The making of ethology: The association for the Study of Animal Behaviour, 1936–1986

The paper reviews the history of the Association for the Study of Animal Behaviour in its 50th anniversary year. Having discussed the founding of the Institute for the Study of Animal Behaviour in 1936, the paper establishes its principal aims, follows its fortunes before and during the war, traces its role in the expansion and institutionalization of ethology in Britainbetween 1945 and 1950, and summarizes its transformation into a flourishing scientific society in the 1950s and 1960s. It is concluded that the history of the Association is, to a striking extent, a microcosm of the making of ethology as a successful scientific discipline.     

Parasitism increases offspring size in a damselfly: experimental evidence for parasite-mediated maternal effects

The effects of parasites on host fitness and the fitness effects of maternal effects are widely discussed. In this study, I conducted an experiment linking both aspects. I manipulated the ectoparasite load (Acari: Arrenurus cuspidator) of damselflies, Coenagrion puella, and found that larvae from mothers with high parasite loads were larger (assessed by head width) than larvae from mothers with low parasite loads. Furthermore, there was a negative correlation between the number of eggs laid and parasite load. Parasitized mothers thus seemed to have fewer, but probably better, offspring. The ecological significance of these parasite-mediated maternal effects remains to be tested. However, size-dependent cannibalism almost certainly has important consequences for population dynamics. Copyright 1999 The Association for the Study of Animal Behaviour.     

Courtship song rhythms in Drosophila yakuba

We studied the courtship songs of males from several strains of Drosophila yakuba. There was clear evidence for two types of pulse songs, generated by the male's wing vibration, which we called 'thud' song and 'clack' song. Clack song was generated by both wings, at distances further from the female than the thud component, which was produced by one-wing displays. The carrier frequency of clack song was considerably higher than that of thud, whereas the interpulse intervals (IPI) of thud song, which usually predominated, were shorter. Furthermore, thud song revealed a cycling of IPIs with a period of about 70 s, significantly longer than that of D. melanogaster or D. simulans. Copyright 1999 The Association for the Study of Animal Behaviour.     

Synchronous polyandry and multiple paternity in the frog Crinia georgiana (Anura: Myobatrachidae)

Multiple paternity has rarely been reported in anuran amphibians, with only three previous documented examples. For the Australian frog Crinia georgiana, we observed synchronous polyandry in an average of 44% of matings observed at four field sites. This suggests matings involving more than one male are common in this species. One to eight males were observed in amplectant groups with second males amplexed ventrally. Genetic analyses, using allozyme electrophoresis, of offspring from two matings indicated that at least two of three possible males fathered offspring. Third males were unlikely to have shared paternity, explained by their inappropriate position during amplexus. Multiple paternity may be more common in frogs than has been reported. Copyright 1999 The Association for the Study of Animal Behaviour.     

Endogenous rhythms of locomotor activity in the high-shore limpet, Helcion pectunculus (Patellogastropoda)

Helcion pectunculus, a high-shore, crevice-dwelling limpet, is active during nocturnal low tides and during daytime low tides whilst in the shade. We examined whether this activity is controlled by an internal clock or purely by exogenous stimuli, such as light levels and tidal phase. Maximum entropy spectral analysis (MESA) revealed that the limpets possess a free-running endogenous rhythm of locomotor activity with both circadian (period 28.1 h) and circatidal (period 13.8 h) components. We suggest that this rhythm plays a role in allowing individuals to avoid unfavourable environmental conditions. The exogenous entrainment factor of the endogenous circatidal rhythm in H. pectunculus is the time of exposure to air, whilst the zeitgeber for the circadian component is not yet known. Copyright 1999 The Association for the Study of Animal Behaviour.     

Impact of geographical origin on mating behaviour in two species of Biomphalaria (Planorbidae: Gastropoda)

Studies of inbreeding and outcrossing have traditionally concentrated on matings within populations. The influence of geographical origin on mate choice in animals from different populations has received less attention. We investigated whether planorbid snails mated preferentially within their own population or with snails from other populations. Snails from three Biomphalaria pfeifferi strains and three B. glabrata strains were allowed to mate with conspecifics in the laboratory. We recorded their matings at night using time-lapse video. When they could choose between sympatric and allopatric snails, Biomphalaria snails significantly preferred the former: snails of each population mated more often with sympatric than with allopatric snails. This tendency to avoid outcrossing may indicate that, in some species, local adaptations can be more valuable than genetic novelties. Copyright 1999 The Association for the Study of Animal Behaviour.     

