Eberhard Curio

The functional organization of anti-predator behaviour in the pied flycatcher: A study of avian visual perception ☆

1. 1. The pied flycatcher (Ficedula hypoleuca Pallas), a palaearctic songbird, is endangered in its breeding grounds by a number of highly diverse predators and, on occasion, by several avian nest competitors. The ecological impact of the various dangers upon the adult P.F. and/or its brood is broadly assessed and the defence methods described. 2. 2. In order to elucidate part of the stimuli which elicit two distinct anti-predator responses, mobbing and snarling attacks, enemy dummies were presented to over 2200 territorial subjects in the course of 12 years, utilizing three German populations (Berlin, Hessen, Brunswick) and one in Spain (La Granja). Comparison with mobbing responses to the live enemy give confidence in the dummy experiment as a suitable and valid method of approach. 3. 3. Mobbing movements and calls together with their characteristic interrelationships are described as a function of response strength RS. Phenomena as diverse as warming-up, after-response, and short-term fluctuations of the calling rate, all of which are a function of RS, can be causally explained by a unifying concept called ‘catch’. 4. 4. A number of external and internal factors tend to increase or diminish mobbing responsiveness. Opportunity to see live redbacked shrikes (= redbacks) (Lanius collurio) neither detectably affected the response to shrikes nor to incomplete shrike patterns. Subjects when tested repeatedly with the same dummy stimulus tend to remain significantly at the same RS level. RS data from parents and their offspring are presented, the proper evaluation of which in terms of heritability has suffered so far from lack of suitable statistics. Evidence for spontaneity of mobbing derives from vacuum alarms of both wild and captive, hand-raised birds. 5. 5. Three similar-sized enemies, e.g. pigmy owl (Glaucidium passerinum), male redback, and great spotted woodpecker (Dendrocopus major) are recognized by various sign stimuli, the physical complexity and/or the degree of interaction of which increase(s) in that order. Interaction follows the principle of ‘stimulus dilation’ both in terms of RS as well as of the underlying aroused motivation M. The latter conclusion is permitted through the derivation of the functional relationship RS = f(M). Two simple formalisms are proposed that can account for ‘weighted summation’ of sign stimuli with stimulus dilation being a special case. 6. 6. Novelty can be dismissed as an explanation for the high-intensity mobbing of shrikes and owls. However, novel bird-shaped models of about shrike-size do elicit some alarm when properly oriented and minimally patterned, suggesting a new version of the ‘rarity principle’ of danger recognition. Recognition of the perched predator is at the same time specific enough not to be mistaken by harmless bird species resembling either enemy, and sufficiently unspecific as to cope with at least two shrike and several owl species. 7. 7. A varying fraction out of eighty-eight hand-raised, predator-naive birds responded, though somewhat sub-normally, when tested from 5 weeks up to nearly 3 years of age to live owls and shrikes. Live, novel control birds released some mobbing typical for them from yearling birds, but not at 8 weeks of age. It is concluded that recognition of owls, shrikes, and novel birds is innate (as defined here, see C.2.2). Whether predator-unrelated, ‘subsidiary’ experiental factors would contribute to the response predictability of birds growing up normally is doubtful as suggested by RS levels of hand-raised as compared to wild-caught subjects familiarized with captivity. The innate nature of recognition accords well with a number of observations, among which the wholesale failure to condition, by five different methods, and mobbing in both wild and captive birds to neutral and novel stimuli is the most conspicuous. 8. 8. The hypothesis of at least two perceptual channels decoding either owls or shrikes and subserving a common response mechanism received strong support from five pieces of evidence: (a) Sign stimuli of both predators do not effectively combine thus explaining at the same time the low releasing value of the redback female, (b) An identical change of both predators leads to a different effect in each case, (c) Habituation of the response to the shrike neither affects the response to the owl, nor does the latter lead to dishabituation. (d) The owl response is capable of raising the stimulus value of an otherwise ineffective owl model but not that of an otherwise ineffective shrike (or novel bird) model, (e) Factors associated with a foreign territory abolish almost entirely the response to shrikes (and novel birds), but not the owl response. Differential evaluation of identical sign stimuli, a range of distinctly different (low) releasing values, and, presumably, the susceptibility to habituation leads one to invoke a third channel in its own right that is tuned to novel birds. The functional independence of the three channels envisaged is underlined by the lack of intra-individual correlation of responses to two classes of objects. 9. 9. The adaptiveness of nest defence strategies in general is derived from the compromise achieved between protection of the brood and that of the defending adults. Owl-shrike recognition in particular is not only currently maintained but also has arisen by the pressures from owls and shrikes as evidenced by the precise fit between (a) stimulus configuration and corresponding IRM, and (b) perceptual capabilities and the geographical distribution of both enemies. In order to elucidate the way in which these exert selection pressure a more direct approach to the problem of survival value is needed. 10. 10. In an attempt at a synthesis, a coherent scheme is proposed which accounts for the results of both stimulus and response analysis. Its most prominent features are distinct though non-unitary, danger-specific perceptual channels which converge before or at the adaptively appropriate common response mechanism M. It is argued that not only recognition of at least several danger stimuli is innate (para. 7), but also the multi-channel organization of recognition itself. Factors that are apt to modify RS with the stimulus remaining constant (para. 4) either affect the channel activated or M (plus that channel?). The nature of the channels and evolutionary implications considering the ecological diversity of the impact by predators upon perceptual mechanisms of the prey are discussed. Finally, the maintenance of the IRM concept is advocated if used as a shorthand description of a rigorously defined stimulus-response correspondence and the operations performed to establish it.

