From eminent biologists like Alfred Russel Wallace and Charles Darwin to famous authors such as Rudyard Kipling in his Just So Stories, many people have asked, “Why do zebras have stripes?” There are many explanations, but until now hardly any have been seriously addressed or even tested. In Zebra Stripes, Tim Caro takes readers through a decade of painstaking fieldwork examining the significance of black-and-white striping and, after systematically dismissing every hypothesis for these markings with new data, he arrives at a surprising conclusion: zebra markings are nature’s defense against biting fly annoyance. Popular explanations for stripes range from camouflage to confusion of predators, social facilitation, and even temperature regulation. It is a serious challenge to test these proposals on large animals living in the wild, but using a combination of careful observations, simple field experiments, comparative information, and logic, Caro is able to weigh up the pros and cons of each idea. Eventually—driven by experiments showing that biting flies avoid landing on striped surfaces, observations that striping is most intense where biting flies are abundant, and knowledge of zebras’ susceptibility to biting flies and vulnerability to the diseases that flies carry—Caro concludes that black-and-white stripes are an adaptation to thwart biting fly attack. Not just a tale of one scientist’s quest to solve a classic mystery of biology, Zebra Stripes is also a testament to the tremendous value of longitudinal research in behavioral ecology, demonstrating how observation, experiment, and comparative research can together reshape our understanding of the natural world.
|Publisher:||University of Chicago Press|
|Product dimensions:||6.30(w) x 9.10(h) x 1.10(d)|
About the Author
Tim Caro is professor of wildlife biology at the University of California, Davis. He is also the author of Cheetahs of the Serengeti Plains: Group Living in an Asocial Species and Antipredator Defenses in Birds and Mammals, both published by the University of Chicago Press, as well as Conservation by Proxy: Indicator, Umbrella, Keystone, Flagship, and Other Surrogate Species.
Read an Excerpt
By Tim Caro
The University of Chicago PressCopyright © 2016 The University of Chicago
All rights reserved.
Stripes and equids
1.1 The question of stripes
Zebras are one of the most visually arresting animals in nature because they have contrasting and regular black and white striped coats. They look like no other mammal and have a strikingly different colored coat from the familiar but closely related domestic horse. To most people, they are exceptionally beautiful. As far back as 1824, Burchell, after whom the plains zebra is sometimes named, wrote, "I stopped to examine these zebras with my pocket telescope: they were the most beautifully marked animals I had ever seen: their clean sleek limbs glittered in the sun, and the brightness and regularity of their striped coat, presented a picture of extraordinary beauty, in which probably they are not surpassed by any quadruped with which we are at present acquainted. It is, indeed, equaled in this particular, by the dauw (mountain zebra) whose stripes are more defined and regular, but which do not offer to the eye so lively a colouring" (p. 315).
Outside of Africa, zebras have long been popular curiosities. For instance, Grevy's zebras were brought to ancient Rome to draw chariots in circuses in AD 211–217, and quaggas were used to pull carriages in Hyde Park, London, in the 1800s (MacClintock 1976). Yet despite the animals' attraction, the riddle of why zebras have stripes has never been satisfactorily solved (Cloudsley-Thompson 1999; Ruxton 2002; Caro 2011). Long debated as far back as the nineteenth century by Wallace (1867a, 1879) and Darwin (1871), it has fomented much discussion by other great biologists (Poulton 1890; Beddard 1892; G. Thayer 1909; Mottram 1916; Cott 1940) and keen observers of natural history (Kipling 1902; Selous 1908; Cloudsley-Thompson 1984; Kingdon 1979; Morris 1990). Now, there are many intriguing ideas, but few have been tested experimentally, and it is difficult to take insights from similarly colored species because repeatedly alternating black and white stripes are found in so few vertebrates. Examples include the zebra duiker (see Appendix 1 for scientific names); okapi; some snakes, such as the desert banded snake and California king snake; and fishes, including the zebra shark, zebra moray, and zebra red dorsal. Unfortunately, the adaptive significance of striping patterns in snakes and fishes is also poorly understood (e.g., Seehausen, Mayhew, and Van Alphen 1999; Allen et al. 2013; Kelley, Fitzpatrick, and Merilaita 2013). In short, the reasons that three species of equid have striped pelage have not lent themselves to easy investigation. This book tries to fill that gap.
