Main
Anthropogenic climate change is causing substantial loss of habitat in
global ecosystems, with devastating effects on biodiversity [1,2].
Changes in behaviour are often the first response of individuals to
disturbance [3–5], yet behavioural responses and their ecological
consequences, especially in real-world settings, are poorly understood
relative to direct lethal impacts [6]. When faced with acute
disturbances, organisms can adopt temporary behavioural changes that
increase their chances of survival. [7]. For instance, when
resources are depleted, individuals can conserve energy by changing
activity levels [8] or reducing territorial behaviour [9].
Despite the significant ramifications for population persistence,
species coexistence and wider ecosystem function [10], the
mechanisms that underlie these behavioural shifts are unclear. This gap
in knowledge hinders our capacity to predict the resilience of
populations to environmental change, and to understand the implications
for population and community dynamics.
Economic models provide a useful lens for understanding behavioural
flexibility [11]. Aggressive behaviour, which functions to defend
territories and maintain access to resources, can be dynamically
regulated according to the costs and benefits of defence [12]. This
dynamic regulation predicts a hump-shaped relationship between
aggression and resource availability, where aggression is highest at
intermediate resource levels. Decreased aggression of reef fish in
response to resource depletion offers partial support for this model
[9], but the critical test lies in determining whether aggression
returns to pre-disturbance levels following resource recovery. Resolving
this question would improve predictions of population resilience to
ongoing environmental changes.
An alternative explanation for behavioural change following disturbance
posits differences in fixed behavioural phenotypes across individuals
within a population. In this case, natural selection can lead to a loss
of individuals with an uneconomic level of aggression, which directly
impacts on the probability of aggressive encounters within the
population. Under such a scenario, a return to pre-disturbance
frequencies of behaviour relies on processes that occur over a
substantially longer time period, i.e. an increase in the proportion of
aggressive individuals either through immigration or reproduction.
Reproduction is likely to be delayed or reduced when individuals are
energetically compromised following resource depletion [13,14], and
a return of aggressive behaviour could be further limited if such
behaviours are heritable rather than learned. Thus, reverting back to
the original state hinges on several variables, including extant
behavioural diversity from which to replenish affected populations,
dispersion rates, reproductive rates and the extent of variation in
aggressive behaviour within the repertoires of individuals. If behaviour
is fixed, the subsequent loss of behavioural diversity following
disturbance could affect the potential of the population to adapt to
future environmental changes [15]. Therefore, identifying which
mechanism is in action can provide vital information on how quickly
populations can recover behaviourally from disturbance, if they can
recover at all, and the potential ramifications at the community and
ecosystem scale.
Coral reef fishes offer an excellent model system with which to explore
behavioural responses to disturbance and are particularly vulnerable to
environmental change. In particular, butterflyfishes are highly reliant
on live coral [16], have small home territories [17], are
abundant and easy to identify [18], and their behaviours can
reliably be assessed in the field [e.g. 9,14,19]. Butterflyfishes
also display a range of territoriality, with a species’ levels of
aggression positively correlated to their degree of feeding
specialisation [20,21]. Here, we use an unprecedented dataset that
tracks aggressive behaviour between 23 species of butterflyfishes on
three reefs in Japan from 2016-2022. This includes surveys through a
full cycle of disturbance and resource recovery, following a mass coral
bleaching event in 2016. In the year after this disturbance, corals (the
primary food source of butterflyfishes) were significantly depleted
throughout the Indo-Pacific (18-65% loss,) leading to a three-fold
reduction in aggressive territorial defence [9]. Here, we undertake
the first test of the long-term impact of altered resource availability
on aggressive behaviour in the field to ask whether the reduction in
aggression (1) reverts to pre-disturbance levels, indicating behavioural
flexibility, or (2) persists in the population indicating that behaviour
is fixed. To ascertain the fit with the predictions of the economic
model of defendability, we also tested (3) whether the main food source
of the butterflyfishes (Acropora corals) recovered in abundance,
and (4) if changes in aggression could be a by-product of potential
changes in the relative abundance of Chaetodon species caused in
response to the bleaching event.