Tomas Redondo

Avian Nest Defence: Theoretical Models and Evidence

Functional explanations for variations in levels of avian nest defence have been often based upon assumptions concerning optimal allocation of reproductive effort. Such a theoretical framework has led to the formulation of mathematical models aimed at predicting patterns of nest defence in the field. Here, a model is proposed that, starting from a general theoretical standpoint about optimal parental care, integrates previous models and generates new predictions concerning variables not previously included, namely predatory risk for both parents and offspring and age-dependent defensive tactics of nestlings. Optimal levels of parental defence are then expected to increase with (1) parent-offspring relatedness, (2) brood size, (3) offspring quality, (4) potential risk for the offspring, (5) offspring age, and (6) enhancement of offsprings self-defensive tactics while (7) parental residual reproductive value and (8) potential risk for parents are expected to exert a negative effect upon optimal levels of defence. Empirical data are reviewed for testing the models predictions. Available data provide strong support for predictions concerning parameters 4, 5, 6, and 8. Failed tests concerning parameters 2 and 3 are shown to be flawed in the sense that we should expect defence levels to reflect intra-, instead of inter-individual variations in size and quality of the brood. A more detailed analysis is made concerning variations in residual reproductive value-correlated traits, such as brood number or time in the breeding season. It is argued that, when dealing with such traits, severe violations of basic assumptions (i.e. coeteris paribus statements or absence of an actual correlation between such traits and residual reproductive value) can occur, leading to unexpected results. It is concluded that life-history theory can account for most of the variability observed in nest defence patterns.

FREQUENT COPULATIONS DESPITE LOW SPERM COMPETITION IN WHITE STORKS (CICONIA CICONIA)

White Storks Ciconia ciconia paired for ca. 30 days before laying a clutch. During this period, mates copulated frequently (160 copulations/pair; 0.4 copulations/daylight h), but copulation rate was drastically reduced a week before laying of the eggs. Both fewer copulation attempts by males and lower female receptivity accounted for this reduction. This pattern was the same regardless of whether pairs nested solitarily or in colonies. Colonial as well as solitary males spent more time at the nest before egg-laying while the opposite trend was found for females. Consequently, females were more likely to remain alone at their nests while ovulating. Colonial birds had ample opportunities for engaging in extra-pair copulations (EPC) during the female fertile period, but these were very infrequent (0.4% of all successful copulations) and involved recently-paired birds exclusively. This suggests that sperm competition in this species is of little relevance for explaining patterns of pair copulations. Accordingly, males did not guard their female mate and the timing of copulation was poorly tuned to chances of fertilizing the females eggs. However, it remains to be explained why storks copulated so much and for a prolonged period when the risk of EPC was so low. It is suggested that copulations may be part of a signalling system by which males advertise and females assess the physical condition of the male, which is likely to correlate with the ability of males to forage efficiently for them and their offspring. In support of this possibility, males who copulated frequently fed chicks at a higher rate during the nestling period.

Begging at high level simultaneously impairs growth and immune response in southern shrike (Lanius meridionalis) nestlings

Theoretical models suggest that begging should be costly in order to be evolutionarily stable. However, evidence for such a cost is contradictory (e.g. for growth costs) or scant (e.g. for immunological costs). Here, we experimentally test the existence of both costs in southern shrike (Lanius meridionalis) nestlings. Nestlings were paired by nest of origin and similar body mass. In each pair, a nestling was forced to beg for about 30 s h−1, whereas the other begged for only 2 s, both nestlings receiving the same quantity of food. At the same time, the nestling response to an antigen (phytohaemagglutinin) was measured. Nestlings forced to beg for longer showed a reduction in growth rate and in immunocompetence when compared to control chicks. The two costs occurred independently of each other and were negatively correlated to time begging. These results strongly support models of honest signalling as well as scramble competition, which predict that begging should be costly in order to be evolutionarily stable.

