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.