Compound tool construction by New Caledonian crows.

The construction of novel compound tools through assemblage of otherwise non-functional elements involves anticipation of the affordances of the tools to be built. Except for few observations in captive great apes, compound tool construction is unknown outside humans, and tool innovation appears late in human ontogeny. We report that habitually tool-using New Caledonian crows (Corvus moneduloides) can combine objects to construct novel compound tools. We presented 8 naïve crows with combinable elements too short to retrieve food targets. Four crows spontaneously combined elements to make functional tools, and did so conditionally on the position of food. One of them made 3- and 4-piece tools when required. In humans, individual innovation in compound tool construction is often claimed to be evolutionarily and mechanistically related to planning, complex task coordination, executive control, and even language. Our results are not accountable by direct reinforcement learning but corroborate that these crows possess highly flexible abilities that allow them to solve novel problems rapidly. The underlying cognitive processes however remain opaque for now. They probably include the species' typical propensity to use tools, their ability to judge affordances that make some objects usable as tools, and an ability to innovate perhaps through virtual, cognitive simulations.

Social transmission of tool use and tool manufacture in Goffin cockatoos (Cacatua goffini).

Tool use can be inherited, or acquired as an individual innovation or by social transmission. Having previously reported individual innovative tool use and manufacture by a Goffin cockatoo, we used the innovator (Figaro, a male) as a demonstrator to investigate social transmission. Twelve Goffins saw either demonstrations by Figaro, or 'ghost' controls where tools and/or food were manipulated using magnets. Subjects observing demonstrations showed greater tool-related performance than ghost controls, with all three males in this group (but not the three females) acquiring tool-using competence. Two of these three males further acquired tool-manufacturing competence. As the actions of successful observers differed from those of the demonstrator, result emulation rather than high-fidelity imitation is the most plausible transmission mechanism.

State-dependent valuation learning in fish: banded tetras prefer stimuli associated with greater past deprivation.

Humans and some birds and insects sometimes prefer alternatives associated with greater past cost or need, sometimes affording losses. It has been proposed that this is widespread because learning may include knowledge about both the physical properties of alternatives and state-dependent fitness gains. We examine the phenomenon for the first time in a fish, the banded tetra (Astyanax fasciatus). During training we paired two different color cues to identical food rewards, one under greater deprivation than the other. We then tested preference between these cues under both deprivation states. Consistent with previous results in other taxa, the fish preferred the cue associated with previous greater deprivation regardless of the condition under which they were tested. These results provide further support to the view that organisms assign value using state-dependent increments in fitness during learning. Although generally adaptive, under experimental conditions state-dependent valuation learning can lead to paradoxical choices.

Interval timing in mice does not rely upon the circadian pacemaker.

The suprachiasmatic nucleus (SCN) of the hypothalamus is a precise timekeeper that controls and synchronizes the circadian period of countless physiological and behavioural functions and entrains them to the 24 h light/dark cycle. We examined the possibility that it is also indirectly involved in measurement of a briefer interval by observing the effects of lesions targeted at the SCN, and abolishing circadian rhythmicity, upon interval timing behaviour. Fourteen house mice (Mus musculus) were trained to estimate a 10 s interval using a modified peak procedure, and then underwent electrolytic lesions. Six individuals became behaviourally arrhythmic. Peak interval performance was then assessed in 12:12 light/dark conditions and in constant darkness. No significant change in peak characteristics was observed as a consequence of the lesion for either rhythmic or arrhythmic groups. These results show that the accurate measurement of 10 s requires neither a functioning circadian pacemaker nor entrained behavioural rhythmicity.

Relative importance of perceptual and mnemonic variance in human temporal bisection.

