Mate-guarding male desert locusts act as parasol for ovipositing females in an extremely hot desert environment

Abstract

The desert locust, Schistocerca gregaria, is an infamous transboundary pest. Although many desert-inhabiting ectotherms are nocturnal to avoid lethal hot temperatures, desert locusts move diurnally in the world's most extreme thermal environment, Sahara Desert (Magor et al., 2008; Uvarov, 1977). It is difficult for locusts to survive in such harsh environments; however, their adaptive strategies have been understudied due to lack of field studies (Cullen et al., 2017; Maeno et al., 2019, Maeno, Piou, Kearney, et al., 2021).

During field observations over 10 years on these locusts (Maeno et al., 2019, 2023; Maeno, Piou, Kearney, et al., 2021; Maeno, Piou, Ould Ely, et al., 2021), we noticed that gregarious-behaving desert locust females began to aggregate and oviposit after sunset when the ground temperature (T_g) decreased (Maeno, Piou, Ould Ely, et al., 2021). We can easily understand that this behavior is adaptive because the ground temperature at night is not a risk factor for thermal constraints and because predation pressure could be low. However, some delayed-laying females began to lay eggs the following morning. These individuals were exposed to extremely hot conditions, with T_g beyond 50°C, which many insects cannot tolerate (Figure 1a,b) (Heinrich, 1999). Female desert locusts generally lay eggs underground by extending their abdomen (Uvarov, 1977). As oviposition takes a few hours (mean + SE: 143 + 8 min (range 93–192 min), n = 14), immobile ovipositing females could not use common behavioral thermoregulatory strategies for cooling and were exposed to lethal thermal conditions; this raises the question of how ovipositing female locusts cope with adverse hot conditions. Even the Sahara silver ant, Cataglyphis bicolor, which is known as the most heat-tolerant insect (up to 55.1°C), frequently perches on plants and runs for cooling (Pfeffer et al., 2019). The mechanisms by which ovipositing female locusts avoid overheating remain unknown. To address this, we conducted field observations and experiments in Mauritania in 2013, 2016, and 2022.

During these field surveys, we observed daytime oviposition following nighttime group oviposition at a sandy and clay grounds site. During daytime (10:00–15:00), the majority of ovipositing females were mounted by males (2013: 96.8%, n = 439; 2016: 89.3%, n = 28; 2022: 95.6%, n = 206). These observations coincide with high rates of mate-guarded females during the night (Maeno, Piou, Ould Ely, et al., 2021). Mate-guarding males mounted the back of ovipositing females, exposing themselves to solar rays while maintaining a distance from the ground (Figure 1a). When the temperature increased, the ovipositing pairs oriented themselves parallel to the Sun's rays (Figure 1b). A similar thermal orientation was observed for marching gregarious nymphs and sexually matured lekking males on the hot ground (Maeno et al., 2023; Maeno, Piou, Kearney, et al., 2021). Thermal images were recorded using an infrared thermal camera. Thermography images showed that during the day, the body temperatures (T_b) of the ovipositing pairs' were significantly lower than T_g (Figure 1c and Appendix S1: Figure S1). In contrast, T_b was higher than T_g at night when the temperature was the lowest (Figure 1d; Appendix S1: Figure S1). Freely mobile copulating pairs maintained a low T_b by moving under the shade at midday (Appendix S1: Figure S1). These results indicated that mate-guarded ovipositing females could avoid overheating even under lethally hot conditions.

Mate guarding is generally considered the physical guarding of a female to deny rival males the opportunity to mate with her and is one of the most commonly used defensive strategies observed in various taxa, including mammals (Nichols et al., 2010), birds (Birkhead, 1979), fishes (Alonzo & Warner, 2000), lizards (Cooper, 1999), and insects (Shuker & Simmons, 2014). Our results imply that mate guarding by males may also cool the females.

Accordingly, we hypothesized that mate-guarding males served as a “parasol” to prevent females from overheating. To test this “parasol hypothesis,” either single or mating-postured pairs were tethered on exposed ground at midday, and their T_b was continuously monitored in the field using a multichannel thermopair logger (Appendix S1: Figure S2). Although T_g exceeded the critical thermal maximum (CT_max) of 54.7°C (Maeno et al., 2023), T_b was significantly lower in mate-guarded females than in single females (Tukey–Kramer honestly significant difference [HSD] test, p < 0.05). Mate-guarding males also maintained a lower T_b than single males (Tukey–Kramer HSD test, p < 0.05). These results suggest that both sexes of the mating pairs could cool without shading. Females lay eggs 2–15 cm underground (Uvarov, 1977). Even just 1 cm underground, the temperature was approximately 6°C lower than that at the ground surface; thus, ovipositing females may also be cooled by their extended abdomen. Our Sun exposure experiments did not replicate this effect; thus, our results may be overestimated, and the T_b of freely ovipositing females may be lower in live animals.

Desert locusts have a relatively high physiological heat tolerance and regulate their temperature by altering their posture and microhabitats (Maeno et al., 2023; Maeno, Piou, Kearney, et al., 2021). Furthermore, we found that the immobile ovipositing pairs employed various behavioral solutions often associated with mate guarding, including temporal Sun shields (i.e., mating males), conductance from substrate, and minimization of the body surface exposed to the Sun. Parasol-like morphological structures may obstruct the animals' movements; thus, mate-guarding males are convenient temporal Sun shields for highly mobile desert locusts (Figure 2). These results suggest that mate guarding can mitigate extremely hot conditions and contribute to expanding the use of ecological niches.

It is hoped that identifying times when desert locust are inactive and intensively spraying pesticides will lead to environmentally and health-conscious pest control that does not use more pesticides than necessary. Spraying pesticides on locusts while the male is riding on the female's back to avoid overheating may be effective for control.

This thermal adaptation could allow desert locust to adapt to future climate change. It would be interesting to know how mate-guarding behavior has evolutionarily shaped the thermoregulatory strategies of other locusts and insect species in other locations and seasons.

Koutaro Ould Maeno designed and performed the research, analyzed the data, and wrote the paper. Sidi Ould Ely, Sid'Ahmed Ould Mohamed, Mohamed El Hacen Jaavar, Ahmed Salem Benahi, and Mohamed Abdallahi Ould Babah Ebbe reviewed the final manuscript and organized field surveys.

The authors declare no conflicts of interest.