Conservation needs ethologv

With the number of species and near-to-natural habitats rapidly dwindling, conservation has become an undebatable necessity. There have been some laudable, successful species conservation projects but there have also been many deplorable failures. The failures are exacerbated by limited funding. Conservationists depend on funding by national government organizations (NG0s) and by private sponsors, more than other practitioners of organismic biology do. To maximize their success, conservationists would be well advised to heed the messages resulting from animal behaviour study (i.e. ethology) and/or to involve ethologists in their projects. Here, I illustrate how ethology can benefit both in situ and ex situ conservation measures; the need for conservation-oriented behaviour research is paramount.

Determinants of brood defence in the great tit Parus major L.

SummaryGreat tits (Parus major) tending nestlings reacted defensively to a live predator (Glaucidium perlatum; domestic cat) and the playback of a mixed species mobbing chorus, or to the latter alone. Defensive behaviour, mainly mobbing, reflected the risk taken and is assessed by five measures. Multivariate and contingency analyses revealed that at least 11 of 16 contextual independent variables affected the risk taken. Incremental effects are due to: Age of young, sex of the defending bird, the expected number of neighbouring mobbers, low temperature, wet canopy, the raptors distance from cover, coniferous forest, advancing season. A decremental effect is exerted by a large brood that is older. Annual differences in defence arise probably from demographic factors such as fecundity, which in turn affect the parents benefit-cost ratio (number of young of the same sex as the parent/residual reproductive value of the parent).While the effects of annual fecundity, age of young and season were predicted on the basis of this benefit-cost ratio, the failure to verify an incremental effect of brood size runs counter to established theory. We conclude that parents gear their defence efforts to energy investment, past or future, and are mal-adapted to brood size as a promotor of risk taken. The influence of the habitat is poorly understood. At least three factors (age and number of young, parents sex) act additively on part of the response. Despite the large number of variables examined, about 43% of the total response variance remains unexplained.While four defence measures are determined by at least 10 contextual factors, a fifth measure, the males minimum distance from the raptor, is determined by one other factor, the appearance of the ♀ male. The latter leads us to assume an additional, social rôle of brood defence.Risk-assessment by great tits leading to risk-aversive defence behaviour is governed by evolved restraints rather than by momentary constraints. Examples are provided by the effects of weather and cover.

Towards a methodology of teleonomy.