We investigated the relative contributions of perception and reference memory to behavioural variability in a temporal discrimination with human subjects. We used two temporal bisection tasks. In both tasks each trial consisted of a sequential presentation of three intervals, two standards, and a probe, and subjects were asked to judge the similarity of each probe against the two standards. In a "single bisection", the standards' duration was constant across trials. In a "roving bisection", the two standards were trial unique. We compared our results with the predictions from a model related to Scalar Expectancy Theory, with the added assumption that the decision process minimizes the expected number of errors given the information available. The model shows that if errors in reference memory were dominant the psychometric function should be identical for single and roving tasks, and if perceptual errors were dominant the psychometric function should be steeper for the single than for the roving bisection. As we found that psychometric functions were steeper for the single than for the roving tasks, we concluded that perceptual errors are dominant.

To walk or to fly? How birds choose among foraging modes.

We test the predictive value of the main energetic currencies used in foraging theory using starlings that choose between two foraging modes (walking versus flying). Walking is low-cost, low-yield, whereas flying is the opposite. We fixed experimentally, at 11 different values, the amount of flight required to get one food reward, and for each flight cost value, we titrated the amount of walking until the birds showed indifference between foraging modes. We then compared the indifference points to those predicted by gross rate of gain over time, net rate of gain over time, and the ratio of gain to expenditure (efficiency). The results for the choice between modes show strong qualitative and quantitative support for net rate of gain over time over the alternatives. However, the birds foraged for only a fraction of the available time, indicating that the choice between foraging and resting could not be explained by any of these currencies. We suggest that this discrepancy could be accounted for functionally because nonenergetic factors such as predation risk may differ between resting and foraging in any mode but may not differ much between foraging modes, hence releasing the choice between foraging modes from the influence of such factors. Alternatively, the discrepancy may be attributable to the use of predictable (rather than stochastic) ratios of effort per prey in our experiment, and it may thus be better understood with mechanistic rather than functional arguments.

Foraging rate versus sociality in the starling Sturnus vulgaris.

It is well established that social conditions often modify foraging behaviour, but the theoretical interpretation of the changes produced is not straightforward. Changes may be due to alterations of the foraging currency (the mathematical expression that behaviour maximizes) and/or of the available resources. An example of the latter is when both solitary and social foragers maximize rates of gain over time, but competition alters the behaviour required to achieve this, as assumed by ideal free distribution models. Here we examine this problem using captive starlings Sturnus vulgaris. Subjects had access to two depleting patches that replenished whenever the alternative patch was visited. The theoretical rate-maximizing policy was the same across all treatments, and consisted of alternating between patches following a pattern that could be predicted using the marginal value theorem (MVT). There were three treatments that differed in the contents of an aviary adjacent to one of the two patches (called the 'social' patch). In the control treatment, the aviary was empty, in the social condition it contained a group of starlings, and in a non-specific stimulus control it contained a group of zebra finches. In the control condition both patches were used equally and behaviour was well predicted by the MVT. In the social condition, starlings foraged more slowly in the social than in the solitary patch. Further, foraging in the solitary patch was faster and in the social patch slower in the social condition than in the control condition. Although these changes are incompatible with overall rate maximization (gain rate decreased by about 24% by self-imposed changes), if the self-generated gain functions were used the MVT was a good predictor of patch exploitation under all conditions. We discuss the complexities of nesting optimal foraging models in more comprehensive theoretical accounts of behaviour integrating functional and mechanistic perspectives.

Sexual dimorphism and species differences in HVC volumes of cowbirds.

Cowbirds exhibit extensive variation in their social, territorial, and reproductive behaviors. Nissl-stained brain sections of specimens from a previous study (J. C. Reboreda, N. S. Clayton, & A. Kacelnik, 1996) were used to study the gross anatomy of a song control nucleus in 3 South American cowbirds (bay-winged, Molothrus badius; shiny, M. bonariensis; and screaming, M. rufoaxillaris). Cowbird high vocal center (HVC) volumes were consistently higher in males than in females in all 3 species. The largest HVC size of females found in bay-winged cowbirds is consistent with observations that females of this species, but not of the other 2 species, occasionally sing. The extent of the sexual dimorphism of relative HVC size was highest for the sexually dichromatic and promiscuous shiny cowbirds and smaller for the monochromatic and monogamous bay-winged and screaming cowbirds, suggesting that selection pressures associated with morphological traits and social systems are reflected in brain architecture.

