Offspring Recognition Research Articles

Release of classical transmitters and nitric oxide in the rat olfactory bulb, evoked by vaginocervical stimulation and potassium, varies with the oestrus cycle.

In vivo microdialysis was used to investigate the effects of ovariectomy and the oestrus cycle on vaginocervical stimulation-evoked classical transmitter and nitric oxide release in the olfactory bulb of anaesthetized (urethane) and conscious rats. During pro-oestrus/oestrus, vaginocervical stimulation (1 or 10 min) significantly increased concentrations of glutamate, aspartate, GABA, noradrenaline, dopamine and nitric oxide (citrulline) but failed to do so in met-oestrus/di-oestrus or following ovariectomy. Potassium chloride-evoked GABA, noradrenaline and nitric oxide release in the olfactory bulb was also significantly enhanced during pro-oestrus/oestrus. The effects of vaginocervical stimulation on olfactory bulb transmitter release during pro-oestrus/oestrus were significantly reduced by pelvic or vagus nerve section. Basal concentrations of classical transmitters and nitric oxide in the olfactory bulb did not vary across the oestrus cycle although noradrenaline and dopamine levels were reduced following ovariectomy. These results confirm our previous electrophysiological data showing that the olfactory bulb mitral cells are only excited by vaginocervical stimulation during pro-oestrus/oestrus. They also suggest that sex hormones acting primarily at the level of the olfactory bulb dramatically enhance the ability of vaginocervical stimulation to evoke release of both classical transmitters and nitric oxide in this region. Such alterations in neurochemical release in the olfactory bulb may be important for mediating plasticity changes underlying olfactory recognition of mates or offspring.

Individual sibling recognition in experimental broods of common tern chicks

Studies of kin recognition in birds have usually examined parent–offspring recognition, while studies of sibling recognition are relatively rare. Using choice experiments, we studied the development of sibling recognition among common tern, Sterna hirundo, chicks and tested the cues used for recognition. We collected newly hatched common tern chicks and raised them in a laboratory in 10 artificial broods of three. Chicks showed a significant preference for broodmates (‘siblings’) over familiar nonsiblings (nonsiblings from neighbouring broods) when first tested at 4 days posthatching, earlier than previously reported. Preferential approach to siblings was most common in broods with low levels of intrabrood aggression. Responsiveness of test chicks was highest when test chicks and stimulus chicks could both see and hear each other and lowest when they could only hear each other. Sibling-biased approach did not depend on stimulus and test chicks seeing each other, only on test chicks seeing (and probably hearing) stimulus chicks. Surprisingly, no preference was shown for siblings over strange nonsiblings, suggesting that a preference for siblings may involve learning the identity of not only siblings, but also of chicks from neighbouring broods.

Proximate and ultimate causes of adoption in ring-billed gulls

From 1987 to 1994, the annual frequency of adoption by breeding pairs at a Lake Erie ring-billed gull,Larus delawarensis, colony ranged from 3 to 37% (average 8%/year,N=7 years) and, on average, foster parents raised 0.5 fewer of their own chicks to fledging than pairs that did not adopt. The key evolutionary question is: why do some individuals apparently suffer the costs associated with a behaviour that appears to enhance the fitness of others? From 1992 to 1995, I investigated the proximate and ultimate causes of adoption in ring-billed gulls from the perspectives of both the foster parents and adopted chicks, and tested predictions that differentiated between various competing adaptive and nonadaptive hypotheses that have been proposed to explain it. While I was able to demonstrate a breeding cost, I failed to identify any benefits to foster parents. Thus, the adaptive hypotheses that rely on the foster parents benefiting were not supported (e.g. kin selection, reciprocal altruism, acquisition of parenting experience). From the foster parent’s perspective, adoption was mediated through errors in parent–offspring recognition. Under natural conditions, most fostering pairs were tending small chicks (<6 days old) at the time of adoptions; in chick-transfer experiments, resident parents did not discriminate against foreign chicks until their own chicks were 7–9 days old. Chicks (N=25) that subsequently abandoned their natal nests were lighter, and grew at a slower rate, than chicks that survived to fledging in their home broods. Thus, departing chicks were at a survival disadvantage in their home broods. Chicks that gained acceptance into foreign broods where they were older/larger than the resident chicks realized high survival at the expense of their foster siblings and parents. Based upon individual growth rates and the corresponding survival probabilities, disadvantaged chicks approximately doubled their survival chances through foster care. Why has selection not eliminated adoption? I argue that adoption is an evolutionary arms race between the two principle actor groups; disadvantaged chicks, which benefit through foster care, and host parents, which avoid providing foster care (e.g. infanticide). In ring-billed gulls, selection has failed to eliminate adoption because the long-term reproductive cost (estimated at 4%, this study) of an occasional adoption is probably offset by the relatively higher costs associated with stricter kin discrimination mechanisms (e.g. parental infanticide).

