Introduction
Within an individual, the expression of labile traits (e.g., behavioural, physiological or morphological traits such as body mass) can exhibit variation with individuals adjusting their phenotypes over time or in response to environmental changes. Moreover, within-individual plastic changes in multiple traits can also be associated across traits (Dingemanse et al. 2012; Dingemanse and Dochtermann 2013). If the expression of multiple traits is based on a shared underlying mechanism or these traits affect each other via a feedback loop (Sih et al. 2015), we would expect to find an association between within-individual changes in multiple traits. For instance, if exercise elevates the plasma level of corticosterone in mice (Girard et al. 2002), the daily pattern of exercise is expected to align with that of corticosterone levels. In addition, as a high metabolic rate is needed to express energetically demanding behaviour (such as risk-taking behaviour), within-individual changes in the resting metabolic rate are expected to parallel those in risk-taking behaviour (e.g, Cornwell et al. 2020). The correlation between changes in multiple traits within an individual is termed a ”within-individual trait correlation” (Dingemanse and Dochtermann 2013). Multiple traits may change (or fluctuate) in the same direction within an individual, causing a positive within-individual trait correlation (scenarios 1 and 3 in Figure 1). Conversely, traits may change (or fluctuate) in opposite directions within an individual, causing a negative within-individual trait correlation (scenarios 2 and 4 in Figure 1).
Within-individual trait correlations are strongly expected when trait expression is dependent on age (scenarios 1 and 2 in Figure 1). Notably, since individual differences in behaviour can stem from variations in state variables (Biro and Stamps 2008; Dingemanse and Wolf 2010; Wolf and Weissing 2010; Sih et al. 2015), age-related decreases in labile state variables (e.g., body mass, metabolic rate and hormone levels) are expected to correspond with decreases in behaviours, leading to positive within-individual correlations between state variables and behaviours (scenario 1 in Figure 1). In this scenario, physiological deterioration with ageing may diminish state trait levels, subsequently reducing the expression of state-dependent behavioural traits and resulting in a positive within-individual correlation between state and behaviour. For example, in male field crickets Gryllus campestris , both body mass and exploration decrease with age, leading to a positive within-individual correlation between body mass and exploration (Santostefano et al. 2016). In addition to ageing, there may be a positive feedback loop between body mass and exploration in the field cricket (e.g., reduced body mass decreases exploration, and vice versa), further contributing to a positive within-individual correlation between body mass and exploration.
In addition, within-individual trait correlation can be an outcome of age-related changes in future fitness expectations (i.e., residual reproductive value, Williams 1966). According to the asset protection principle (Clark 1994), individuals tend to take more risks when their future fitness expectation is low, and when the reproductive costs from injury or death are less important (Clark 1994; Luttbeg 2017). Consequently, older individuals with lower expected future fitness are more likely to exhibit risk-taking behaviour (e.g., Dammhahn 2012; Fisher et al. 2015; Ory et al. 2015; Moschilla et al. 2018), potentially resulting in strongly positive within-individual correlations among risk-taking behaviours. Moreover, if age-related decreases in state variables such as body mass reflect changes in future fitness expectations (e.g., body mass determines dominance), a decrease in body mass with age would be integrated with the age-related increase in multiple risk-taking behaviours, resulting in a negative within-individual correlation between body mass and risk-taking behaviour (scenario 2 in Figure 1).
Overall, the direction of within-individual trait correlations between state and behaviour can vary depending on the trait-specific mechanisms leading to age-related increase/decrease or fluctuation (Figure 1). Recent meta-analyses have indicated a weak relationship between state and behaviour at both the within-individual and among-individual levels (Niemelä and Dingemanse 2018); however, this might be attributed to a paucity of studies conducting frequent repeated measurements of labile traits with longer intervals between repeated measures. Therefore, it is imperative to assess within-individual trait correlations to identify the underlying trait-specific or common mechanisms shaping age-related plasticity. However, within-individual correlations have garnered considerably less attention from behavioural ecologists (Dochtermann 2023).
In this study, we tracked individual male cicadas Tettigetta isshikii (Figure 2) in their natural habitat and repeatedly assessed their plant use, calling activity, and body mass. We investigated age-related changes in these traits, partitioned trait variance into among- and within-individual levels, and estimated among- and within-individual correlations among these traits. In this study, we predicted that two behaviours, plant use and calling activity, would reflect the boldness of each male. Cicadas actively use plants as shelters, adjusting their location within the plant to hide themselves (Steward et al. 1988). Different plant species vary in structural characteristics, such as leaf size and density, suggesting the shelter they provide for cicadas may differ by species. Cicadas might prefer plants with larger, denser leaves to protect them from aerial predators (e.g., robber fly). T. isshikii also feeds on herbaceous plant sap and lays its eggs in plant stems, potentially using the plants as shelters by hiding underneath the leaves (Jiman Heo, personal observation). In our study area, plants such as Erigeron annuus (Daisy fleabane), Thalictrum aquilegiifolium (Meadow rue), orMiscanthus sinensis (Chinese silver grass) have narrow or small leaves, whereas only 2 plants, Convallaria majalis (Lily of the valley) and Polygonatum odoratum (Solomon’s seal), have large leaves and occurs in discrete clusters (Figure 3). As a result, onlyC. majalis and P. odoratum may effectively function as a shelter for T. isshikii. Thus, we predicted that the increased use of narrow-leafed plants might indicate greater boldness in the face of potential predators. In addition, male T. isshikii produces calls to attract females, and females respond with wing-flicking sounds (Jiman Heo, personal observation). However, calling songs of cicadas increases predation risk by predators such as the robber fly (Hou et al. 2017), suggesting that calling can also be considered a risk-taking behaviour of male T. isshikii .
We predicted that trait-specific mechanisms shaping age-related plasticity would determine within-individual trait correlations. If physiological deterioration leads to both reductions in calling activity and boldness with age as well as weight loss in male cicadas after eclosion and maturation, positive within-individual correlations between body mass and risk-taking behaviours are expected (scenario 1 in Figure 1). In contrast, according to the asset protection principle, male cicadas might increase the expression of risk-taking behaviours with age, even as body mass decreases (scenario 2 in Figure 1). This scenario could lead to negative within-individual correlations between body mass and risk-taking behaviours. Consequently, we predicted that the integration of age-related plasticity in multiple traits of male cicadas would hinge on the trait-specific mechanisms governing age-related changes.