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Colors of Doom: What does the tsetse see?

Alexander Fuentes

Stanford University

Parks and People: Dilemmas of Protected Area Conservation in East

Sophomore College 2017

October 18, 2017

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Introduction

Tourists are often warned to beware exhibiting the colors of blue or black if traveling to the tsetse-infested areas of Sub-Saharan

Africa, as these colors may summon the voracious Glossina, also known as the . Amidst the kingdom, many tourists will notice the savannas are occasionally adorned with royal blue and black textiles. In fact, these “flags” are tsetse fly traps, decorated with the “colors of doom” that the tsetse fly is presumed to be most attracted to. Are these colors truly dangerous to display in Figure 1. A tsetse fly trap. the grasslands, or is merely legend?

Background

Glossina prefer to dwell in bushes and during the dry season reside in shaded wooded areas. According to the World Health Organization, there are 29 to 31 species and sub-species of tsetse. Like house , tsetse flies are 8 to 17 millimeters long, but the tsetse fly is distinguishable in that it folds one directly on top of the other in a scissor-like fashion. The tsetse also possesses a long, branched proboscis that extends forward. Tsetse flies are unique vectors in that both the male and female bite. They feed during the day on bloodmeal, with a predilection for swine, and buffalo. The tsetse relies heavily on visual and olfactory cues to find its prey.

The tsetse fly is the primary for African , also known as African sleeping sickness. is caused by two parasite species: brucei gambiense and rhodesiense. T.b. rhodesiense is also known as East Fuentes 3

African sleeping sickness, and T.b. gambiense as West African sleeping sickness (Word Health

Organization). The gambiense form of African Trypanosomiasis is responsible for 98% of sleeping sickness epidemic cases. The rhodesiense form is found in eastern and southern

Africa and affects mostly livestock and wildlife, with only being accidentally infected; rhodesiense has been responsible for large outbreaks in the past, however, and this form of the is much more rapid and acute (Franco, et al. 2014).

This paper will focus on the tsetse flies in and nearby countries in . The tsetse species I will focus in my analysis include G. pallidipes, G. swynnertoni, and G. morsitans. The geographic distributions of these tsetse are as follows: G. pallidipes most oftenly reside in Tanzania, , , , and ; G. swynnertoni in Tanzania and

Kenya; and G. morsitans in Tanzania, , and Zimbabwe.

Impact on Parks and Peoples

The tsetse fly is a prominent vector of

African trypanosomiasis, also known as African sleeping sickness, a disease endemic to Tanzania (see Figure 2).

Trypanosomiasis is a threat to more than 60 million people throughout

Africa.

Figure 2. Human African Trypanosomiasis is endemic to Tanzania and demarcated by climatic restrictions. Fuentes 4

Historically, the distribution of pastoralist communities has been shaped by the tsetse. As illustrated in Figure 2, many of the tropical and eastern regions of Africa are tsetse-infested. In these areas, local people have adapted non-milking practices as the cattle would be infected by sleeping sickness and fail to produce or reproduce. "A belt defined by tsetse flies" would be created in which it would not be economical to raise cattle (Durham B 2017). Because the tsetse fly is dependent on specific climatic and temperature restrictions, the disease itself has also been restricted between the “14th latitude north and the 29th latitude south on the African continent” (“African Trypanosomiasis”).

In a study sampling eight sites in the

Ngorongoro Crater Conservation Area, of 193 livestock, 47 % of cattle, 91.7 % of sheep, and Figure 3. Impact of cattle distribution in tsetse 60.8 % of goats were found to harbor a form of infested areas (“Tsetse fly costs agriculture billions every ”). the Trypanosoma brucei parasite (Ruiz et al.

2015). Local sheep and goats in East Africa were found to be carriers of the T. brucei rhodesiense subspecies, which causes acute human trypanosomiasis (Ruiz et al. 2015). Most of these sampled belonged to pastoralist (Maasai) herdsmen.