Behavioral adjustment to modifications in the temporal parameters of the environment.

We study the dynamics of behavioral transitions when European starlings (Sturnus vulgaris) experience stepwise changes in the value of a meaningful time interval. Subjects were primed to respond at a certain time T1. After extensive training, the primed time changed to a new value T2. In Experiment 1 subjects were reinforced on 40% of the trials and they experienced a single transition which lasted until asymptotic behavior was reached. Starlings showed a progressive adjustment to T2, with no obvious discontinuities. In Experiment 2, probability of reinforcement was initially 20%, and the schedule switched to extinction after a varied number of trials were reinforced at the post-transition time. The number of post-transition reinforcements was used as independent variable. Behavior was examined in extinction to judge the state of temporal performance after a controlled amount of experience. Under these conditions, adjustment to T2 took place in two stages, and there was an intermediate phase when behavior changed little. These results are consistent with the hypotheses that animals continuously update the subjective probabilities that reinforcement comes at any given time and that responding occurs when the current estimate is above a certain threshold. We show that in spite of the continuous updating of time estimates, responding can show either continuous or discontinuous adjustments depending on the vicinity of the pre- and post-transition times and the probability of reinforcement.

Risky choice and Weber's Law.

We present a family of models of choice between behavioural alternatives with stochastic outcomes (risky choice) based on the effects of Weber's Law in memory. These models generalise and extend a model of risk sensitive foraging originally proposed by Reboreda & Kacelnik [(1991) Behav. Ecol. 2, 301-308], which yielded qualitative predictions (risk-aversion for amount of food and risk-proneness for delay to food). We now demonstrate how this approach can predict quantitatively the partial preferences between two alternative options with any mean and variance in their outcomes, and the certainty equivalent of an option consisting of any set of probabilistic outcomes. The approach is also relevant to the economics and psychology of risk sensitivity because it predicts risk aversion for any desirable outcome (such as monetary gains) and risk seeking for any undesirable gain (such as monetary losses). Our models are process-based rather than purely normative, and are based on linear expected utility as a function of expected outcomes. They do not account for all observed aspects of risky choice, but their descriptive performance betters that of existing functional models and requires fewer parameters.

Optimal foraging and beyond: how starlings cope with changes in food availability.

Foraging adaptations include behavioral and physiological responses, but most optimal foraging models deal exclusively with behavioral decision variables, taking other dimensions as constraints. To overcome this limitation, we measured behavioral and physiological responses of European starlings Sturnus vulgaris to changes in food availability in a laboratory environment. The birds lived in a closed economy with a choice of two foraging modes (flying and walking) and were observed under two treatments (hard and easy) that differed in the work required to obtain food. Comparing the hard with the easy treatment, we found the following differences. In the hard treatment, daily amount of work was higher, but daily intake was lower. Even though work was greater, total daily expenditure was smaller, partly because overnight metabolism was lower. Body mass was lower, but daily oscillation in body mass did not differ. Feces' caloric density was lower, indicating greater food utilization. Energy expenditure rate expressed as multiples of basal metabolic rate (BMR) increased during the working period from 3.5 x BMR (easy) to 5.2 x BMR (hard), but over the 24-h period, it was close to 2.4 x BMR in both treatments. We also found that rate of expenditure during flight was very high in both treatments (52.3 W in easy and 45.5 W in hard), as expected for short (as opposed to cruising) flights. The relative preferences between walking and flying were incompatible with maximizing the ratio of energy gains per unit of expenditure (efficiency) but compatible with maximizing net gain per unit of time during the foraging cycle (net rate). Neither currency explained the results when nonforaging time was included. Time was not a direct constraint: the birds rested more than 90% of the time in both treatments. Understanding this complex picture requires reasoning with ecological, physiological, and cognitive arguments. We defend the role of optimality as an appropriate tool to guide this integrative perspective.

Sexual differences in memory in shiny cowbirds.

