Discussion
Here we demonstrate how butterflyfishes respond to the loss and
subsequent recovery of their primary food source by adjusting their
aggression levels in line with resource availability. We found that this
was unlikely to be caused by a reshuffling of the butterflyfish
community, or a selective removal of more aggressive individuals, but
more plausibly linked to energy conservation during an acute disturbance
event. Once coral cover recovered, aggression returned to
pre-disturbance levels, demonstrating the importance of behavioural
plasticity to maintain species persistence during environmental
disturbances. As predicted by models of economic defendability, the drop
in the probability of aggressive interactions occurring on Iriomote
following bleaching, closely matched the availability of the primary
food resource for many butterflyfish species; staghorn Acropora corals. Similarly, as coral cover recovered, in years following the
bleaching event, so did aggressive interactions. While we do not have
sufficient replication to statistically analyse aggression at the
species level across the four years, visual examination of trends
suggest the majority of species closely followed the these trends
(Supporting information). Engaging in territorial and aggressive
interactions carries a significant energetic cost [26], both in
terms of energy directly allocated to the behaviour [27], and
opportunity cost due to reduced feeding [28]. Thus, a decline in
aggressive interactions is likely to lead to lower energy consumption
during an ongoing disturbance event. Reductions in energy-intensive
behaviours during times of low resource availability may be a successful
evolutionary strategy to conserve energy, and species with higher levels
of behavioural plasticity tend to have a higher survival during
disturbance events [29,30]. As environmental disturbances become
more frequent and more severe globally, it is increasingly important to
understand how these processes play out in the long-term.
Altered behaviour is invariably linked to a trade-off between energy
expenditure (maintenance, growth, reproduction) and energy acquisition,
and populations are unlikely to persist on either extreme of this
trade-off spectrum. In species or individuals with a high degree of
behavioural variability or capacity to adapt their behaviour, we would
expect behaviour to always be close to optimum for a given resource
availability. For example, urban nesting birds that experienced an
increase in availability of nesting and foraging sites during Covid-19
lockdowns were less territorially aggressive [31]. Similarly, male
black-throated blue warblers (Setophaga caerulescens ) that were
given a supplemental diet reduced their singing rates, representative of
territorial behaviour, in favour of behaviours more directly linked to
increased reproductive success, such as mate guarding [32]. In
contrast, we would expect strong selective pressure against individuals
with limited behavioural flexibility, such that the population and
community composition is altered in affected ecosystems [33,34].
The variation in extent and frequency of disturbance will also interact
with a species’ life history strategy, potentially affecting some
species disproportionally. For species with a relatively short lifespan,
a severe disturbance event can have a large impact on population
dynamics and leave populations with little time to recover between
events. However, shorter generation times facilitate more rapid
evolutionary adaptation through natural selection. Butterflyfish can
live over a decade, with mean maximum age for common species spanning
5-10 years [35], and attain sexual maturity within the first two
years of life [36]. The demography of this family of reef fishes
suggest they are likely to experience multiple disturbance events
throughout their life cycle. Studies of animal behaviour are often
limited in spatial and temporal replication making it difficult to tease
apart whether it is behavioural plasticity at the level of an individual
or within populations, or adaptative selection across generations, that
is the underlying mechanism of altered behaviour. By monitoring the
abundance and species composition of a community over time we can
disentangle whether behavioural changes can be plausibly explained by
the selective removal of individuals with maladaptive behavioural
traits.
In this study, we found weak evidence of a reshuffling of the
butterflyfish community post bleaching, however this pattern was largely
driven by rare species. There was no significant shift in the relative
proportions of the four most common species in the population, nor an
overall change in the abundance of butterflyfishes. We predicted that
the degree of feeding preference specialisation would affect how species
responded to coral mortality, as highly specialised species are more
constrained by resource availability than generalists [37].
Butterflyfishes display a range of dietary preferences, from highly
specialised obligate coral feeders that feed exclusively on a small
subset of Acropora species (e.g. C. trifascialis ), to
facultative coral feeders whose diet consists of over 80% corals (e.g.C. citrinellus ), through to invertivores (e.g. C.
vagabundus ). However, the relative abundance of these three feeding
guilds (facultative, obligate coral feeders, and invertivores) did not
differ significantly between the four surveyed years. Combined, these
results suggest that a plasticity in behaviour, rather than selective
removal of aggressive individuals, species or feeding guilds, has
allowed this butterflyfish population to adapt to shifting resource
availability and weather the storm of a substantial disturbance event.
Our results follow the classic pattern of the economic defendability
model, where individuals must balance the advantages (e.g. energy
gained) and disadvantages (e.g. energy lost) associated with competing
for the resource to maximise fitness. For example, individuals risk a
net loss of fitness if engaging in aggression over an ephemeral or
highly mobile resource that is difficult or impossible to defend
effectively [11]. Under this model, aggression is predicted to be
highest at intermediate resource availability, where resources are
limited yet abundant enough to warrant energy investment into aggressive
interactions. It follows then that aggression is predicted to be low at
both extremes of the resource availability spectrum where resources are
either too abundant to require investment in aggressive interactions, or
so scarce that such investment is associated with reduced
fitness[38]. While Brown’s model of economic defendability has been
supported in a multitude of systems at varying fixed levels of resource
availability (e.g salmonids[39], herbivorous damselfishes[40]
and convict cyclids[41]), our current understanding is largely based
on such static snapshots in time. This is the first time the model has
been tested in the context of environmental change, using repeated
sampling in the field during an ongoing disturbance event.
While a temporary behavioural shift to conserve energy may have allowed
this population to weather the storm of a large-scale disturbance event,
these findings do not suggest reef fishes are safe from anthropogenic
climate change. Only species with adaptable behaviour can access this
short-term survival strategy. For example, birds with a capacity to
alter migration routes can avoid wintering sites that have suffered
habitat loss, while their less flexible counterparts will suffer the
consequences of reduced resource availability [42]. Second, a
behavioural response to habitat loss hinges on the reliability of cues
to assess habitat quality, with incorrect cues leading to maladaptive
behaviours (e.g. caught in ecological traps) [43]. Indigo buntings
(Passerina cyanea ) for example, prefer forest edge habitat due to
a low abundance of predators in naturally created edges. However, the
birds are equally attracted to anthropogenically created edges that
contain increased numbers of nest predators, and suffer lower
reproductive success as a result [44,45]. Finally, the frequency of
disturbance events is likely to increase, reducing the capacity for
systems to recover fully between events, limiting the effectiveness of
behavioural shifts [46].
Habitat loss remains one of the most pervasive threats against global
biodiversity, reshuffling ecosystems and communities and causing a
worldwide biodiversity crisis. Here we have demonstrated that a
community of butterflyfishes alters their behaviour in line with
resource availability by engaging in fewer aggressive interactions when
resources are low, and returning to pre-disturbance behaviours as
resources recover. The most plausible explanation to understand this
change in behaviour is a reduction in energy expenditure during
environmental change, to maintain optimal responses following the
economic defendability model. While good news for this family of reef
fishes benefiting from relatively rapid resource recovery, our findings
highlight the vulnerability of individuals, and species, with low
behavioural flexibility. Further, behavioural flexibility may not
safeguard species experiencing environmental change where the
conditions, magnitude of disturbance, or other variables are not as
favourable to recovery. Our findings further emphasise the importance of
understanding behavioural responses to habitat loss to predict how
ecosystems may adapt to future environmental conditions.