The parasite, after invading the and - barrier, has vast neurological effects on its victims. Symptoms of sleeping sickness in humans and animals may include intermittent fever, swollen lymph nodes, and aching muscles and joints in the first stages of the Fuentes 5 disease. The disease culminates in progressive mental deterioration, ataxia, a disturbed sleep schedule, and finally if untreated.

Beyond Human African trypanosomiasis’s direct effects on people, both human and animal are detrimental to the economic viability and the nutritional potential of human populations, decreasing the overall welfare in endemic regions. In Tanzania, tsetse flies pervade about one-third of the 940,000 square miles mainland, accounting to a loss of approximately 4.75 billion USD in agricultural potential (Ruiz et al. 2015). According to the World Health

Organization, the parasite is detrimental to both agricultural development and cattle rearing.

Trypanosomiasis’ impact is especially critical because of globalization, deforestation, climate change, and loss of blood meal species. Domesticated livestock are becoming a prominent target for the tsetse (Ruiz et al. 2015). In summary, African trypanosomiasis has a very significant influence on both parks and people, and on shaping the boundaries and economic and health prospects of the continent of Africa. Thus, to mitigate the increasing impact of African trypanosomiasis, it is important to understand the mechanics of the disease’s primary vector, and incorporate effective community-based strategies into and policy.

Hypotheses

In this paper I will investigate three hypotheses:

1) The tsetse fly is attracted to dark colors, especially blue and black. Also, the tsetse fly is least attracted to lighter colors of green and yellow.

2) Animals with dark colors suffer higher rates of tsetse bites than animals with lighter colors. Fuentes 6

3) The tsetse fly is repelled from black and white stripes, such as those of the , because the stripes may create an optical illusion to the flies.

The second hypothesis follows from the first hypothesis, for if tsetse flies are attracted to darker colors generally, then one would expect animals with dark colors to endure more tsetse bites.

Research Question

This paper will investigate the question: what colors and patterns are the tsetse fly attracted to and repelled from, and how can this knowledge be used to mitigate the impact of African trypanosomiasis on people, livestock, and wildlife?

Methods of Hypothesis #1

Hypothesis 1: The tsetse fly is attracted to dark colors, especially blue and black, and least attracted to lighter colors of green and yellow.

When travelling longer distances of up to over 90 meters, tsetse flies are guided by chemical

(olfactory) cues to find their blood meal. These include cattle odors, , and urine.

Once within closer range to their hosts, the tsetse relies on visual cues, such as shape, size, movement, contrast vs background, color, pattern (Mehlhorn, 2008).

The most attractive color to the tsetse fly is royal blue, with a high reflectivity at 650 nm (mid blue) and low ultraviolet reflectivity. Generally, the attractiveness of a surface is increased by blue and red reflectivity, and diminished by ultraviolet and green-yellow reflectivity (Mehlhorn,

2008). The correlation between color and tsetse fly attraction can be observed in a Zimbabwe Fuentes 7 study, in which colored fabrics and paints were measured using an ultraviolet spectrophotometer to create tsetse traps with 53 different colors (Green, C. H., and S. Flint, 1986). Each trap is a cube of 90 cm side, with the entrance at the base of one side along with a cloth cover (see Figure

4). These traps were positioned 100 m apart from one another. The color of the cloth in each trial is manipulated as the independent variable. The dependent variable is the “trap score,” or the percent of flies trapped in the cubes.

Colors were selected based on their reflectivity between 300 and 700 nanometers. Paint was added to specific colored fabrics that reflected specific color radiations. The reflection of blue on the electromagnetic spectrum could be made by mixing paints that reflected more visible blue light (Green, C. H., and S. Flint, 1986).

Figure 4. Isometric view of cubed tsetse fly trap (Green, C. H, 1988).

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Figure 5. The relationship between blue reflectivity and trap score was further investigated using a color series made by mixing white and yellow paints, since white Brigh and yellow differ mainly in their blue reflectivity (Green, C. H., and S. Flint. 1986). Here, the lowercase letters represent a spectrum of white and yellow colors (a = most t

white and g = most yellow) in which whiter pigments have higher blue reflectivity. royal blue emerged as the “best” trap material. Green and yellow had the lowest trap scores and were considered unattractive to the tsetse (Green, C. H., and S. Flint. 1986).