In this chapter, I first outline the functional hypotheses and associated mechanisms that have been proposed for why zebras have evolved black and white striped pelage. This task has been conducted by others (e.g., Cloudsley-Thompson 1984; Kingdon 1984; Morris 1990; Ruxton 2002; Egri, Blaho, Kriska, et al. 2012), but my purpose here is to make this list comprehensive and recast these ideas into larger functional categories that then enable us to use ecological data to bear on the evolutionary drivers of striping. I then briefly describe the natural history and external coloration of zebras and other equids since many interspecific comparisons will be made in this book, and finally summarize what is known about zebra hair.
1.2 Hypotheses for striping in equids
1.2.a Antipredator hypotheses
By far the most renowned and popular ideas as to why zebras are striped center on stripes reducing the likelihood of zebras being hunted or killed by predators. These come in several guises.
The first notion as to why zebras have stripes is for concealment against predators. Close up and in daylight, zebras' contrasting black and white livery is very conspicuous to the human eye, but at a distance and under low illumination, when predators hunt, zebras might be difficult to see, and early ideas about zebra coloration focused on this. Wallace (1896), the father of the field of animal coloration, remarked, "It may be thought that such extremely conspicuous markings as those of the zebra would be a great danger in a country abounding with lions, leopards and other beasts of prey; but it is not so. Zebras usually go in bands, and are so swift and wary that they are in little danger during the day. It is in the evening, or on moonlight nights, when they go to drink, that they are chiefly exposed to attack; and Mr Francis Galton, who has studied these animals in their native haunts, assures me, that in twilight they are not at all conspicuous, the stripes of white and black so merging together into a gray tint that it is very difficult to see them at a little distance" (p. 220). We now call this type of coloration background matching. G. Thayer (1909) argued that stripes conceal zebras in "reeds and grasses, or even bare-limbed bushes and low trees, or sand streaked with shadows of any of these plants, or quiet water striped with their reflections — its obliterative effect must be almost perfect" (p. 138). It is not clear whether Thayer's purported mechanism was background matching or disruptive coloration where false edges break up the outline of the animal, because he stated, "The stripes ... still play their true obliterative part 'cutting the beast to pieces'" (p. 138). Certainly Cott (1940), in his benchmark and influential book on animal coloration, as well as subsequent authors (e.g., Matthews 1971; McLeod 1987), thought that stripes broke up the continuous surface contour of the animal and thereby masked the margin of the body or the body's appendages; these biologists also subscribed to the idea that zebras were difficult to see at a distance (see also Hingston 1933). Cotton (1998) was of the opinion that stripes might produce a shimmering effect in a heat haze. In addition, Cott and others such as Cloudsley-Thompson (1980) proposed that narrowing of the dark flank stripes and lighter belly acted as countershading, making the body appear flat and difficult to recognize as a prey object (see also Mottram 1916). Thus, there are actually three different mechanisms that have been proposed for striping being a form of crypsis: background matching, disruptive coloration, and countershading.
Darwin remarked, "The zebra is conspicuously striped, and stripes on the open plains of South Africa cannot afford any protection" (Darwin 1906, p. 832). Darwin was likely referring to protective coloration, used in Victorian times in the sense of background matching. Conspicuous coloration, however, can also offer protection in another way by advertising antipredator defenses as Wallace (1896) and Poulton (1890) recognized, and this theme was picked up by other authors. For example, shortly afterward, Selous (1908, p. 22), the infamous big game hunter, wrote, "Never in my life have I seen the sun shining on zebras in such a way as to cause them to become invisible or even in any way inconspicuous on an open plain, and I have seen thousands upon thousands of Burchell's zebras." Similarly, Roosevelt (1910), another hunter and Selous's companion in the bush, described zebras coming down to a waterhole to drink: "They were always very conspicuous, and it was quite impossible for any watcher to fail to make them out" (p. 561), and "Never in any case did I see a zebra come down to drink under conditions which would have rendered it possible for the most dull-sighted beast to avoid seeing it" (p. 561).