Parent–offspring recognition in thick-billed murres (Aves: Alcidae)

Using field experiments, we investigated the development of parent–offspring recognition in the thick-billed murre,Uria lomvia. Cross-fostering experiments (N=73) showed that the likelihood of parents accepting a foreign chick decreased with chick age. Simultaneous-choice playback experiments demonstrated that chicks discriminate between the calls of their parents and both strange and familiar adult conspecifics from as early as 3days old. In presentation experiments with chicks of fledging age (≥14days), adults responded more strongly to the calls of their own chicks than to other familiar chicks from the same breeding ledge. Results are consistent with those of earlier studies of parent–offspring recognition in the congeneric and ecologically similar common murre,U.aalge, which were among the first to suggest that parent birds and their chicks can identify each other's calls.

Offspring recognition by mother crab spiders with extreme maternal care

Maternal care is provided by several spider species, but there are no reports of mother spiders recognizing their young, which suggests that maternal care can be exploited by unrelated individuals. Diaea ergandros , a crab spider with extreme, sacrificial maternal care, does accept unrelated spiderlings ( ca 43.9% of spiderlings) into its nest in areas of high nest density. However, a field and a laboratory experiment with mother spiders and natural and adoptive spiderlings demonstrated that mothers did recognize their own offspring. Recognition was not expressed in survival as adopted (unrelated) spiderlings had similar survival rate to that of natural offspring. Instead it was displayed in growth; mother D. ergandros caught large prey items for their own offspring, but not for adopted spiderlings, and so natural offspring grew more than adopted spiderlings. Also, mothers produced trophic oocytes, which are important for the sacrificial care that influences spiderling survival, only when they lived with their own offspring.

Parent–offspring recognition in tree swallows,Tachycineta bicolor

Parent–offspring recognition appears to be highly developed in species in which the risk of misdirecting care is high (e.g. colonial species). Some of the best evidence for this relationship comes from comparative work on swallows of the family Hirundinidae. Using methods followed in earlier studies, we determined whether parent–offspring recognition occurs in the tree swallow,Tachycineta bicolora non-colonial species closely related to the highly colonial bank swallow,Riparia ripariaand the solitary rough-winged swallow,Stelgidopteryx ruficollisParents did not discriminate between playbacks of the calls of their own versus non-related nestlings. However, older nestlings called more in response to playback of parental calls than non-parental calls, suggesting that they recognized their own parents. Despite significant individual variation in parental and nestling calls, variation in tree swallow nestling calls was lower than analogous calls in the bank swallow. Our results provide further support for a positive relationship between recognition, individual variation in call structure and coloniality.

Olfactory memory and maternal behaviour-induced changes in c-fos and zif/268 mRNA expression in the sheep brain.