Another study investigating the optimization of the color and fabric of tsetse targets found that the best blue targets attract three times the amount of tsetse because of the cloths’ UV reflectance levels. “Hence selecting fabrics for use in targets must be based on spectral analysis of the fabrics' reflectance across the spectrum visible to tsetse.” In other words, certain pigments of blue make more attractive targets, and this nuance in color variation should be considered when creating tsetse fly traps (Lindh, J.M., et al. 2012).

Results of Hypothesis #1 Fuentes 9

Evidence supports the hypothesis, but with royal blue as the most attractive color to the tsetse, and blue and black as the prime colors for the tsetse fly. Yellow and green are the least attractive colors for the tsetse. Furthermore, studies have also found that blue attracts the tsetse fly and solid black entices it to land (“Catching Tsetse”). This insight into the drivers of the tsetse fly may be useful in conjunction with scented lures to entice tsetse flies in traps that may sterilize or exterminate them, thus reducing tsetse populations.

Methods of Hypothesis #2

Hypothesis #2 - Animals with dark colors suffer higher rates of tsetse bites than animals with lighter colors.

A 2016 study at National Park quantified tsetse feeding preferences from

304 G. swynnertoni and 89 G. pallidipes abiding in wilderness areas rich in potential hosts

(Auty, et al. 2016). The most common bloodmeals for G. swynnertoni were the

(94/220), buffalo (48/220) and giraffe (46/220). Meanwhile, G. pallidipes favored the buffalo

(26/46), giraffe (9/46) and elephant (5/46). In the study, Thomson’s gazelle, the zebra and the wildebeest were not fed on by the Glossina swynnertoni tsetse flies. Similarly, G. pallidipes did not feed on the impala, Thomson’s gazelle or wildebeest (Auty, et al. 2016). In general, some wild animals (kob, zebra, wildebeest, oryx) are rarely, if ever, bitten by tsetse flies, possibly because their colors are less attractive (Franco, et al. 2014). Fuentes 10

Figure 6. Percentage of tsetse blood meals for (a) Glossina swynnertoni out of 220 sample animals (Auty, et al. 2016).

Figure 7. Percentage of tsetse blood meals for (b) Glossina pallidipes out of 46 sample animals

(Auty, et al. 2016).

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Below are visuals of the wildlife found least attractive to tsetse.

Thomson’s Gazelle (top left). Kob (top right). Impala (bottom left). Wildebeest (bottom right).

The zebra is also one

of the least attractive

animals to the tsetse. Fuentes 12

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Some of the most attractive animals to the tsetse were the hippopotamus, elephant, giraffe, and buffalo. Most of the more tsetse-attractive animals are darker-skinned. The giraffe is a clear outlier, however. However, these animals on average have a greater surface area, and are less agile, which may make them more easily targets for the tsetse fly.

Many , such as the Tanzanian starlings, or the lilac-breasted roller, have bright blue that should theoretically attract the tsetse. The vervet monkey also has a vivid blue scrotum that varies in color salience depending on the monkey’s social rank (Wolff, K. et al. 1976). However, animals smaller than a porcupine are not usually fed upon by tsetse flies in the wild, this includes most birds (“Feeding Habits of Tsetse Flies”). Instead, blood from large (buffalo, elephant and giraffe) were a significant component of the tsetse fly diet. These larger mammals have greater surface areas that may likely make them more vulnerable to the tsetse. Moreover, very active animals such as monkeys are also not fed much upon, possibly because they are more able to kill biting flies (“Feeding Habits of Tsetse Flies”).

