Benefits of zebra stripes: Behaviour of tabanid flies around zebras and horses

Benefits of zebra stripes: Behaviour of tabanid flies around zebras and horses. Tim Caro et al. PLOS, February 20, 2019. https://doi.org/10.1371/journal.pone.0210831

Abstract: Averting attack by biting flies is increasingly regarded as the evolutionary driver of zebra stripes, although the precise mechanism by which stripes ameliorate attack by ectoparasites is unknown. We examined the behaviour of tabanids (horse flies) in the vicinity of captive plains zebras and uniformly coloured domestic horses living on a horse farm in Britain. Observations showed that fewer tabanids landed on zebras than on horses per unit time, although rates of tabanid circling around or briefly touching zebra and horse pelage did not differ. In an experiment in which horses sequentially wore cloth coats of different colours, those wearing a striped pattern suffered far lower rates of tabanid touching and landing on coats than the same horses wearing black or white, yet there were no differences in attack rates to their naked heads. In separate, detailed video analyses, tabanids approached zebras faster and failed to decelerate before contacting zebras, and proportionately more tabanids simply touched rather than landed on zebra pelage in comparison to horses. Taken together, these findings indicate that, up close, striped surfaces prevented flies from making a controlled landing but did not influence tabanid behaviour at a distance. To counteract flies, zebras swished their tails and ran away from fly nuisance whereas horses showed higher rates of skin twitching. As a consequence of zebras’ striping, very few tabanids successfully landed on zebras and, as a result of zebras’ changeable behaviour, few stayed a long time, or probed for blood.

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Introduction

The function of zebra stripes has been a source of scientific interest for over 150 years generating many hypotheses including camouflage, confusion of predators, signaling to conspecifics, thermoregulation and avoidance of biting flies [1] but contemporary data show that only one stands up to careful scrutiny [2–4]. Briefly, regarding camouflage, zebra stripes are difficult for lion Panthera leo and spotted hyaena Crocuta crocuta predators to resolve at any great distance making crypsis against mammalian predators an unlikely benefit [5]. Regarding confusion of predators, zebras do not have the sort of striping pattern that aids in confusion [6] and African lions take zebra prey disproportionately more than expected suggesting an absence of confusion effect [7]. Regarding social benefits, rates of grooming and patterns of association are no greater in striped equids than in unstriped equids [3]. Finally, there are no thermoregulatory benefits to striping based on controlled experiments using water drums [4], infrared photography of free-living herbivores [3] and logical argument in regards to flank striping [8].
Instead, there is an emerging consensus among biologists that the primary function of contrasting black and white stripes on the three species of zebras is to thwart attack from tabanids, and possibly glossinids, stomoxys and other biting muscoids based on laboratory and field experiments with striped materials [3, 9–12] and on comparative evidence [13]. In Africa where zebras live, tabanids carry diseases fatal to zebras including trypanosomiasis, equine infectious anemia, African horse sickness and equine influenza [14] and zebras are particularly susceptible to infection because their thin pelage allows biting flies to probe successfully with their mouthparts [13]. The exact mechanism by which stripes prevent flies from obtaining a blood meal is less well understood, however. Flies may fail to detect a zebra from a distance, or from close up, either as a result of misinterpreting optic flow as they approach [15], by interfering with cues that promote a landing response [9, 16], or even by disrupting the polarization signature of their host [12]. Unfortunately, detailed observations of biting flies in the vicinity of live zebras have so far been unavailable but such information would help elucidate the stage at which stripes exert an effect on host seeking by biting flies.
In this study we compare several measures of behaviour of wild tabanid horse flies around captive zebras and domestic horses living in the same habitat using direct observations and video footage. We also compare the behaviour of tabanids around horses wearing differently coloured cloth coats, report on the duration of time that tabanids spend on equids with different coloured pelage, and compare the behaviour of horses and zebras in response to biting fly annoyance.

Conclusion

In summary, multiple lines of evidence indicate that stripes prevent effective landing by tabanids once they are in the vicinity of the host but did not prevent them approaching from a distance. In addition, zebras appear to use behavioural means to prevent tabanids spending time on them through constant tail swishing and even running away. As a consequence of both of these morphological and behavioural defenses, very few tabanids are able to probe for a zebra blood meal as evidenced by our data.
Three additional but more speculative points may be made in closing. First, we found that rates at which tabanids circled and touched a single grey horse were lower than for zebras although landing rates did not differ significantly (Table Ba-c in S1 File). This was in contrast to comparisons between zebras and horses of other colours where circling and touching rates did not differ but where zebras enjoyed fewer landings per unit time. More work on grey pelage in relation to fly annoyance is clearly needed because stripes will appear grey from a distance to flies (Text A in S1 File).
Second, we found that there was no difference in rates at which tabanids moved across the surface of striped or uniform coats. Since black and white stripes give off different heat loads during the day [30–32], they could possibly confuse a tabanid if it tried to locate a capillary by thermal sensitivity (although we have no evidence that they do this). If stripes did prevent a tabanid from locating a capillary we might expect greater rates of searching zebra pelage but this was not the case.
Third, extremely high rates of tail flicking were seen in the zebra/wild ass hybrid at Dundry (Text B in S1 File) similar to that observed in African wild asses at the Tierpark Zoo (table 5.3 in [3]) suggesting that tail flicking may in part be a species-specific trait. Striping is also a species specific trait and also under partial genetic control (as witnessed by mother-offspring striping similarities, for example, TC pers obs). Therefore both morphological and behavioural anti-parasite defense strategies appear to be under strong selection in zebras.