In sheep maternal behaviour and the formation of the selective olfactory, ewe/lamb bond are induced by feedback to the brain from stimulation of the vagina and cervix during parturition. In the present study, we have used in situ hybridization histochemistry to quantify changes in cellular expression of two immediately-early genes, c-fos and zif/268, in order to identify activated brain regions during the induction of maternal behaviour and olfactory bonding as well as regions where plastic changes are occurring during with the formation of the olfactory memory associated with bonding. Three different treatment groups were used. One group gave birth normally, became maternal and were allowed to interact with their lambs for 30 min. A second group received exogenous treatment with oestradiol and progesterone to induce lactation and then received a 5-min period of artificial stimulation of the vagina and cervix (VCS) which reliably induces maternal behaviour but could not interact with lambs. A final control group received exogenous hormone treatment but no VCS or interaction with lambs. Compared to the control group, post-partum animals and animals that had received VCS showed increased c-fos expression in a number of cortical regions (cingulate, entorhinal and somatosensory), the mediodorsal thalamic nucleus and the lateral habenula, the limbic system (bed nucleus of the stria terminalis, lateral septum, medial arnygdala, dentate gyrus and the CA3 region of the hippocampus) and the hypothalamus (medial preoptic area, mediobasal hypothalamus, paraventricular nucleus, supraoptic nucleus and periventricular complex). The group that gave birth and had contact with their lambs for 30 min had significantly enhanced c-fos mRNA expression in the cingulate cortex compared to those receiving VCS and additionally showed significantly increased c-fos mRNA expression in olfactory processing regions (olfactory bulb, piriform cortex and orbitofrontal cortex). Expression of zif/268 was significantly increased in the entorhinal cortex, orbitofrontal cortex and dentate gyrus of the parturition group compared to either the control or the VCS alone groups. These results show a clear differentiation between neural substrates controlling the expression of maternal behaviour and those involved in the olfactory memory process associated with selective recognition of offspring although at the level of the hippocampus and cingulate cortex there may be some degree of overlap. Alterations in zif/268 at tertiary processing sites for olfactory information (orbitofrontal cortex) and the entorhinal cortex and dentate gyrus may reflect plastic changes occurring during the early stages of olfactory memory formation.

Olfactory nest recognition by British storm-petrel chicks

Precocial or semi-precocial chicks of underground-nesting seabirds are able to explore the immediate confines of the nest site. Therefore, the development of a cognitive ability that allows chicks of colonial seabirds to return to their own nest during the nestling period may be necessary if contact between young and parents is maintained simply by strong nest-site attachment. In Procellariiformes olfaction may play an important role in navigation of adults to colony sites and nesting burrows. A series of experiments with British storm-petrel,Hydrobates pelagicus, nestlings suggested that they also possess an olfactory homing ability and that they are capable of nest recognition a few days after brooding ceases. As there is apparently no parent–offspring recognition in this species, and adults direct care towards any young that stays in its nest, the ability of chicks to recognize their own nests by smell is likely to be selected for.

Neural Control of Maternal Behaviour and Olfactory Recognition of Offspring

In terms of reproductive success the quality and duration of maternal care exhibited by any particular species is of paramount importance, and yet compared with the amount of research studying the control of reproductive cycles, sexual behaviour, and fertility, it has historically received considerably less attention. However, we are now beginning to understand how the brain is organised to mediate this complex behaviour and how its expression is orchestrated by different hormonal and neurochemical factors. This review summarises a series of neuroanatomical, electrophysiological, in vivo sampling and behavioural neuropharmacological experiments carried out in sheep. These have attempted to define the neural circuitry and hormonal neurotransmitter systems involved both in the control of maternal behavoiur per se and in the selective olfactory recognition of lambs, which is the basis of an exclusive emotional bond between mother and offspring.

Mother–offspring recognition in two Australian lizards, Tiliqua rugosaand Egernia stokesii

Abstract. Kin recognition has been reported in many animal taxa, but rarely in lizards. Newly born clutches from two viviparous Australian skink species, Tiliqua rugosaand Egernia stokesii, were either left with their mothers, separated at birth and kept with a foster mother, or kept completely isolated from any adults. In experimental trials mothers were presented with their own and with non-related young in gauze bags, and their attention to each young lizard was measured by the number of directed tongue flicks and the time in contact. There was a consistent tendency in both species for mothers to direct more attention to their own young, whether they had been kept together or apart. Foster mothers directed more attention to their own non-familiar young than to their familiar foster young. In reciprocal experiments, young lizards of both species consistently directed more attention to their own mothers than to unrelated females, even when they had been isolated from their mothers from birth. Olfactory cues are probably important for recognition. Using these cues, lizards can recognize kin,and discriminate between kin and non-kin even if the latter have been in close association. It wasnot possible to determine if the discrimination was genetically based, or if it was acquired during orshortly after birth. The presence of mother–offspring recognition suggests that family groups maybe a component in the social organization of these species.