Avian brood parasites depend on other species, the hosts, to raise their offspring. During the breeding season, parasitic cowbirds (Molothrus sp.) search for potential host nests to which they return for laying a few days after first locating them. Parasitic cowbirds have a larger hippocampus/telencephalon volume than non-parasitic species; this volume is larger in the sex involved in nest searching (females) and it is also larger in the breeding than in the non-breeding season. In nature, female shiny cowbirds Molothrus bonariensis search for nests without the male's assistance. Here we test whether, in association with these neuroanatomical and behavioural differences, shiny cowbirds display sexual differences in a memory task in the laboratory. We used a task consisting of finding food whose location was indicated either by the appearance or the location of a covering disk. Females learnt to retrieve food faster than males when food was associated with appearance cues, but we found no sexual differences when food was associated with a specific location. Our results are consistent with the view that parasitism and its neuroanatomical correlates affect performance in memory tasks, but the effects we found were not in the expected direction, emphasising that the nature of avian hippocampal function and its sexual differences are not yet understood.

Starlings' preferences for predictable and unpredictable delays to food.

Risk-sensitive foraging theory is based on the premise that unpredictable runs of good or bad luck can cause a variable food source to differ in fitness value from a fixed food source yielding the same average rate of gain but no unpredictability. Thus, risk-sensitive predictions are dependent on the food intake from variable sources being not only variable but also unpredictable or 'risky' in outcome. This study tested whether unpredictability is a component of the value that foraging starlings, Sturnus vulgarisattribute to food sources that are variable in the delay to obtain food. Two groups of birds chose between a fixed and a variable delay option; the variable option was unpredictable in the risky group and predictable in the risk-free group in the overall rate of intake it yielded. In both groups the fixed option was adjusted by titration to quantify the magnitude of preference for predictable and unpredictable variance. On negative energy budgets both groups were significantly risk-prone, with the risky group being significantly more risk-prone than the risk-free group. Switching the birds to positive budgets by doubling the size of each food reward had no significant effect on preference, and similar trends to those found with negative budgets were observed. These results are not readily explained by risk-sensitive foraging theory, but may be explained by the algorithm used by the birds to attribute value to average expected rewards.

Normative and descriptive models of decision making: time discounting and risk sensitivity.

The task of evolutionary psychologists is to produce precise predictions about psychological mechanisms using adaptationist thinking. This can be done combining normative models derived from evolutionary hypotheses with descriptive regularities across species found by experimental psychologists and behavioural ecologists. I discuss two examples. In temporal discounting, a normative model (exponential) fails while a descriptive one (hyperbolic) fits both human and non-human data. In non-humans hyperbolic discounting coincides with rate of gain maximization in repetitive choices. Humans may discount hyperbolically in non-repetitive choices because they treat them as a repetitive rate-maximizing problem. In risk sensitivity, a theory derived from fitness considerations produces inconclusive results in non-humans, but succeeds in predicting human risk proneness and risk aversion for both the amount and delay of reward in a computer game. Strikingly, and in contrast with the existing literature, risk aversion for delay occurs as predicted. The predictions of risk aversion for delay may fail in many animal experiments because the manipulations of the utility function are not appropriate. In temporal discounting animal experiments help the interpretation of human results, while in risk sensitivity studies human results help the analysis of non-human data.

Risk-sensitivity: crossroads for theories of decision-making.

Most actions result in one of a set of possible outcomes. To understand how this uncertainty, or risk, affects animals' decision-making some researchers take a normative approach, asking how an animal should respond to risk if it is maximizing its fitness. Others focus on predicting responses to risk by generalizing from regularities in behavioural data, without reference to cognitive processes. Yet others infer cognitive processes from observed behaviour and ask what actions are predicted when these processes interact with risk. The normative approach (Risk-sensitivity Theory; RST) is unique in predicting a shift in a subject's response to risk as a function of its resource budget, but the predictions of this theory are not yet widely confirmed. In fact, evidence suggests a strong bias towards risk-proneness when delay to reward is risky and risk-aversion when amount of reward is risky, a pattern not readily explained by RST. Extensions of learning theory and of Scalar Expectancy Theory provide process-based explanations for these findings but do not handle preference shifts or provide evolutionary justification for the processes assumed. In this review we defend the view that risk-sensitivity must be studied with theoretical plurality.

