Roger Schürch

Evolutionary causes and consequences of consistent individual variation in cooperative behaviour.

Behaviour is typically regarded as among the most flexible of animal phenotypic traits. In particular, expression of cooperative behaviour is often assumed to be conditional upon the behaviours of others. This flexibility is a key component of many hypothesized mechanisms favouring the evolution of cooperative behaviour. However, evidence shows that cooperative behaviours are often less flexible than expected and that, in many species, individuals show consistent differences in the amount and type of cooperative and non-cooperative behaviours displayed. This phenomenon is known as ‘animal personality’ or a ‘behavioural syndrome’. Animal personality is evolutionarily relevant, as it typically shows heritable variation and can entail fitness consequences, and hence, is subject to evolutionary change. Here, we review the empirical evidence for individual variation in cooperative behaviour across taxa, we examine the evolutionary processes that have been invoked to explain the existence of individual variation in cooperative behaviour and we discuss the consequences of consistent individual differences on the evolutionary stability of cooperation. We highlight that consistent individual variation in cooperativeness can both stabilize or disrupt cooperation in populations. We conclude that recognizing the existence of consistent individual differences in cooperativeness is essential for an understanding of the evolution and prevalence of cooperation.

Waggle dance distances as integrative indicators of seasonal foraging challenges

Even as demand for their services increases, honey bees (Apis mellifera) and other pollinating insects continue to decline in Europe and North America. Honey bees face many challenges, including an issue generally affecting wildlife: landscape changes have reduced flower-rich areas. One way to help is therefore to supplement with flowers, but when would this be most beneficial? We use the waggle dance, a unique behaviour in which a successful forager communicates to nestmates the location of visited flowers, to make a 2-year survey of food availability. We “eavesdropped” on 5097 dances to track seasonal changes in foraging, as indicated by the distance to which the bees as economic foragers will recruit, over a representative rural-urban landscape. In year 3, we determined nectar sugar concentration. We found that mean foraging distance/area significantly increase from springs (493 m, 0.8 km2) to summers (2156 m, 15.2 km2), even though nectar is not better quality, before decreasing in autumns (1275 m, 5.1 km2). As bees will not forage at long distances unnecessarily, this suggests summer is the most challenging season, with bees utilizing an area 22 and 6 times greater than spring or autumn. Our study demonstrates that dancing bees as indicators can provide information relevant to helping them, and, in particular, can show the months when additional forage would be most valuable.

The building-up of social relationships: behavioural types, social networks and cooperative breeding in a cichlid.

Consistent individual differences in behavioural types may not only cause variation in life-history decisions, but may also affect the choice of social partners and sociality in general. Here, we tested whether and how behavioural type influences the establishment of social ties using the cooperatively breeding cichlid, Neolamprologus pulcher. In a habitat saturation experiment with individuals pre-tested for behavioural type, we first analysed whether behavioural type affected the likelihood of settlement (i.e. social status), group sizes, and the types of dominant and subordinate individuals accepted as group members. Corrected for effects of body size and sex, the behavioural type did not affect settlement. However, bold dominant males only accepted smaller females, and grouped with bold subordinates, while shy dominant males accepted larger females than themselves, and grouped with shy subordinates. Second, we analysed the relationships between behavioural type and the aggressiveness or affiliation social network. Behavioural type significantly affected the number and quality of connections within the two networks. We show that behavioural types affect group composition, social networks and status achieved, in interaction with body size. Thus, the interactions within groups may depend not only on age, size and sex, but also on the behavioural type of the individuals involved.

