Temperature‐related breakdowns in the coordination of mating in Enchenopa binotata treehoppers (Hemiptera: Membracidae)

Abstract

Temperature influences the expression of a wide range of behavioral traits in ectotherms, including many involved in the initiation of pair formation and mating. Although opportunities to mate are thought to be greatest when male and female activity overlap, sex‐specific behaviors and physiology could result in mismatched thermal optima for male and female courtship. Here, we investigate how conflicts in the thermal sensitivity of male and female courtship activity affect patterns of mating across temperatures in Enchenopa binotata treehoppers (Hemiptera: Membracidae). These plant‐feeding insects coordinate mating with plant‐borne vibrational signals exchanged in male–female duets prior to pair formation. We manipulated temperature across an ecologically relevant range (18–36ºC) and tested the likelihood of individual male and female E. binotata to engage in courtship activity using vibrational playbacks. We then staged male–female mating interactions across the same temperature range and quantified the thermal sensitivity of mating‐related behaviors across stages of mating. Specifically, we measured the timing of duetting, the likelihood for key pre‐copulatory behaviors to occur, whether the pair mated, and copulation duration. We found sex‐specific thermal sensitivity in courtship activity: Males showed a clear peak of activity at intermediate temperatures (27–30ºC), while females showed highest activity at the hotter thermal extreme. Mating rates, courtship duets, and copulatory attempts were less likely to occur at thermal extremes. Also, duetting occurred earlier and copulation was shortest at higher temperatures. Overall, our data suggest that sexes differ in how temperature affects mating‐related activity and some processes involved in mate coordination may be more sensitive than others across variable thermal environments.

Effect of short-term exposure to high temperatures on reproductive behaviors and physiological enzyme activities in Zeugodacus tau

“…The mating rates in the treatment -control and controltreatment combinations were the highest at 38°C and 34°C, respectively, and the thermal sensitivity of the mating behavior of males was higher than that of females. Leith et al (2020) have also reported sexspeci c thermal sensitivity in the courtship activity of Enchenopa binotata. The authors reported that the males of this species exhibited a distinct peak of activity at moderate temperatures, while the females exhibited the greatest activity at the hot thermal extreme.…”

“…Such behavioral adaptation strategies for survival during adverse environmental stresses are also reported in other insects, such as hormesis and stimulated parasitic behavior induced in Encarsia formosa upon exposure to sublethal concentrations of spirotetramat (Yang et al, 2021), the increased courtship and heightened copulation behavior observed in Trichogramma chilonis exposed to an insecticide (Wang et al, 2020), etc. Temperature is also reported to in uence the expression of a wide range of behavioral traits in ectotherms, including several traits involved in the initiation of pair formation and mating (Leith et al, 2020). In the mating process of fruit ies, the male insects exhibit a series of courtship behaviors to attract females, while a high proportion of female insects refuse to mate (Shelly, 2001;Aquino and Joachim-Bravo, 2014).…”

“…Moreover, insect behavior and physiology differ between male and female members, particularly in terms of thermal sensitivity and physiological enzyme activities (Brandt et al, 2018;Macchiano et al, 2019). Consequently, when the environmental temperature changes, females and males may exhibit mismatching behaviors in most actively seeking or being receptive to potential mates (Leith et al, 2020). In this context, the present study hypothesizes that an increase in the ambient temperature would cause Z. tau to adopt different mating behavior strategies and physiological response mechanisms to adapt to the high-temperature stress, the mating activity patterns, and physiological metabolism exhibited by female and male insects at the same high temperature were different.…”

Harvesters (Arachnida: Opiliones) mate more at cooler temperatures, but the effect of temperature on mating varies across years

“…Behavioral processes at all stages of mating change with temperature as a result (Leith et al, 2021). In the precopulatory stages, temperature affects the likelihood of individuals engaging in a precopulatory activity—an important prerequisite for mating in many animals—with the highest activity often occurring at intermediate temperatures (Brandt et al, 2018; Eberhard et al, 2019; Leith et al, 2020; Macchiano et al, 2019). Thus, the likelihood of mating to occur also often peaks at intermediate temperatures (Huey & Stevenson, 1979; Leith et al, 2020; Leith et al, 2021) with notable exceptions (Brandt et al, 2018).…”

“…In the precopulatory stages, temperature affects the likelihood of individuals engaging in a precopulatory activity—an important prerequisite for mating in many animals—with the highest activity often occurring at intermediate temperatures (Brandt et al, 2018; Eberhard et al, 2019; Leith et al, 2020; Macchiano et al, 2019). Thus, the likelihood of mating to occur also often peaks at intermediate temperatures (Huey & Stevenson, 1979; Leith et al, 2020; Leith et al, 2021) with notable exceptions (Brandt et al, 2018). Ambient temperature also affects copulation duration: copulation duration is often longest at colder temperatures (Brandt et al, 2018; Costa & Sotelo, 1984; Jiao et al, 2009; Katsuki & Miyatake, 2009; Leith et al, 2020; Michiels, 1992; Vasudeva et al, 2018; Yenisetti et al, 2006).…”