The effect of variability in the food supply on the daily singing routines of European robins: a test of a stochastic dynamic programming model

A stochastic dynamic programming (SDP) model offers a general explanation of daily singing routines in birds, but remains almost untested empirically. I examined a central prediction of the SDP model, that a more variable food supply decreases the bird's song output at dawn, relative to its song output at dusk. I provided supplementary food to make the food supply more or less variable over 2-week periods in the territories of free-living European robins Erithacus rubecula. Robins sang relatively less at dawn than at dusk after weeks in which their supplementary food supply was variable, and more at dawn than at dusk after weeks in which their food supplementation was constant. These results provide strong support for the prediction of the SDP model. Copyright 1999 The Association for the Study of Animal Behaviour.     

Social anxiety, relationships and self-directed behaviour among wild female olive baboons

Self-directed behaviour (SDB) can be used as a behavioural indicator of stress and anxiety in nonhuman primates (Maestripieri et al. 1992, Animal Behaviour, 44, 967-979). We investigated the effect of nearest neighbours' relative dominance status on the SDB of sexually mature female olive baboons, Papio anubis. When the animal nearest to (within 5 m of) a female was a dominant individual, SDB rates (a combined measure of self-scratching, self-grooming, self-touching, body shaking and yawning) increased by ca. 40% over those observed when the nearest neighbour was a subordinate. The results indicate that (1) SDB can be used as a measure of uncertainty during the social interactions of cercopithecine primates and (2) as there was considerable variation in SDB response according to the nature of the dominant individual, SDB can be used to assess relationship security (i.e. the perceived predictability of a relationship for one partner). Finally, in combination with measures of affiliation rate, SDB may provide insight into relationship value. Copyright 1999 The Association for the Study of Animal Behaviour.     

The role of urine marking in the foraging behaviour of least chipmunks

Least chipmunks Tamias minimus, occasionally deposit urine on buried patches of seeds after sampling the patch, a behaviour never before reported for rodents. The results of these experiments show that (1) patch-marking is a deliberate act, bearing no resemblance to routine excretion, (2) marking deters both the marker and conspecifics from harvesting attempts, (3) chipmunks can discriminate their own marks from those of others, and (4) the incidence of marking in the wild is at least as frequent, and its deterrent effect as strong as in the laboratory. Although the message conveyed by a mark is clearly exploited by conspecifics, and may benefit kin, the results accord best with prevailing theory advanced for canids, that an olfactory reminder of patch value improves the marker's foraging efficiency. Copyright 1999 The Association for the Study of Animal Behaviour.     

Size-assortative mating, male choice and female choice in the curculionid beetle Diaprepes abbreviatus

In the beetle Diaprepes abbreviatus (L.) females are larger on average than males, as indicated by elytra length. Size-assortative matings were observed in wild populations in Florida and in laboratory mating experiments. We tested three mechanisms for this size-assortative mating: (1) mate availability; (2) mating constraints; and (3) mate choice. We found that mate choice influenced size-assortative mating by: (1) large and small males preferring to mate with large females; (2) large males successfully competing for large females, leaving small males to mate with small females; and (3) females accepting large males as mates more readily than small males. Males increased their reproductive success by mating with larger, more fecund females. They transferred protein to females during mating. Copyright 1999 The Association for the Study of Animal Behaviour.     

Song type switching in the chaffinch, Fringilla coelebs : timing or counting?

The song of many bird species is relatively constant in form, yet each bird has more than one song type, making it an excellent model for studies of the mechanisms underlying switching between behaviour patterns. The chaffinch is a good example. Males sing with eventual variety, repeating each song type in the repertoire a few times before switching to another type. The mechanism triggering these switches is not known. We investigated long continuous recordings of spontaneous singing by six wild males to test two hypotheses: (1) that a maximum number of repetitions limits bout length; or (2) that a switch occurs after a song type bout reaches a maximum duration ('time window'). Strong evidence was found for a temporal limitation: song type bouts with many repetitions were delivered only at a fast rate, whereas bouts consisting of few songs were delivered either fast or slow. Copyright 1999 The Association for the Study of Animal Behaviour.     

'Friendship' for fitness in chimpanzees?

