Discussion
We demonstrated that male cicadas lost body mass, increased calling activity and moved to open habitats (narrow-leafed plants) with age. Such integration of age-related plasticity resulted in negative within-individual covariations between states (body mass) and risk-taking behaviours. This pattern may be attributed to the combined effects of asset protection and energetically demanding mate calling. The age-related decrease in body mass might be due to age-related increase in calling efforts, and the age-related increase in risk-taking behaviours might be due to decreased future fitness expectations with age. Moreover, the integration of age-related plasticity in T. isshikii implies that T. isshikii exhibits a capital breeding reproductive strategy.
Considering the age-related increase in calling activity, physiological deterioration may not occur in wild cicadas, although this remains uncertain. This age-related increase in calling activity might be due to the immaturity of younger males, who are not yet capable of producing calls. However, a quadratic ageing pattern was not evident in male calling activity, as the increased calling activity did not decline with age. This suggests that the changes in calling activity are not due to physiological deterioration. Nevertheless, the possibility of physiological deterioration cannot be entirely dismissed. Despite thorough searches of the habitat, it is possible that non-calling older males were missed, potentially biasing the analysis of age-related changes in calling activity. For instance, a non-linear ageing pattern in calling behaviour might exist, but our study could fail to detect it if non-singing old males were overlooked during our observations.
The age-related increase in risk-taking behaviour among male T. isshikii can be explained by the asset protection principle (Clark 1994). In the analysis of plant use, males were found in narrow or small-leafed plant species with age. Considering that plants provide shelters, T. isshikii may safely hide in large-leafed plants when they were young adults. As male cicadas age, they may prefer staying in narrow-leafed plants to increase body temperature and calling activity, actively advertising their locations to females. Therefore, following the asset protection principle, male cicadas stay in large-leafed plants to maximise protection with no courtship activity during early adulthood, while they move to narrow-leafed plants and actively seek mates during late adulthood. These behavioural strategies likely maximise the reproductive success of male cicadas during their short reproductive periods.
The age-related decrease in body mass among cicadas might be attributed to the stress from repeated net captures as well as the age-related increase in the energetically demanding calling activity. Although we minimised disturbance by quickly confirming their identity before release, the repeated netting could still potentially contribute to a decline in body mass over time. Moreover, if the stress from repeated captures and the principle of asset protection are both active, this stress could reduce body mass and subsequently lead to increased risk-taking behaviours. Therefore, we cannot completely rule out the possibility that our collecting methods may influence the ageing process of cicadas, potentially affecting the within-individual correlations between body mass and risk-taking behaviours.
Instead of the role of stress in shaping within-individual correlations between body mass and risk-taking behaviours, the age-related decrease in body mass and increase in risk-taking behaviour in male cicadas may imply the resource allocation strategies for reproduction. There are two extreme resource allocation strategies according to the timing of reproduction: capital breeding and income breeding (Jönsson and Jonsson 1997; Drent and Daan 1980). Capital breeders accumulate resources before the reproductive period and utilise them during reproduction, while income breeders depend on current resource acquisition during reproduction (Jönsson and Jonsson 1997). Considering the continuum from pure capital breeding to pure income breeding, many insect species lean towards being income breeders. Although larval nutritional conditions influence adult phenotypes and life history (reviewed in Scriber and Slansky 1981; Awmack and Leather 2002; Han and Dingemanse 2015; Koyama and Mirth 2018), many insects consume macronutrients during the reproductive period and use resources acquired during the adult stage directly for reproduction (i.e., income breeders). Some insect species are recognised as capital breeders (Tammaru and Haukioja 1996; Boggs 1997; Kemp and Alcock 2003; Casas et al. 2005; Johnson 2006; Bauerfeind and Fischer 2008; Rhainds et al. 2008; Pöykkö 2009; Davis et al. 2016), but cicadas have not been extensively studied in this context.