Dancing Bees Communicate a Foraging Preference for Rural Lands in High-Level Agri-Environment Schemes

Since 1994, more than €41 billion has been spent in the European Union on agri-environment schemes (AESs), which aim to mitigate the effects of anthropomorphic landscape changes via financial incentives for land managers to encourage environmentally friendly practices [1-6]. Surprisingly, given the substantial price tag and mandatory EU member participation [2], there is either a lack of [1] or mixed [1, 2, 7] evidence-based support for the schemes. One novel source of data to evaluate AESs may be provided by an organism that itself may benefit from them. Honeybees (Apis mellifera), important pollinators for crops and wildflowers [8, 9], are declining in parts of the world from many factors, including loss of available forage from agricultural intensification [10-13]. We analyzed landscape-level honeybee foraging ecology patterns over two years by decoding 5,484 waggle dances from bees located in the center of a mixed, urban-rural 94 km(2) area, including lands under government-funded AESs. The waggle dance, a unique behavior performed by successful foragers, communicates to nestmates the most profitable foraging locations [14-16]. After correcting for distance, dances demonstrate that honeybees possess a significant preference for rural land managed under UK Higher Level AESs and a significant preference against rural land under UK Organic Entry Level AESs. Additionally, the two most visited areas contained a National and Local Nature Reserve, respectively. Our study demonstrates that honeybees, with their great foraging range and sensitive response to forage quality, can be used as bioindicators to monitor large areas and provide information relevant to better environmental management.

Negative Feedback Enables Fast and Flexible Collective Decision-Making in Ants

Positive feedback plays a major role in the emergence of many collective animal behaviours. In many ants pheromone trails recruit and direct nestmate foragers to food sources. The strong positive feedback caused by trail pheromones allows fast collective responses but can compromise flexibility. Previous laboratory experiments have shown that when the environment changes, colonies are often unable to reallocate their foragers to a more rewarding food source. Here we show both experimentally, using colonies of Lasius niger, and with an agent-based simulation model, that negative feedback caused by crowding at feeding sites allows ant colonies to maintain foraging flexibility even with strong recruitment to food sources. In a constant environment, negative feedback prevents the frequently found bias towards one feeder (symmetry breaking) and leads to equal distribution of foragers. In a changing environment, negative feedback allows a colony to quickly reallocate the majority of its foragers to a superior food patch that becomes available when foraging at an inferior patch is already well underway. The model confirms these experimental findings and shows that the ability of colonies to switch to a superior food source does not require the decay of trail pheromones. Our results help to resolve inconsistencies between collective foraging patterns seen in laboratory studies and observations in the wild, and show that the simultaneous action of negative and positive feedback is important for efficient foraging in mass-recruiting insect colonies.

Incorporating variability in honey bee waggle dance decoding improves the mapping of communicated resource locations

Honey bees communicate to nestmates locations of resources, including food, water, tree resin and nest sites, by making waggle dances. Dances are composed of repeated waggle runs, which encode the distance and direction vector from the hive or swarm to the resource. Distance is encoded in the duration of the waggle run, and direction is encoded in the angle of the dancer’s body relative to vertical. Glass-walled observation hives enable researchers to observe or video, and decode waggle runs. However, variation in these signals makes it impossible to determine exact locations advertised. We present a Bayesian duration to distance calibration curve using Markov Chain Monte Carlo simulations that allows us to quantify how accurately distance to a food resource can be predicted from waggle run durations within a single dance. An angular calibration shows that angular precision does not change over distance, resulting in spatial scatter proportional to distance. We demonstrate how to combine distance and direction to produce a spatial probability distribution of the resource location advertised by the dance. Finally, we show how to map honey bee foraging and discuss how our approach can be integrated with Geographic Information Systems to better understand honey bee foraging ecology.

Intra-dance variation among waggle runs and the design of efficient protocols for honey bee dance decoding

Summary Noise is universal in information transfer. In animal communication, this presents a challenge not only for intended signal receivers, but also to biologists studying the system. In honey bees, a forager communicates to nestmates the location of an important resource via the waggle dance. This vibrational signal is composed of repeating units (waggle runs) that are then averaged by nestmates to derive a single vector. Manual dance decoding is a powerful tool for studying bee foraging ecology, although the process is time-consuming: a forager may repeat the waggle run 1- >100 times within a dance. It is impractical to decode all of these to obtain the vector; however, intra-dance waggle runs vary, so it is important to decode enough to obtain a good average. Here we examine the variation among waggle runs made by foraging bees to devise a method of dance decoding. The first and last waggle runs within a dance are significantly more variable than the middle run. There was no trend in variation for the middle waggle runs. We recommend that any four consecutive waggle runs, not including the first and last runs, may be decoded, and we show that this methodology is suitable by demonstrating the goodness-of-fit between the decoded vectors from our subsamples with the vectors from the entire dances.