It has been repeatedly suggested that primates trade social services for fitness benefits in their relationships with the opposite sex. We tested this proposal in a colony of captive chimpanzees, Pan troglodytes, by examining behavioural data on grooming, agonistic support and food sharing in relation to genetically established paternity. We found no support for the notion of trade. First, males did not sire more offspring with females that they actively groomed more frequently, that they supported more often or with which they shared food more frequently. Correspondingly, females did not give birth to more offspring sired by males from which they received more services. Second, males that showed more affiliative behaviour towards females in general did not sire more progeny. Furthermore, females did not bear more offspring sired by males to which they themselves directed more sociopositive behaviour. Results from this captive colony are compatible with those reported for chimpanzees under natural conditions. Copyright 1999 The Association for the Study of Animal Behaviour.     

Patch choice and risk: relative competitive ability is context dependent

The relative abilities of individual cichlids, Tilapia zillii to obtain food under scramble competition was highly repeatable between trials using a single input source, regardless of whether the input was constant or variable. However, when given a choice between two patches differing only in their temporal variability in input about an identical mean, an individual's rank based on intake in one patch was uncorrelated with either its intake in the other patch or its intake in the single-patch trials. In the two-patch trials, certain individuals both spent more time in food patches and visited patches more often than others, and overall the fish spent more time in the constant rate patch than the variable patch, leading to more items being consumed from the constant rate patch. We discuss possible causes and consequences of this dependence of relative competitive ability on the context of the foraging situation. Copyright 1999 The Association for the Study of Animal Behaviour.     

Receiver psychology and the evolution of multicomponent signals

Many animals produce and respond to signals made up of multiple components. For example, many avian sexual displays are highly extravagant combinations of visual and acoustic elements, and are described as being 'multicomponent'. One possible reason for the evolution of such complex signals is that they provide more reliable information for receivers. However, receivers also influence signal evolution in another important way, by how they perceive and process signals: signallers will be selected to produce signals that are more easily received. The potential role of receiver psychology in the evolution of multicomponent signals has not previously been considered; in this review I present psychological results that support the notion that two components are better received than one alone. Detection can be improved by producing two components together, thus reducing the reaction time, increasing the probability of detection and lowering the intensity at which detection occurs. Discriminability of multicomponent stimuli is also made easier through better recognition, faster discrimination learning and multidimensional generalization. In addition, multicomponent stimuli also improve associative learning. I show that multicomponency does indeed improve signal reception in receivers, although the benefits of producing components in two sensory modalities (bimodal multicomponent signals) may be larger and more robust than producing them in just one (unimodal multicomponent signals). This highlights the need for consideration of receiver psychology in the evolution of multicomponent signals, and suggests that where signal components do not appear to be informative, they may instead be performing an important psychological function. Copyright 1999 The Association for the Study of Animal Behaviour.     

Staying in plastic containers interferes with the orientation of clock-shifted homing pigeons

Staying in plastic containers ventilated with natural air during transport and while waiting at the release site was found to affect the initial orientation of pigeons, Columba livia f. domestica, that were exposed to a 6-h clock-shift. The deflection from the mean direction of controls was significantly smaller, and the mean vector length was significantly shorter, than that of clock-shifted pigeons transported in conventional wooden cages. This effect was most pronounced when the birds stayed in plastic containers for the first and second time. Nonshifted control birds seemed to be largely unaffected by plastic containers. There was no influence on homing performance, which suggests a transient nature of the effect. Since the clock-shifted birds had access to the same orientational cues as the controls, we suggest that their sun compass was impaired by stress. We discuss general implications of this container effect, particularly in relation to some cases of olfactory deprivation where containers have been used and stress-induced side-effects cannot be excluded. Copyright 1999 The Association for the Study of Animal Behaviour.     

Urinary chemical cues affect light avoidance behaviour in male laboratory mice, Mus musculus

Chemical signals from conspecifics can influence the behaviour and neuroendocrine axis of mice. Several different molecules are excreted with urine, depending on hormonal level, and can indicate the sex of the emitter. In male mice, these chemicals are the major urinary proteins (MUPs) and some small volatile odorant molecues that are found bound to them. We tested adult males for light avoidance behaviour in a two-chamber apparatus, with one light and one dark side, in the presence or absence of male urinary substances. The presence of chemical cues on either side of the cage was expected to modify light avoidance behaviour. The volatiles released from purified MUPs had the same effect as whole adult male urine, in that they induced a faster onset of exploration of the light compartment. The results show that mice can use the information carried by the odorant molecules released by MUPs to recognize the urine of male mice, and respond appropriately. Copyright 1999 The Association for the Study of Animal Behaviour.     