In mammals, warning coloration, also called aposematism, usually takes the form of black and white coloration, most memorably in skunks and stink badgers, where it is associated with production of toxic secretions, but it may also advertise other defenses such as quills (Caro 2013). Simply by analogy, then, the black and white external appearance of zebras might advertise dangerous kicks and bites that equids are known to deliver (Matthews 1971; Kruuk 1972) and thereby warn predators not to attack them.
Another constellation of ideas for stripes thwarting predation is through confusing the predator. Several mechanisms have been proposed, any of which might be involved. Possibly stripes might make it difficult to count zebras accurately if the stripes on adjacent individuals appear to form a continuous line, making it difficult to distinguish individuals from one another. Another possibility is that if members of a herd flee together, the stripes on different individuals appear to merge into a single line of black and white stripes. This might make it challenging for a predator to isolate an individual visually and so target its final attack accurately (Kruuk 1972; Eltringham 1979; Morris 1990). Alternatively, stripes might make it difficult to follow a single zebra in a herd that is fleeing erratically. Another form of confusion is that white and black stripes might shimmer and apparently shift, making it difficult for a predator to concentrate on either stationary or fast-moving prey (Morris 1990). Yet another possibility is that stripes cause motion dazzle, defined as "markings that make estimates of speed and trajectory difficult by the receiver" (Stevens and Merilaita 2011, p. 5). Here stripes, vertical, oblique, and horizontal, are believed to interfere with the observer's perception of the speed at which a zebra moves (Morris 1990). Experimental work with objects moving across a computer screen demonstrates that humans perceive zigzag striped patterns as moving more slowly than plain objects (Scott-Samuel et al. 2011; Stevens, Yule, and Ruxton 2008; Stevens et al. 2011; Hughes, Troscianko, and Stevens 2014; but see von Helversen, Schooler, and Czienskowski 2013). Optical illusions could even be involved (see Hall et al. 2016), including the "wagon-wheel effect," where vertical flank stripes generate motion signals in the opposite direction to actual movement, or the "barber's pole illusion," where diagonal stripes on the rump produce motion signals 50°–60° away from the actual movement direction (How and Zanker 2013). A final idea is that stripes running perpendicular to the body's outline cause it to appear larger than similar-sized objects that have stripes running parallel to the body's outline (Cott 1940; Vaughan 1986; Morris 1990) or that vertical stripes cause the object to appear shorter and fatter (Helmholtz  1962). Either effect might confuse the predator and cause it to misjudge the position of the area of the body on which it plans to land, thereby preventing it from making proper contact with prey.
Patterns of striping are different in every individual zebra and offer the opportunity for humans to keep track of an individual in a herd. If predators can do the same and are loath to pursue individuals in good physical condition, then it might be beneficial for individuals in good condition to wear stripes to make sure they can be personally recognized. Under this hypothesis, it is conjectured that stripes are a signal that advertises an individual's quality (Ljetoff et al. 2007), a type of antipredator defense that in other mammals is usually mediated through behavior (Caro 2005).
