DOI: 10.5061/dryad.7d7wm3801
title: Rapid resource depletion on coral reefs disrupts competitor recognition processes among butterflyfish species

description: Avoiding costly fights can help conserve energy needed to survive rapid
 environmental change. Competitor recognition processes help resolve
 contests without escalating to attack, yet we have limited understanding
 of how they are affected by resource depletion and potential effects on
 species coexistence. Using a mass coral mortality event as a natural
 experiment and 3,770 field observations of butterflyfish encounters, we
 test how rapid resource depletion could disrupt recognition processes in
 butterflyfishes. Following resource loss, heterospecifics approached each
 other more closely before initiating aggression, fewer contests were
 resolved by signalling, and the energy invested in attacks was greater. In
 contrast, behaviour towards conspecifics did not change. As predicted by
 theory, conspecifics approached one another more closely and were more
 consistent in attack intensity yet, contrary to expectations, resolution
 of contests via signalling was more common among heterospecifics.
 Phylogenetic relatedness or body size did not predict these outcomes. Our
 results suggest that competitor recognition processes for heterospecifics
 became less accurate after mass coral mortality, which we hypothesise is
 due to altered resource overlaps following dietary shifts. Our work
 implies that competitor recognition is common among heterospecifics, and
 disruption of this system could lead to suboptimal decision-making,
 exacerbating sublethal impacts of food scarcity.
description: (a) Study system Taxon. Coral reef
 butterflyfishes (genus Chaetodon) offer a model field system to examine
 how changes in resource availability can affect competitor recognition
 processes for several reasons. First, butterflyfishes show clear
 signalling (e.g., tail-up while head angled down, erection of the dorsal
 fin) and attacks during both conspecific and heterospecific encounters
 [23, 24], and changes in resource availability can lead to changes in
 aggression both within and among species [7, 25]. Secondly,
 butterflyfishes use predominantly visual cues for species recognition
 [26-28]. Thirdly, individuals of many butterflyfish species form stable
 mated pairs [24], meaning that conspecific aggression is overwhelmingly
 driven by access to food rather than reproduction. Fourth, the phylogeny
 of butterflyfishes is well resolved [29], which allows us to test the
 hypothesis that behavioural responses involved in the competitor
 recognition process can be predicted by phylogenetic relatedness of
 species [4, 8]. Field Sites. We observed encounters
 among butterflyfishes at five regions across the central Indo-Pacific:
 Iriomote (Japan; 123.7° E, 24.4° N), Christmas Island (Indian Ocean;
 105.6° E, 10.4° S), Luzon (the Philippines; 120.8° E, 13.7° N), Aceh
 (Indonesia; 95.1–95.3° E, 5.4–5.9° S) and Bali (Indonesia; 115.6° E, 8.4°
 S). We visited reefs up to 12 months either side of a global mass coral
 bleaching event [7]. We recorded data on 17 reefs in total, comprising of
 3 to 4 sampled reefs per region. Reefs were separated by &gt; 1 km
 non-reef patches (corallivorous butterflyfish territories are generally
 &lt; 0.2 km2) [30] to sample different populations. For further
 information on field sites and data collection, see Keith et al
 [7]. (b) Data collection We used a
 well-established protocol to observe butterflyfishes on snorkel or SCUBA
 depending on depth and visibility [31, 32]. Focal individuals were
 followed at a distance of 2–4 m for five minutes following an acclimation
 period (~1 minute) to check that the individual was responding naturally
 (that is, feeding). Butterflyfish are often found in a mated pair, so to
 ensure independence of sampled individuals, only one individual of each
 pair was recorded. To reduce the risk of selecting the same fish as a
 focal individual twice, we used a U-shaped search pattern and attempted to
 observe one individual from every pair present on the reef. When a
 congeneric individual from outside the mated pair came within 1 m of the
 focal individual, we assumed they were aware of each other’s presence with
 the potential to interact, and therefore recorded an encounter.