Cicadas do not strictly adhere to a pure capital breeding strategy because they are known to consume a substantial amount of xylem sap as adults (Cheung and Marshall 1973). Both nymph and adult cicadas feed on xylem (Brown and Chippendale 1973; Cheung and Marshall 1973; WHITE and STREHL 1978), which contains mainly water (99%) but includes nutrients such as carbohydrates, amino acids, and proteins at very low concentrations (Satoh et al. 1992; Dafoe and Constabel 2009). Water intake may be the primary aim of adult cicada’s intake of xylem sap because the water loss across the cuticle is high in cicada (Hepler et al. 2023). Instead, in cicadas, the nutrient necessary for reproduction may be collected during nymphal stage. Both nymphs and adults rely on nutritionally poor xylem sap for nutrient intake (Cheung and Marshall 1973; WHITE and STREHL 1978). However, as the nymphal stage is much longer compared to adult stage, nymphs can have enough time to accumulate reserves and grow (White and Lloyd 1975). Thus, adult cicadas seem to rely on resources stored during the larval stage for reproduction. Actually, female cicada fecundity is also known to depend on resource acquisition during the larval stage (Brown and Chippendale 1973). Therefore, we suggest that the capital breeding strategy is more prominent in T. isshikii . To further evaluate whether resource allocation strategies during cicada reproduction are more aligned with those of capital breeders along the income-capital breeding continuum, future studies should investigate how food intake during nymph and adult stages affects reproductive output.
Alternatively, if body mass influences agility in escaping predators in cicadas, this can also lead to within-individual correlations between body mass and risk-taking behaviours. In flying insect species, heavier body mass has been shown to reduce individual agility in escaping predators, increasing predation risk (McLachlan et al. 2003; Roitberg et al. 2003). Although the relationship between predation rate and body mass has not been assessed in cicada species, poor agility caused by heavy body mass during early adulthood may make calling males more vulnerable to predators such as robber flies. Therefore, it might be advantageous for young males to reduce their calling activity and move cautiously. However, as body mass decreases with age, increased agility in escaping predators can reduce the predation risk of older males. This may enable older males to be more active in finding mates and producing calls. Thus, the relationship between body mass and predation risk may explain within-individual correlations between body mass and risk-taking behaviours in our study. However, if body mass affected predation risk in cicadas, a negative among-individual correlation would also be expected between risk-taking behaviours and body mass, but we found no such correlation. Therefore, we suggest that within-individual trait correlations in T. isshikii are not explained by a relationship between body mass and predation risk.
While individual-level behavioural studies with repeated measures experimental design have been extensively conducted across various animal taxa in the wild (as reviewed in Hertel et al. 2020), such investigations are less common in insects (but see Fisher, David, et al. 2015; Fisher, James, et al. 2015; Niemelä et al. 2015; Golab et al. 2021; Niemelä et al. 2021). This scarcity might arise from the challenges of distinguishing and tracking individual insects in their natural habitats. Despite a recent study demonstrating the existence of personality traits in cicadas under laboratory conditions (Roth et al. 2022), no studies have tracked individual cicadas in the wild, repeatedly measured their behaviour, and assessed individual differences. Our field study addressed this gap, providing insights into the behavioural ecology of cicadas, specifically shedding light on the reproductive and life history strategies of T. isshikii males. Our study revealed the integration of age-related plasticity in body mass and risk-taking behaviours, resulting in within-individual correlations among these traits in male cicadas. The asset protection principle could explain the age-related increase in calling activity and the preference for narrow-leafed plants. Such an age-related increase in energetically demanding behaviour may also cause an age-related decrease in body mass. While adult cicadas rely on nutritionally poor xylem sap, the age-related decrease in body mass was associated with an age-related increase in risk-taking behaviour, suggesting that T. isshikii males resemble capital breeders more than income breeders. Thus, we emphasise that studying individual behaviour in the wild is crucial to achieve a comprehensive understanding of the behavioural ecology of the study animal and the evolutionary processes that shape their behaviours and life-history strategies in the wild.