Oxidative Stress Mediates Physiological Costs of Begging in Magpie (Pica pica) Nestlings

Background Theoretical models predict that a cost is necessary to guarantee honesty in begging displays given by offspring to solicit food from their parents. There is evidence for begging costs in the form of a reduced growth rate and immunocompetence. Moreover, begging implies vigorous physical activity and attentiveness, which should increase metabolism and thus the releasing of pro-oxidant substances. Consequently, we predict that soliciting offspring incur a cost in terms of oxidative stress, and growth rate and immune response (processes that generate pro-oxidants substances) are reduced in order to maintain oxidative balance. Methodology/Principal Findings We test whether magpie (Pica pica) nestlings incur a cost in terms of oxidative stress when experimentally forced to beg intensively, and whether oxidative balance is maintained by reducing growth rate and immune response. Our results show that begging provokes oxidative stress, and that nestlings begging for longer bouts reduce growth and immune response, thereby maintaining their oxidative status. Conclusions/Significance These findings help explaining the physiological link between begging and its associated growth and immunocompetence costs, which seems to be mediated by oxidative stress. Our study is a unique example of the complex relationships between the intensity of a communicative display (begging), oxidative stress, and life-history traits directly linked to viability.

Dishonest begging and host manipulation by Clamator cuckoos

Brood parasites may be favoured over host nestlings due to variation in the honesty of their begging signals. Begging behaviour of great spotted cuckoo nestlings and their host magpie nestlings was recorded when controlling food need. Cuckoo begging effort was dishonest as an indicator of nutritional need, whilst magpie begging was not. Cuckoos begged for longer and emitted more calls at a higher rate irrespective of the degree of food deprivation, although in contrast to magpies, cuckoos ate food in relation to their need. Energetic and predation costs are unlikely to account for these differences. Differences in indirect inclusive fitness costs can explain the more intensive begging by cuckoos. Magpie parents given a choice favoured larger nestlings and those begging more intensively. Cuckoos obtained more food and a larger share than magpies of a similar size. Magpies therefore received less food in the presence of a cuckoo, and cuckoos received a similar share irrespective of their size. Lack of relatedness to their magpie hosts therefore allows cuckoos to exploit a set of adaptive rules in the host parents and manipulate them into providing the latter with preferential care.

Early stages of vocal ontogeny in the magpie (Pica pica)