Repeatability and Heritability of Behavioural Types in a Social Cichlid

Aim. The quantitative genetics underlying correlated behavioural traits (‘‘animal personality”) have hitherto been studied mainly in domesticated animals. Here we report the repeatability (R) and heritability (h2) of behavioural types in the highly social cichlid fish Neolamprologus pulcher. Methods. We tested 1779 individuals repeatedly and calculated the h2 of behavioural types by variance components estimation (GLMM REML), using 1327 offspring from 162 broods from 74 pairs. Results. Repeatability of behavioural types was significant and considerable (0.546), but declined from 0.83 between tests conducted on the same day, to 0.19 on tests conducted up to 1201 days apart. All h2 estimates were significant but low (e.g., pair identity h2 = 0.15 ± 0.03 SE). Additionally, we found significant variation between broods nested within the parent(s), but these were not related to several environmental factors tested. Conclusions. We conclude that despite a considerable R, h2 in this cichlid species is low, and variability in behavioural type appears to be strongly affected by other (non)genetic effects.

The functional significance of buccal feeding in the mouthbrooding cichlid Tropheus moorii

The mouthbrooding cichlid Tropheus moorii exhibits an exceptional degree of maternal investment. Females produce very large eggs, which are incubated for a period of six weeks, and they feed their young in the mouth while starving themselves. Only very few fish species are known to feed their young. We hypothesized that feeding may either (1) benefit females directly if young develop faster, or (2) provide a size advantage to young. To distinguish between these mutually non-exclusive hypotheses, we measured costs and benefits arising for mouthbrooding females when feeding their young. Field observations revealed that mouthbrooding females reduced bite rates, locomotion and territorial defence compared to non-brooding adults. Feeding rates correlated positively with locomotion, as fish moving around more also spent more time with territory defence and other social interactions. This suggests that buccal feeding is costly when compared to mere incubation without feeding the young. In an experiment, in which we controlled the access of females to food, we showed that these costs are apparently not counterbalanced by a benefit to females through a shorter incubation duration. Rather, fed young were larger, heavier and had higher burst-swimming speeds. The extreme maternal investment of T. moorii appears to yield fitness benefits to females by producing larger and stronger young, which consequently should have better survival chances in their natural environment.

Dancing Bees Improve Colony Foraging Success as Long-Term Benefits Outweigh Short-Term Costs

Waggle dancing bees provide nestmates with spatial information about high quality resources. Surprisingly, attempts to quantify the benefits of this encoded spatial information have failed to find positive effects on colony foraging success under many ecological circumstances. Experimental designs have often involved measuring the foraging success of colonies that were repeatedly switched between oriented dances versus disoriented dances (i.e. communicating vectors versus not communicating vectors). However, if recruited bees continue to visit profitable food sources for more than one day, this procedure would lead to confounded results because of the long-term effects of successful recruitment events. Using agent-based simulations, we found that spatial information was beneficial in almost all ecological situations. Contrary to common belief, the benefits of recruitment increased with environmental stability because benefits can accumulate over time to outweigh the short-term costs of recruitment. Furthermore, we found that in simulations mimicking previous experiments, the benefits of communication were considerably underestimated (at low food density) or not detected at all (at medium and high densities). Our results suggest that the benefits of waggle dance communication are currently underestimated and that different experimental designs, which account for potential long-term benefits, are needed to measure empirically how spatial information affects colony foraging success.