Results from Hypothesis #2 Fuentes 14

If tsetse flies are more likely to be attracted to darker colors such as blue and black, as well as bright royal blue, then do darker colored animals suffer higher rates of bites? Some lighter colored wildlife animals such as the Thomson’s gazelle, kob, and impala have lower rates of being targeted by the tsetse. Though there may be a possible correlation, outliers such as the giraffe bring into question the validity of the hypothesis. A future study would need to further test this hypothesis with an objective measure of “lightness” and “darkness” of animal color, as well as investigate the role of surface area and tsetse susceptibility. Furthermore, other factors that may contribute to more bites from the tsetse, such as larger animals possessing a larger surface area, should be considered in a further study. In addition, behavioral traits that may hinder tsetse bites, such as the vervet monkey’s greater ability to kill biting flies, should also be investigated in future study. Though color may very likely play an important role in tsetse attraction (Auty, et al. 2016), current data are inconclusive to support the hypothesis that darker colored animals receive higher rates of tsetse bites.

Methods for Hypothesis #3

Hypothesis #3 - The tsetse fly is repelled from black and white stripes, such as those of the zebra, because the stripes may create an optical illusion to the flies.

“The most longstanding hypothesis for zebra striping is crypsis, or camouflaging, but until

now the question has always been framed through human ” -Amanda Melin, zebra stripe

researcher and assistant professor of biological anthropology (Bailey 2016).

Melin study challenges the human-centric concept that have stripes for , suggesting that zebras may have evolved black and white stripes to repel the tsetse fly. Current hypotheses for the function of zebra stripes include thermoregulation, social interaction, predator Fuentes 15 avoidance, and avoiding ectoparasite attack (Caro 2014). The question remains, why do zebras have stripes, and how might this evolutionary have been influenced by the tsetse fly?

Here I will be focusing on the impact of ectoparasite attack on the zebra. The tsetse fly, an ectoparasite, can inject animal and human trypanosomiasis through its painful bite. Modern-day

A lion rests in an acacia tree in Tarangire National Park (September 15, 2017). Lesikar, a local guide, affirms that one reason the lions climb the tree is to avoid tsetse flies. wildlife in Tanzanian national parks have evolved adaptive behaviors in part to avoid or ward off tsetse fly. For example, in Tarangire National Park, Tanzania, lions perch on trees, partly to avoid flies (Lesikar, personal communication, 2017). Similarly, ostriches may flap their wings to ward off tsetse flies (Jackson, personal communication, 2017).

In a 1992 Zimbabwe study, tsetse flies were shown to avoid horizontal black and white striped targets (Gibson, et al. 1992). Vertical stripes were much less attractive to the tsetse than solid black or white surfaces (Gibson, et al. 1992). On average, striped models caught significantly fewer tsetse and other flies than solid black or white models (Waage 1981). An important study Fuentes 16

in the field of zebra stripe research found that black and white striped models caught fewer

Glossina morsitans and G. pallidipes in the field than black or white models whether moving or

stationary (Caro 2014). Few flies of either species (G. morsitans and pallidipes) landed on or

even circled the horizontal stripes (Caro 2014). The study also presented a correlation between

the boldness of stripes in various zebra species and the predominance of tsetse flies in their

natural habitat (Caro 2014).

Wildlife biologist Tim Caro chronicles in his book, Zebra Stripes, his own field research in

which he strode through zebra territory in a black-

and-white striped suit. Caro counted the number of

tsetse that bit him, discovering that fewer flies bit

him as he wore zebra stripes than when he wore

darker wildebeest pelt.

Left. Caro sporting a black-and-white zebra striped suit as he walks across zebra territory, counting the tsetse that bite him.

Top and bottom right. Caro comparing the effects of wearing zebra skin to wildebeest skin on tsetse bites. Fuentes 17

Figure 8. As the map below shows, striping is most abundant in places where biting flies and equids live together.

One hypothesis mentioned in Caro’s book, Zebra Stripes, for how the stripes may repel the tsetse is through optical illusion, namely the wagon-wheel effect or the barber's pole illusion, in which the stripes appear to be moving opposite of the animal's actual movement direction.