Das einzige für die Biologie kennzeichnende Problem der Anpassung von Organismen an ihre Umwelt hat nicht die Bearbeitung erfahren, die es verdient hätte. Als einer der Hauptgründe für diese Lage wird das Fehlen einer formalisierten Methodenlehre für die naturwissenschaftliche Erforschung von Anpassungen, die Teleonomie, angesehen. Nach kurzer Streifung begrifflicher und ihrer Erforschung nach noch offenen Grundfragen, z. B. dem Ökonomieprinzip, wird ein methodischer Ansatz vorgelegt, mit dem Anpassungen entdeckt und ihrer Entstehung nach erforscht werden können. Die teleonomen Methoden umfassen 1. Das Aufsuchen von Korrelationen zwischen untersuchter Eigenschaft und Umwelt, die wie üblich weit oder aber eng, innerhalb der Grenzen des Organismus gefasst sein kann. Die notorische Vieldeutigkeit solcher Korrelationen macht einer Deutung als Ursache-Wirkungs-Beziehung zwischen der Selektion und der von ihr geformten Eigenschaft dort Platz, wo sichergestellt werden kann, dass nur ein Selektionsdruck am Werke ist. 2. Die Veränderung einer Eigenschaft und die daran anschliessende Prüfung auf verschiedenen Fortpflanzungserfolg bei so veränderten und unverändert gebliebenen Gliedern einer Art. Verhaltensweisen, die sich im Experiment oft als unveränderbar erweisen, können auf ihre Funktion hin untersucht werden, indem man ihre Wirkung auf die Umwelt verändert und entsprechend den Fortpflanzungserfolg der betroffenen Individuen miteinander vergleicht 3. Mit Hilfe von Varianten einer Art unter gleichen Selektionsbedingungen kann der Selektionswert einer Eigenschaft quantitativ ermittelt werden. In einem Anhang wird versucht, einige der häufigsten Irrtümer und Missverständnisse klarzustellen, die auch heute noch einer erfolgreichen Teleonomie entgegenstehen.

The hearing of an avian predator and its avian prey

SummaryAuditory tuning curves of a small songbird, the great tit (Parus major), and of its principal avian predator, the European sparrowhawk (Accipiter nisus), were determined by an operant positive reinforcement conditioning procedure, using the method of constant stimuli. Thresholds were measured by the criterion of a 50% correct response and a d′ of 1.5 for intra- and interspecific comparison, respectively. The best frequency of both species was 2 kHz, the hawk being 6.5 dB SPL more sensitive than the tit. Although the high-frequency cutoff was very similar in both species, at 8 kHz the great tit was about 30 dB more sensitive than the sparrowhawk. The hearing abilities of the prey and its predator are discussed with reference to the acoustic alarm communication of great tits confronted with sparrowhawks. Two alarm calls lie in the frequency range of the best hearing of both the hawk and the tits: the mobbing call and a call given in response to a nearby hawk when fleeing from it. In contrast, the “seeet” call, an alarm call given mainly in response to distant flying sparrowhawks, can only be heard well by the tit. The implications of these results for hypotheses concerning the evolution of alarm calls in small songbirds are discussed.

An anti predator response in the great tit parus major is it tuned to predator risk

SummaryTwo semi-quantitative predictions about the intensity of defence against a predator based on the associated costs and benefits as a function of predator species, were examined in great tits (Parus major) feeding nestlings. One premise was that defence behaviour is adaptive. Defence comprised of vocalizing and homing in on a live raptor near the nest hole. The intensity of defence as judged by two measures of approaching (Minimum Distance, Average Distance) varies with the species of raptor, i.e. sparrowhawk ♀ (Accipiter nisus), pigmy owl (Glaucidium perlatum), and tawny owl (Strix aluco). With the exception of the response to the pigmy owl, defence intensities proved to conform to both predictions; the tits correctly assessed the relative overall risk from each predator (“predator pressure”) i.e. its degree of specialization on great tits, and the immediate risk of defence. The failure to verify the predictions regarding the pigmy owl is thought to derive from our incomplete assessment of the cost function and/or from the response being mal-adaptive.The male takes a greater risk, exceeding the females by an amount independent of the species of raptor. The sexual difference remains functionally unexplained.