1.2.b Antiparasite hypotheses
The second major but less well known hypothesis comes from experiments showing that biting flies are less likely to land on black and white striped surfaces than on uniform surfaces or objects of other colors (R. Harris 1930). Females of several biting insect taxa require a blood meal to reproduce and may cause great annoyance while feeding on hosts, including equids. A handful of experimental studies have investigated this. Waage (1981) found that black and white striped boards caught fewer Glossina morsitans and G. pallidipes tsetse flies (glossinids) in the field than all-black boards or all-white boards whether the boards were moving or stationary; and similar results were found for tabanids (horseflies and deerflies). He argued that stripes might obliterate the stimulus of the body edge or reduce the amount of contrast of the animal's form against its background, or else be too narrow to elicit attraction. He believed that attraction from a distance rather than the landing response was influenced by striping. Brady and Shereni (1988) found similar results for Glossina morsitans and Stomoxys calcitrans (stable flies), demonstrating a reduction in landings as stripe number and stripe thinness increased. G. Gibson (1992) showed that tsetse flies were much less attracted to vertically striped and gray targets than black or white surfaces and that horizontally striped targets caught <10% as many flies as any other target. She suggested that horizontal stripes might appear to a tsetse fly to be inconspicuous patches of dark and light, while some edges of the animal perpendicular to the alignment of stripes might be difficult to detect due to absence of lateral inhibition. It may therefore be noteworthy that stripes on all parts of a zebra's body except the forehead lie perpendicular to the outline of the animal's body. Egri, Blaho, Kriska, and colleagues (2012) showed that tabanids are less likely to land on black and white striped surfaces than uniform black or (arguably) white surfaces, that this effect is more marked as stripe width declines, and that the most effective deterrent stripe widths used in their experiments matched the range of stripe widths found on the three species of zebra. They also demonstrated that tabanids are attracted to horizontally polarized light and argued that, due to backscattering, white hair should reflect light with a lower degree of polarization than black or brown hair (Horvath et al. 2008; Horvath et al. 2010). Biting flies transmit several dangerous diseases — most famously tsetse flies transmit trypanosomiasis (sleeping sickness), known to be lethal to domestic horses (Molyneux and Ashford 1983) — so stripes might reduce the likelihood of zebras catching diseases. In summary, there are at least two related ideas here: that stripes impede the landing responses of glossinids, tabanids, or Stomoxys biting flies and that they achieve this by altering the brightness or polarization properties of reflected light.
1.2.c Communication hypotheses
The third major hypothesis for the evolution of striping in equids is that stripes act as markers in the context of social interactions. The first idea is that stripes serve to distinguish zebras from other species. Wallace (1891) noted that "the stripes therefore may be of use by enabling stragglers to distinguish their fellows at a distance." (p. 368), and Darwin (1906), quoting Hunter, remarked that "a female zebra would not admit the addresses of a male ass until he was painted so as to resemble a zebra" (p. 825). Also striping patterns might help zebra species to distinguish one another in areas of sympatry — namely, between Grevy's and plains zebra in northern Kenya, and between plains and mountain zebra in southern Africa — because hybridization can occur. Certainly different patterns of striping on the rump in each species are quite obvious (Morris 1990).
A second idea is that stripes serve to direct allogrooming behavior (mutual grooming) of conspecifics toward the subject's mane, neck, and withers, areas that cannot be reached by the subject itself (Kingdon 1984). Stripes are conjectured to mimic folded skin that appears when the neck of a uniformly colored herbivore is twisted or bent, so stripes might guide a conspecific to these particular areas of the body that are in need of ectoparasite removal.
A closely related idea concerns social cohesion (Kingdon 1979). Allogrooming might promote social bonding as suggested for domestic horses (Kimura 1998) and help keep subgroups together when they aggregate in large herds characteristic of some zebra species (Ruxton 2002). As an offer of support, Kingdon cites observations that zebras come to a halt parallel to each other and in close proximity to each other more than do domestic horses, and that captive Grevy's zebras with their thin stripes prefer to stand next to a panel of fine rather than thick stripes. Stripes, he argued, would be unable to operate in this way in equid species with shaggy winter coats (Kingdon 1984; but see Morris 1990).
Third, striping is believed to foster communication between conspecifics. First, unique striping patterns present on each individual might aid in individual recognition (Darwin 1871; Klingel 1977; Morris 1990). More specifically, patterns on the rump might help other zebras follow one another (Kingdon 1984). Alternatively or additionally, stripes might allow individuals to be clearly seen at a specific distance and so enable them to keep apart (Cloudsley-Thompson 1999).
A fourth idea postulates that some aspect of striping, perhaps stripe thicknesses or brightness of pelage, advertises the condition of the individual that might be used in contest competition or in mate choice.
Excerpted from Zebra Stripes by Tim Caro. Copyright © 2016 The University of Chicago. Excerpted by permission of The University of Chicago Press.
All rights reserved. No part of this excerpt may be reproduced or reprinted without permission in writing from the publisher.
Excerpts are provided by Dial-A-Book Inc. solely for the personal use of visitors to this web site.