Gibson also suggested that horizontal stripes might appear to a tsetse fly to be inconspicuous patches of dark and light, while the edges of the animal perpendicular to the alignment of stripes might be difficult to detect because of the absence of lateral inhibition

(Gibson, et al. 1992). Lateral inhibition is the “characteristic pattern of connections among neurons in the eyes of most animals,” and helps to explain the phenomena of optical illusions

(Grobstein). Fuentes 18

Figure 9. Optical illusion: The barber pole may appear to move only downward or rightward only when it is in fact rotating rightward and downward along an axis.

Results for Hypothesis #3

Research supports the hypothesis that black and white stripes do not attract and may even repel the tsetse which may have had evolutionary benefits for the zebra. Because the tsetse relies heavily on visual cues, it is plausible that the zebra’s stripes create an optical illusion that confuses and repels the tsetse.

Conclusions

My first hypothesis investigated what specific colors the tsetse is attracted to, and found that specific colors (bright royal blue, dark blue and black) are most attractive, and green and yellow are the least attractive. Studies testing different colored pigments in tsetse fly traps supported my first hypothesis. The results led into my second hypothesis, which explored whether darker colored animals are more attractive to the tsetse than lighter colored animals. Evidence for the hypothesis was overall inclusive, with further research needed to factor in animal surface area (in that bigger land animals are easier targets than smaller animals), behavior (e.g. defensive strategies, such as kicking and -flicking, which could deter tsetse flies) and other traits that could attract or repel the tsetse fly. Finally, through my third hypothesis I found consistent Fuentes 19 evidence that striped patterns repel the tsetse, specifically black and white stripes such as those of the zebra. I hypothesized that tsetse deterrence may be due to the tsetse stripes confusing the tsetse through creating an optical illusion. While current evidence supported this claim, I would also like to test other hypotheses as to why stripes repel the tsetse fly.

Recommendations and Future Directions

In general, it is recognized by international and national organizations that a reduction of the tsetse population will also mitigate the rates of trypanosomiasis transmission.

Thus, insight into the mechanics of what attracts and repels the tsetse fly can offer significant leverage into mitigating the impact trypanosomiasis on people, livestock, and wildlife. One creative recommendation for repelling the Could zebra print be both a stylish tsetse fly is investigating the use of zebra striped and effective bug repellent? clothing or textiles in areas with high tsetse density. Picture courtesy of Alibaba.com

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A potential solution to eradicate the tsetse fly (picture courtesy of Thomson Safaris).

Though tsetse fly traps, in conjunction with odor baits, may serve as effective tools to eradicate or sterilize tsetse flies, simply adding more traps may not be enough! Public health initiatives and disease control strategies should work in collaboration community stakeholders such as

Tanzanian Maasai communities and local people. A 2005 report published by the World Health

Organization cites the role of community involvement in Uganda, , and which has helped communities be more proactive rather than reactive of sleeping sickness epidemics.

Preventative measures can help minimize economic and health costs in tsetse-vulnerable communities, for these costs can be immense during disease outbreaks. Thus, one potential recommendation for combatting trypanosomiasis involves finding strategies to educate people in the disease and , as well as on how to manufacture, manage, and replace traps.

Finally, additional research could be conducted to see if lighter-skinned colored cattle may be Fuentes 21 less susceptible to the tsetse; these results could have meaningful implications for pastoralist communities and local people in countries affected by trypanosomiasis.

Acknowledgements

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I would like to thank Dr. William Durham and Dr. Susan Charnley for their continuous support to my academic and personal growth, and for encouraging me to pursue a career in academia.

Thank you to the exceptional Sophomore College Assistants Lauren Killingsworth and Antariksh

Mahajan for their moral and scholastic support. Special thanks to Mrs. Marsha Bramowitz and

Mr. Stuart Yusem for providing tsetse samples for my research. Big thank you to the eight

Hoopoe Safaris guides Joyful, Jackson, Muro, Joseph, Lesikar, Aaron, Elias, and Clemence.

Thank you to all the wonderful Stanford alumni, my Sophomore College peers, and to Norm

Robinson for helping organize the travel-study course for which I could conduct my research.

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