The adaptive significance of avian mobbing. III. Cultural transmission of enemy recognition in blackbirds: Cross-species tutoring and properties of learning

Abstract Taped conspecific and alien species mobbing calls suffice to transmit enemy recognition of a conditioned object CS to European blackbirds ( Turdus merula ), though their reinforcing effect is probably less than that of a real blackbird mobber. Blackbirds habituated to the CS learn to mob it in the latter case without impairment, but fail completely if taped conspecific mobbing calls serve as the reinforcer. Mobbing performance of the learner during learning peaks significantly later with a weak CS than with a strong CS. A general mobbing motivation, as measured by mobbing performance over many episodes, is typical for each individual: i.e. responses correlate intra-individually over a wide range of different compound stimuli. A more specific motivation accompanying enemy stimulus learning weakens these inter-response relationships and enhances performance of the learned response; the learned response correlates more strongly with the response during learning than with any other preceding response. This suggests that a specific motivation during engram formation has reinforcing properties. As revealed by multiple regression analysis, all three mobbing elements scored exert their learning-enhancing effect by a strictly intra-element facilitation.

The use of olfaction in the foraging behaviour of the golden-mantled flying fox, Pteropus pumilus, and the greater musky fruit bat, Ptenochirus jagori (Megachiroptera: Pteropodidae).

Double-choice experiments with three adult males of the little golden-mantled flying fox, Pteropus pumilus, and ten adult greater musky fruit bats, Ptenochirus jagori (both Megachiroptera: Pteropodidae), demonstrate that they are able to discriminate accurately between an empty dish and a dish containing fruits of one of several species by odour alone. Tests were run using fruits of six fruit species for Pteropus pumilus and five fruit species for Ptenochirus jagori. The fruit species used are known to be consumed in the wild by Ptenochirus jagori and are, with two exceptions, species of the natural rain-forest habitat. This is the first study to show that fruit bats are also able to assess the ripeness of a fruit exclusively by its odour. The bats preferred ripe over unripe fruits of the same species. Thus, both Pteropus pumilus and Ptenochirus jagori can not only locate fruits by their odour but can also discriminate between ripe and unripe fruits of the same species by olfaction. The results confirm and expand earlier findings on the role of olfactory cues in the orientation of foraging pteropodids.

Brood defense and age of young: a test of the vulnerability hypothesis

SummaryIn many altricial species including the great tit (Parus major) the intensity of brood defense against predators has been shown to increase with the age of the offspring. This effect has been ascribed amongst others to the young becoming more vulnerable as they age (“vulnerability hypothesis”). In a great tit population suffering heavy losses from brood depredation by the great spotted woodpecker (Dendrocopus major), we rendered first and second broods more vulnerable by artificially enlarging the entrance of the nest hole. Contrary to the vulnerability hypothesis, 16 experimental pairs defended their brood against a dummy great spotted woodpecker less vigorously than did 16 control pairs. Nest concealment behavior potentially compromising active defense was minimized by simultaneous playback of nestling distress calls, thus simulating the act of nest predation. This leaves the “brood value hypothesis” as an alternative functional explanation of the defense level — age effect. It predicts that parents should defend their brood in proportion to the “reproductive value” (or some more suitable cohortal equivalent measure) of their offspring. At present, this explanation pertains to one predator species. In first broods, but not in second broods, males defended them more vigorously than did their females. While this parallels previous experiments on brood defense against predators posing a much greater risk to the parents, two functional explanations previously put forward can hardly apply.

The great tit's (Parus major) auditory resolution in azimuth

Summary1.Two male great tits (Parus major) were trained to distinguish between sounds from two locations in an operant two alternative, forced choice procedure with positive reinforcement.2.The angle between the two sound sources, as experienced from the position of the experimental subject, was varied. The angle at which the birds scored 65% correct responses in 60 choices (which corresponds toP = 0.03, two-tailed, binomial test) was defined as the minimum resolvable angle (MRA).3.The resolution in azimuth for four natural vocalizations, the ‘seeet’ alarm call, the ‘scolding’ call, the mobbing call, and a song element, was 45°, 16°, 20°, and 18°, respectively (Fig. 2). The MRAs correlated well with the results from artificial stimuli with a comparable frequency.4.MRAs for 300 ms sine wave stimuli were determined from 500 Hz to 8 kHz: The u-shaped function relating MRA with frequency had a minimum at 2 kHz, with a best MRA of 20°. At 500 Hz and 8 kHz the MRAs were 66.5° and 52°, respectively. MRA of a 300 ms white noise stimulus was 20.5° (Fig. 3).5.The duration of the stimulus had no effect on the resolution in azimuth for a range of durations from 40 ms to 300 ms (Table 1). This suggests that the great tit may locate a sound source in an open loop fashion.