Seasonal changes of hippocampus volume in parasitic cowbirds.

Avian brain plasticity has been demonstrated by seasonal variations in neuroanatomy correlated with changes in singing and hoarding behaviour. We report a new instance of plasticity. Brood parasitism in South American cowbirds involves memory for location of hosts' nests, and is associated with an enlarged hippocampus relative to telencephalon size. This effect holds between sexes and species during the breeding season. We report that for two parasitic species, relative hippocampal volume is smaller during the non-breeding than the breeding season, and that sexual dimorphism present in summer in one of the species is not found in winter. These results support the hypothesis that the avian hippocampal formation shows neuroanatomical plasticity associated with seasonal changes in spatial memory demands.

The evolution of begging: signaling and sibling competition.

In many species, young solicit food from their parents, which respond by feeding them. Because of the difference in genetic make-up between parents and their offspring and the consequent conflict, this interaction is often studied as a paradigm for the evolution of communication. Existent theoretical models demonstrate that chick signaling and parent responding can be stable if solicitation is a costly signal. The marginal cost of producing stronger signals allows the system to converge to an equilibrium: young beg with intensity that reflects their need, and parents use this information to maximize their own inclusive fitness. However, we show that there is another equilibrium where chicks do not beg and parents' provisioning effort is optimal with respect to the statistically probable distribution of chicks' states. Expected fitness for parents and offspring at the nonsignaling equilibrium is higher than at the signaling equilibrium. Because nonsignaling is stable and it is likely to be the ancestral condition, we would like to know how natural systems evolved from nonsignaling to signaling. We suggest that begging may have evolved through direct sibling fighting before the establishment of a parental response, that is, that nonsignaling squabbling leads to signaling. In multiple-offspring broods, young following a condition-dependent strategy in the contest for resources provide information about their condition. Parents can use this information even though it is not an adaptation for communication, and evolution will lead the system to the signaling equilibrium. This interpretation implies that signaling evolved in multiple-offspring broods, but given that signaling is evolutionarily stable, it would also be favored in species which secondarily evolved single-chick broods.

Species and sex differences in hippocampus size in parasitic and non-parasitic cowbirds.

To test the hypothesis that selection for spatial abilities which require birds to locate and to return accurately to host nests has produced an enlarged hippocampus in brood parasites, three species of cowbird were compared. In shiny cowbirds, females search for host nests without the assistance of the male; in screaming cowbirds, males and females inspect hosts' nests together; in bay-winged cowbirds, neither sex searches because this species is not a brood parasite. As predicted, the two parasitic species had a relatively larger hippocampus than the non-parasitic species. There were no sex differences in relative hippocampus size in screaming or bay-winged cowbirds, but female shiny cowbirds had a larger hippocampus than the male.

Preferences for fixed and variable food sources: variability in amount and delay.

Much research has focused on the effects of environmental variability on foraging decisions. However, the general pattern of preference for variability in delay to reward and aversion to variability in amount of reward remains unexplained a either a mechanistic or a functional level. Starlings' preferences between a fixed and a variable option were studied in two treatments, A and D. The fixed option was the same in both treatments (20-s fixed-interval delay, five units food). In Treatment A the variable option gave two equiprobable amounts of food (20-s delay, three or seven units) and in D it gave two equiprobable delays to food (2.5-s or 60.5-s delays, five units). In both treatments the programmed ratio [amount/(intertrial interval+latency+delay)] in the fixed option equaled the arithmetic mean of the two possible ratios in the variable option (ITI = 40 s, latency = 1 s). The variable option was strongly preferred in Treatment D and was weakly avoided in Treatment A. These results are discussed in the light of two theoretical models, a form of constrained rate maximization and a version of scalar expectancy theory. The latter accommodates more of the data and is based on independently verifiable assumptions, including Weber's law.