Helping behaviour in facultatively eusocial hover wasps: an experimental test of the subfertility hypothesis

A candidate explanation for the evolution of eusociality is that helpers are physiologically constrained such that helping is their only realistic option. We tested this subfertility hypothesis in a species of facultatively eusocial hover wasp (Hymenoptera, Stenogastrinae: Liostenogaster flavolineata) by seeing whether helpers that were forced to nest on their own were able to mature their own eggs. One focal helper was left alone on each of 22 nests, from which all other adult wasps (including the dominant) were permanently removed. After 18 days, all but one of the 19 focal helpers that remained on their nests had ovarian development and insemination status characteristic of dominants, and the majority had probably laid eggs. This was in striking contrast to the reproductive status of other helpers removed from the same nests at the start of the experiment. These results provide convincing experimental evidence that females do not become helpers because of some unconditional physiological constraint. There is currently no unequivocal support for the subfertility hypothesis in facultatively eusocial Hymenoptera lacking morphological castes. Copyright 1999 The Association for the Study of Animal Behaviour.     

The influence of nutritional state on shoal choice in zebrafish, Danio rerio

We investigated the mechanisms and functions of shoal choice in relation to nutritional state in the zebrafish. Single fish that had been well fed or food deprived for 2 days were presented with a choice between two stimulus shoals. Food-deprived test fish showed a significant preference for well-fed stimulus fish over food-deprived ones whereas well-fed test fish did not exhibit any significant preference. Subsequent experiments showed that food-deprived test fish had a significantly higher foraging success in shoals consisting of well-fed individuals than in ones that comprised food-deprived fish. No difference in the locomotory behaviour of food-deprived and well-fed stimulus fish was found with respect to the proportion of time spent swimming (as opposed to being motionless), the proportion of time spent in the upper part of the test tank and the number of sharp turns. However, body weight, stomach width (measured directly behind the pectoral girdle) and ventro-dorsal height significantly decreased over a 48-h food-deprivation period. The potential use of the latter factors for the recognition of food-deprived individuals is discussed. Copyright 1999 The Association for the Study of Animal Behaviour.     

Assessing parental effort in a Neotropical parrot: a comparison of methods

Various behavioural or body condition indices are frequently used to measure avian parental effort. To determine which of the indices provide meaningful short-term assessments of parental effort, we used four of them concurrently on breeding green-rumped parrotlets, Forpus passerinus, and then compared the results with field metabolic rate (FMR) measurements obtained using the doubly labelled water (DLW) technique. Nest provisioning rate correlated significantly with FMR among both males and females, while proportion of time away from the nest was correlated with FMR in females but not in males. Adult mass change during the breeding cycle and feeding latency were both unrelated to FMR. Our results suggest researchers should be cautious in assuming that any indirect method of quantifying parental effort is reliable for a particular species. We also tested whether the relatively invasive DLW protocol causes potentially confounding changes in study animals' subsequent behaviour. Paired observations before and after DLW injection showed no measurable changes in parrotlet nest attendance patterns or nest provisioning rate. Copyright 1999 The Association for the Study of Animal Behaviour.     

Prospecting enhances breeding success of first-time breeders in the great cormorant, Phalacrocorax carbo sinensis

In many species of colonial seabirds, young birds visit colonies in the years before they start breeding. This prospecting behaviour may allow them to obtain information that could enhance their future breeding success. We examined the reproductive consequences of prospecting behaviour in the colonial great cormorant, and found support for this idea. New breeders that had been prospecting actively in the previous year obtained breeding sites of higher quality (i.e. closer to sites where conspecifics had fledged young in the previous year) and had higher breeding success than those that had been less active. Prospecting occurred mostly late in the breeding season, and coincided with the time when the majority of the eggs had hatched but before the chicks started fledging, that is, when breeding success in the colony reflected habitat suitability. These results are thus consistent with the use of conspecific reproductive performance as a cue for the quality of a breeding habitat as expected from the 'performance-based conspecific attraction hypothesis'. Copyright 1999 The Association for the Study of Animal Behaviour.