The vocal repertoire of magpie (Pica pica) chicks consists of six calls: Begging Trill (BT), Soft Whistle (SW), Begging Scream (BS), Alarm Call (AC), Distress Call (DC) and Brief Contact Note (BCN). Both BT and SW have a tonal structure and their occurrence is restricted to the nestling period. At fledging, there is a gradual change from BT into BS and a sudden appearance of harsh calls similar to those of adult birds (AC, DC, BCN), without evident transitional forms with preceding tonal calls. Both the existence and the structural design of calls seem to be adapted for providing nestlings with immediate benefits linked to the two major chapters of allocation of parental care. Emission rates of BT increase with hunger motivation under laboratory conditions. Their structure suggests that they are easily located but liable to suffer from environmental degradation. BS of fledglings may be more resistant to degradation, a trait which may facilitate the identification by parents of their own offspring. Both AC and DC attract parents to defend the nest against potential predators, and their structure make them to be easily located and detectable at long distances. BCN are given by fledglings during bouts of locomotory activity (exploration and play) and they probably help in maintaining the cohesion of the group under conditions of poor visibility. In accordance, this call may be fairly located at short distances. The function of SW was unclear. It is given during periods of nestling inactivity between begging bouts, and could be easily elicited by tactile and auditory stimuli. After laboratory experiments, it is concluded that SW serve to indicate parents that nestlings are in good condition, hence to benefit from the parental willingness to invest in a brood with high prospects of survival. Since (i) there is a widespread lack of continuity in the development of adult vocalizations starting from nestling calls, and (ii) nestling calls seem to have evolved to provide birds with benefits in the short-term, these facts argue against the prevailing idea that the main function of calls early in ontogeny is to act as precursors of adult vocalizations. Das Lautrepertoire von Elsternestlingen besteht aus 6 Lautäußerungen: Betteltrillern (BT), Sanftes Pfeifen (SP), Bettelkreischen (BK), Alarmruf (AR), Angstschreien (AS) und kurzer Kontaktruf (KR). BT und SP sind tonal und treten nur während der Nestlingsperiode auf. Zum Zeitpunkt des Ausfliegens geht BT graduell in BK über und plötzlich treten auch ohne vorausgehende tonale Übergangsformen rauhe Rufe ähnlich denen der Altvögel auf (AR, AS, KR). Sowohl die Existenz als auch die Struktur der Lautäußerungen scheinen als Anpassungen im Zusammenhang mit einer Optimierung der Brutpflege zu interpretieren zu sein. Die Emissionsrate von BT steigt unter Laborbedingungen mit der Hungermotivation. Die Struktur legt nahe, daß BT leicht geortet werden kann, aber auch leicht von der Umgebung verschluckt wird. BS der flüggen Jungen scheint davon weniger betroffen zu sein, so daß die Eltern leichter ihre Jungen identifizieren können. AR und AS veranlassen die Altvögel, ihr Nest gegenüber potentiellen Prädatoren zu verteidigen; die Struktur der Laute begünstigt ihre Ortung und Wahrnehmung über größere Entfernungen. KR werden von den flüggen Jungen bei lebhafter lokomotorischer Aktivität (Exploration, Spiel) geäußert; sie tragen vielleicht dazu bei, die Gruppe auch unter erschwerten optischen Kontaktmöglichkeiten zusammenzuhalten. Die Funktion von SP blieb unklar. SP war während inaktiver Perioden zwischen Bettelverhalten zu hören und konnte leicht durch taktile und akustische Reize ausgelöst werden. Nach Laborexperimenten ist zu schließen, daß SP den Eltern „Wohlbefinden” der Jungen anzeigt und so Bereitschaft zur Investition in eine Brut mit hoher Überlebenswahrscheinlichkeit fördert. Daß (1) zwischen den Rufen der Altvögel und dem Repertoire der Nestlingen weitgehend keine kontinuierlichen Übergänge festzustellen und (2) Nestlingsrufe offensichtlich im Hinblick auf kuzfristige Gewinne zu interpretieren sind, spricht gegen die allgemein vorherrschende Ansicht, das Lautrepertoire in frühen Stadien der Ontogenie sei hauptsächlich ein Vorläufer der Adultlaute.

Benefits of Extra Begging Fail to Compensate for Immunological Costs in Southern Shrike (Lanius meridionalis) Nestlings

Theoretical models aimed at explaining the evolution of honest, informative begging signals employed by nestling birds to solicit food from their parents, require that dishonest signalers incur a net viability cost in order to prevent runaway escalation of signal intensity over evolutionary time. Previous attempts to determine such a cost empirically have identified two candidate physiological costs associated with exaggerated begging: a growth and an immunological cost. However, they failed to take into account the fact that those costs are potentially offset by the fact that nestlings that invest more in begging are also likely to obtain more food. In this study, we test experimentally whether a 25% increase in ingested food compensates for growth and immunological costs of extra begging in southern shrike (Lanius meridionalis) nestlings. Three nestmates matched by size were given three treatments: low begging, high begging-same food intake, and high begging-extra food intake. We found that, while a higher food intake did effectively compensate for the growth cost, it failed to compensate for the immunological cost, measured as T-cell mediated immune response against an innocuous mitogen. Thus, we show for the first time that escalated begging has an associated physiological net cost likely to affect nestling survival negatively.

Manipulative begging by parasitic cuckoo nestlings and paradoxical host behaviour.

I am grateful to Fernando Alvarez, Juan Amat, Arnon Lotem, Miguel Rodriguez-Girones and Jesus Zuniga for many helpful criticisms, and to Nick Davies and David Noble for trusting my intuitions too.