future survival and breeding success. Proximate triggers of fledging are unknown: though wing development is likely a primary factor, other physiological changes, such as elevated plasma corticosterone (CORT), may affect fledging behavior. Laysan Albatross (Phoebastria immutabilis) chicks have an extended post−hatching period during which they reach 150% of adult mass. However, approaching fledging, chicks fast for days to weeks and lose mass while still putting energy into feather growth. We evaluated chick morphology and physiology to elucidate proximate triggers of fledging. As in some other species, CORT increased as chicks fasted and lost body mass. At the same time, corticosteroid binding globulin (CBG) declined, thus amplifying free CORT prior to fledging. Once chicks reached a morphological threshold, free CORT levels predicted how long they stayed at the colony: chicks with higher free CORT fledged sooner. To perturb the relationship between body condition, endocrine physiology, and fledging behavior, we supplementally fed chicks for the month before fledging. Fed birds had a slower decrease in body mass, slower decrease in CBG, slower increase in free CORT, and stayed at the colony longer after reaching a morphological threshold. Our study suggests that as chicks lose mass, free CORT acts as a signal of energetic or nutritional state to adjust the timing of fledging.     

Sex differences in begging vocalizations of nestling barn swallows, Hirundo rustica

Parents of sexually reproducing species should adjust their investment in production of sons and daughters in relation to the relative costs and reproductive value of offspring of either sex. Sex allocation mediated by differential allocation of care such as food provisioning, however, requires that parents can identify offspring sex. We analysed sex differences in offspring begging calls that may serve as a cue for parents to discriminate between sons and daughters. A combination of three sonagraphic variables of begging calls of nestling barn swallows allowed us to classify them according to sex at day 16, but not at day 12 after hatching, suggesting that sex differences in begging calls arise during the nestling period as the time of fledging approaches. Hence, parents may be able to discriminate between sons and daughters by auditory cues, which would enable differential allocation of food between offspring during the late nestling and early fledging stages. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.