Why do male birds not discriminate between their own and extra-pair offspring?

A number of recent models of optimal paternal investment predict that males should alter their investment in offspring in response to changes in paternity or certainty of paternity. One way in which it has been suggested that male birds might do this would be to recognize their own offspring and to discriminate in their favour. Despite frequent statements that nothing is known about whether birds possess this ability or whether they exercise it, there is a considerable body of evidence suggesting that males do not discriminate against non-related offspring. This evidence is reviewed and an attempt made to explain the absence of kin discrimination in males under these circumstances by considering potential mechanisms of kin discrimination. Although there is selection for males to discriminate in favour of their own offspring it is argued that they are unable to do so because of conflicts between the male, female and offspring over signalling identity, and because the circumstances associated with extra-pair paternity disrupt the operation of some mechanisms. Male birds might possess behavioural ‘rules of thumb’ which lead to behaviour that appears similar to offspring recognition, but the sophistication of such rules is likely to be limited by the stochasticity inherent in fertilization.

An Experimental Test of Offspring Recognition in Western Bluebirds

An Experimental Test of Offspring Recognition in Western Bluebirds

Neural and Neurochemical Control of Olfactory Recognition of Offspring in Sheep

In sheep, rapid onset of maternal behaviour occurs at parturition and an exclusive bond between a mother and her lambs is established within a few hours after birth. Parturient ewes discriminate between their own lambs and alien lambs: they allow the former to access and suckle the udder, while they reject suckling attempts from the latter, often violently. Olfactory signals from the lambs are the most important cues in this context. Microdialysis measurement of neurochemical substances in the sheep olfactory bulb (OB) reveals increased release of intrinsic (glutamate (GLU), Y-aminobutyric acid (GABA) and dopamine) and centrifugal (noradrenaline (NA) and acetylcholine) neurotransmitters at parturition. Increased release of these transmitters also occurs after artificial vaginocervical stimulation (VCS), which induces ewes to accept alien lambs. Therefore VCS which takes place at parturition plays a key role in triggering the release of these transmitters in the OB and establishing a selective maternal bond. Rapid changes in effectiveness of VCS on release of neurotransmitters occur after the first experience of parturition in primiparous ewes, suggesting that maternal experience with lambs enhances the establishment of a lamb recognition memory at the time of subsequent parturitions. The formation of maternal olfactory memory depends in part on release of nitric oxide (NO) and NA, because inhibition of NO synthase activity or blockade of β-adrenergic receptors or NA release during labour prevents selective bonding and allows ewes t o accept alien lambs. Following selective bonding, the release of GLU and GABA in the OB increases in response to own lamb odours, but not to alien ones, indicating that the importance of these transmitters for mediating the recall of the olfactory memory. Moreover, blockade of GABAA receptors in the OB overcomes a selective bond with own lambs and induces acceptance of alien lambs.

Recognition of Offspring by Females of the Australian Skink, Tiliqua rugosa

Recognition of Offspring by Females of the Australian Skink, Tiliqua rugosa

Establishment of maternal bonding and its mediation by vaginocervical stimulation in goats

To investigate the establishment of offspring recognition in mother goats, 11 females were subjected to two successive 5-min tests with their own kid and an alien, 2 h 30 min postpartum. All mothers accepted their own kid, while nine rejected the alien. This suggests that in goats, 2.5 h are sufficient for the development of an exclusive bond with the kid. We also studied the role of physiological factors mediating maternal bonding in this species. Eight of the nine goats that rejected alien kids were, therefore, submitted to 5 min of vaginocervical stimulation (VCS) immediately following the selectivity tests. Of these eight goats, five changed their behavior after VCS and accepted the alien kid (0/8 before VCS vs. 5/8 after VCS, p = 0.031). Thus, VCS appears to reduce rejection behavior towards alien kids while resulting in a significant increase in their rate of acceptance. Underlying physiological mechanisms by which VCS may act are discussed.

