A Cicada that Ensures Its Fitness during Climate Warming by Synchronizing Its Hatching Time with the Rainy Season

Abstract

A shift in phenology due to climate change is associated with some recent changes in populations, as it can disrupt the synchrony between organisms' requirements and resource availability. This conceptual framework has been developed mostly in systems of trophic interactions. Many coincidental changes, however, are involved in trophic interactions, preventing us from describing the direct impact of phenological shifts on fitness consequences. Here we address the phenological relationship in a simple non-trophic interaction to document a causal process of a warming-driven fitness change in a cicada, Cryptotympana facialis, whose numbers increased dramatically in Osaka, Japan in the late 20th century. We show that synchrony of the rainy season and hatching time may have a substantial influence on hatching success, by 1) shifting the time of completion of embryonic development, and 2) supplying water at various intervals. We estimate the change in hatching time over the last eleven decades (1901-2009) based on meteorological records and the temperature-dependent rate of C. facialis embryogenesis. Our estimate shows that hatching had initially occurred after the rainy season, and that warming had advanced it into the rainy season in the late 20th century. The probability of hatching success was markedly variable, and often very low before this synchronization occurred, but became stably high thereafter. Our findings suggest that the stabilizing effect of this synchrony on fitness was indispensable to the recent population increase of C. facialis.

Spring Temperature Predicts the Long-term Molting Phenology of Two Cicadas,Cryptotympana facialisandGraptopsaltria nigrofuscata(Hemiptera: Cicadidae)

“…Recently, C. facialis has been shown to be increasing as G. nigrofuscata decreases across the most urbanized area of western Japan, Osaka City (Kitamoto 1997, Shiyake 2012. Several previous studies have attributed this compositional shift of the cicada community to the heat island phenomenon (Moriyama and Numata 2011) or to habitat fragmentation combined with avian predation (Takakura and Yamazaki 2007).…”

“…Humidity is also important for the hatching rate of C. facialis and G. nigrofuscata (Moriyama and Numata 2010). Thus, in conjunction with the desiccation dependence of egg hatching, warming influences cicada fitness by synchronizing the hatching phenology of C. facialis (Moriyama and Numata 2011). However, the extent to which these climate variables explain long-term phenology and population fluctuation remains insufficiently understood.…”

Gene duplication and the environmental regulation of physiology and development

“…For instance, seeds or eggs can be highly resistant to dessication, while young seedlings and hatchlings can be highly vulnerable to it. Therefore, the seasonal timing of germination or hatching can be under strong natural selection (Fernandez-Quintanilla et al 1986;Jones et al 1997;Purrington and Schmitt 1998;Seiwa 1998;Visser and Holleman 2001;Donohue 2002;Shimono and Kudo 2003;Donohue et al 2005;Castro 2006; Benard and Toft 2007;van Asch et al 2007;Weekley et al 2007;Watanuki et al 2009; Moriyama and Numata 2011;reviewed in Donohue et al 2010). The ability to restrict such developmental transitions to occur only under specific combinations of permissive environmental conditions can determine life or death.…”

Ecophysiological responses to climate change in cicadas

“…Experimental shifts of potential hatching time windows of C. facialis confirmed a strong influence of synchrony with rainy seasons on their fitness. The hatching rates dropped to approximately 10% in the mid‐summer dry season, whereas they were approximately 70% in the rainy season (Moriyama & Numata, ). Estimation of the hatching time in the past clearly illustrated the process of how warming improved the synchrony of hatching time and rainy season in C. facialis (Fig.…”