Table of Contents
Preface and acknowledgments Chapter 1. Stripes and equids 1.1. The question of stripes 1.2. Hypotheses for striping in equids 1.2.a. Antipredator hypotheses 1.2.b. Antiparasite hypotheses 1.2.c. Communication hypotheses 1.2.d. Thermoregulation hypothesis 1.3. Equid evolution 1.3.a. Plains zebra 1.3.b. Mountain zebra 1.3.c. Grevy’s zebra 1.3.d. African wild ass 1.3.e. Asiatic wild ass 1.3.f. Kiang 1.3.g. Przewalski’s horse 1.3.h. Other equids 1.4. Zebra hair 1.5. Conclusion Chapter 2. Predation and crypsis 2.1. Background matching 2.1.a. Initial discomfort with the idea 2.1.b. Detecting zebras 2.2. Disruptive coloration 2.2.a. Predictions 2.2.b. Sightings at dusk and dawn 2.3. Countershading 2.4. Zebras as seen by nonhumans 2.5. Conclusions Chapter 3. Predation and aposematism 3.1. Aposematism in mammals 3.2. Signaling component of aposematism 3.2.a. Visibility 3.2.b. Noisy behavior 3.3. Defense component of aposematism 3.3.a. Response to predators 3.4. Conclusion Chapter 4. Predation and confusion 4.1. Confusion 4.2. Miscounting numbers of prey individuals 4.3. Striping obscuring outlines of fleeing prey 4.3.a. Lines of stripes shown to humans 4.3.b. Lines of stripes in dangerous situations 4.4. Striping preventing a single prey individual being followed 4.5. Dazzle effect 4.6. Motion dazzle 4.7. Misjudging the size of prey 4.7.a. Subjective and estimated heights and girths 4.7.b. Subjective heights and girths and degree of striping 4.8. Quality advertisement 4.9. Conclusion 4.10. Difficulties with the predation hypothesis Chapter 5. Ectoparasites 5.1. Biting flies 5.2. Behavioral indices of fly infestation in Katavi 5.3. Behavioral indices of fly infestation in Berlin 5.4. Tsetse fly traps 5.4.a. Biconical traps 5.4.b. Cloth traps 5.5. Tabanid traps 5.5.a. Canopy traps 5.5.b. Pelt canopy traps 5.6. Moving objects 5.6.a. Walking in suits 5.6.b. Walking in pelts 5.6.c. Driving with pelts 5.7. Conclusions 5.8. Polarized light 5.8.a. Reflected light 5.8.b. Horvath’s work 5.8.c. Polarization signatures of wild zebras Chapter 6. Intraspecific communication 6.1. Intraspecific signaling 6.2. Species recognition 6.3. Stripes as a facilitator of mutual grooming and social bonding 6.3.a. Allogrooming 6.3.b. Social bonding 6.4. Stripes as a means of individual recognition 6.5. Stripes as an indicator of quality 6.6. Conclusion Chapter 7. Temperature regulation 7.1. Black and white surfaces 7.2. Heat measurements in the field 7.3. Heat management 7.4. Conclusions Chapter 8. Multifactorial analyses 8.1. Comparing hypotheses simultaneously 8.2. The interspecific comparison 8.2.a. Comparative methodology 8.2.b. Overall striping 8.2.c. Striping on different parts of the body 8.2.d. Evaluating the hypotheses 8.3. Conclusions 8.4. The intraspecific comparison 8.5. Concordance on multifactorial analyses Chapter 9. The case for biting flies 9.1. Last man standing 9.2. Host choice 9.3. Ectoparasite population sizes 9.4. Host seeking 9.5. Parasites and diseases transmitted by bloodsucking diptera 9.6. Mechanistic studies 9.7. Further outstanding issues 9.7.a. Multiple functions 9.7.b. Loose ends 9.8. Conclusion Appendix 1. Scientific names of vertebrates mentioned in the text Appendix 2. Nature of wounding seen in African ungulates in Katavi National Park Appendix 3. Families of insects identified in each type of biconical trap color Appendix 4. Families of insects identified in each type of cloth trap color Appendix 5. Photographic sources for comparative analyses Appendix 6. Derivation of zebra phylogenies Appendix 7. Phylogenetic analyses References Index