Développement et sélectivité du lien mère-jeune chez la chèvre et la brebis

The olfactory recognition of the young in ungulates results in a selective maternal behaviour, which is characterized by the exclusive suckling of the litter by the mother, and her refusal to suckle alien young, sometimes accompanied by aggressive behaviour. For ewes, exclusive suckling of the young depends on the recognition of their individual odour by selective learning. Familiarization of the ewe to the odour of her lamb(s) during the initial two to four hours after birth is sufficient for her to distinguish them from aliens. No influence of a maternal labelling of the young, especially through colostrum, has been found in this species. On the contrary, it was thought for a long time that goat kids were labelled with the odour of their mother through her saliva and absorption of colostrum. Moreover, the mother would reject any alien kid labelled by another mother goat, but would accept aliens unlabelled or labelled by herself. Such labelling was believed to develop in about twenty-four hours. However, recent results from our laboratory suggest that the development of selectivity in goats is similar to that of sheep. Moreover, the possibility that a « family odour » might exist in these two species, which are intermediate between monotoccous (e.g. horses) and polytoccous species (e.g. pigs), has remained largely unexplored. Litters of twins or even triplets are indeed frequent in both goats and sheep. Our initial results suggest that in both species some mothers are able to recognize the individual odours of the young from a same litter. Thus, similarities in the mechanisms involved in offspring recognition exist between both species, despite differing characteristics of mother-young relationships during the first days following parturition (sheep being «followers » and goats « hiders »). These results and their possible validity for wild ungulates are discussed in relation to the data available for other species.

Recognition and Parental Investment in Adélie Penguins

Discrimination abilities of Adelie Penguins Pygoscelis adeliae were studied by cross-fostering eggs within two days of laying, chicks within five days of hatching, chicks 11-15 days of age and chicks 17-21 days of age. Our results show that Adelie Penguins have no innate mechanism for recognition of offspring. Discrimination by adults was apparent only after 17-21 days of post-hatching familiarity, which corresponded with the end of the guard stage. By contrast, chicks may have learnt to discriminate adults by 11-15 days of age. During the guard stage, within-brood food allocation by parents was determined by sibling competition.

Microdialysis measurement of oxytocin, aspartate, γ-aminobutyric acid and glutamate release from the olfactory bulb of the sheep during vaginocervical stimulation

Concentrations of oxytocin and amino acids were measured in microdialysis samples taken from the olfactory bulbs of 5 conscious, oestrogen-treated ewes before, during and after a 10-min period of vaginocervical stimulation. Results showed that vaginocervical stimulation induced significant increases in concentrations of oxytocin, aspartate, γ-aminobutyric acid3(GABA) and glutamate in dialysis samples. Concentrations of other amino acids measured were not affected. These findings show that vaginocervical stimulation produces significant changes in neurochemical release in the olfactory bulbs of sheep. Such changes may be involved in the induction of maternal behaviour or the olfactory recognition of offspring.

Timing of Offspring Recognition in Adult Starlings

1. In the Exchange experiments adult starlings feed a strange brood, introduced at their original nest site up to 16 days post hatch, as frequent as their own young, resulting in a normal weight gain of the strange young. 2. Confronted with a 19 day old alien brood and their own young simultaneously, some adults still occasionally feed the strange young while others are already able to restrict their parental care to their own offspring. 3. Not until the young are aged 20 days or more, the adults arc definitely able to discriminate between own and alien young in the immediate vicinity of the original nesting hole (Choice experiments) or within 10 to 20 m (Search experiments). 4. The experiments altogether show that offspring recognition in Starlings develops only a few days prior to fledging, i.e. by the time the young run the risk of intermingling with other conspecific broods.

Parental Care and Social Interactions of Captive Plateau Mice, Peromyscus melanophrys

Parent-offspring interactions and staged dyadic encounters between weanlings and conspecifics of the plateau mouse, Peromyscus melanophrys , were observed in laboratory experiments. Mothers provided most of the parental care, spending nearly 90% of their time with the young in the nest over the 2 weeks following parturition. There was a lack of male involvement in paternal care which is in contrast to other studies that have shown male Peromyscus to take an active role in parental care. Strange females were more aggressive than strange males toward weanlings. Mothers were more aggressive than fathers toward weanlings, and this asymmetry may be a result of the brief encounter the father had with his young on day 1. Additionally, the father's temporary presence in the natal nest may be associated with the acquisition of offspring recognition. The evidence suggests Peromyscus melanophrys has a polygynous mating system.