 Proximity was recorded as the smallest distance observed between
 two individuals during an encounter. Encounter outcomes were recorded as
 passive, where neither individual showed a discernible change in
 behaviour, or aggressive. Aggressive encounters were further subdivided
 into those that involved signalling only and those that escalated to a
 chase [32]. Both forms of aggression are linked strongly to competition
 over food resources, and as the majority of our observed individuals were
 in a pair, the possibility that they were engaging in courtship displays
 with individuals outside of their pair was minimal [32]. Each new observer
 underwent training by an experienced observer (either J-P.H. or S.A.K.)
 until recorded data were identical to ensure standardization. Behaviour
 was unlikely to have been affected by diver presence [33].
 (c) Statistical analysis Data used for
 analysis were restricted to species pairs with at least five encounters
 across five different focal individuals. For some analyses, data were
 restricted further to include only species that were present with these
 minimum sample sizes in both conspecific and heterospecific encounters.
 This reduced dataset ensured that any differences were not driven solely
 by a larger and more variable pool of species in the heterospecific
 encounters. Note that due to this requirement to use a reduced dataset,
 statistical models with more parameters (e.g., generalised linear mixed
 effects models) were not appropriate. The three Philippines reefs did not
 experience significant coral mortality as a result of bleaching and are
 therefore not included in the data for after the coral mortality event.
 All analyses were done in R v.3.6.1. [34]. Prediction
 1: Individuals approach heterospecifics less closely than conspecifics.
 Proximity distances were estimated to the nearest 25 cm in the field (0-24
 cm, 25-49 cm, 50-74 cm, 75-100 cm) and converted to dummy variables (1-4)
 for analysis. To account for non-independence of repeated samples, we
 calculated the mean of the distance categories from the dummy variables
 for each individual across its conspecific and heterospecific encounters
 separately. Use of the mean is appropriate for ordinal data in this case
 because the numeric difference between each category is equal. We then
 used a permutation based two-tailed Mann Whitney U test from the coin
 package [35] with a Monte Carlo-derived approximate distribution to
 determine whether the mean proximity during conspecific encounters was
 significantly different from the mean proximity during heterospecific
 encounters. Data were logged for plotting purposes only.
 Prediction 2: Signalling is more common between conspecifics than
 heterospecifics. We calculated the proportion of aggressive encounters
 that involved visual signalling for conspecific and heterospecific pairs
 both before and after bleaching. To deal with non-independence of samples
 due to repeated measures within individuals (i.e., multiple encounters per
 individual), we bootstrapped the data 1000 times, each time sampling one
 encounter only per individual. For each bootstrapped dataset, we tested
 whether the frequency of signalling (rather than escalation to attack) for
 conspecific and heterospecific encounters, and before and after coral
 mortality within those groups, were significantly different from expected
 using chi-squared permutation tests from the coin package [35], which is
 robust to small or skewed sample sizes. We calculated the mean chi-squared
 statistics and p values, and their 95% confidence intervals, across
 bootstrapped datasets. Prediction 3: Attack intensity
 is more variable between heterospecifics than conspecifics. We used the
 coefficient of variation (CV) to quantify variation in chase distances
 across heterospecific and conspecific encounters relative to the mean. We
 use this approach because the mean chase distance is higher for
 conspecifics, as we would expect from the literature and theory, so a
 measure relative to the mean is essential. To minimise the influence of
 rare long chases, we grouped all that were ³10 m. We tested whether there
 was a significant difference in the CV between conspecific and
 heterospecific chase distances using the modified signed-likelihood ratio
 test for equality of CVs (MLSR), which is robust to differences in sample
 size [36], from the R package cvequality [37].
 Prediction 4: Proximity, signalling and variation in attack
 intensity can be predicted by phylogenetic relatedness and difference in
 body size. To determine whether approach proximity, signalling proportion
 and variation in chase distance could be predicted by phylogenetic
 relatedness, we used branch length between each species pair in the
 phylogeny [29], calculated with the ape package [38]. We also tested
 whether body size could predict these behaviours because it can be a cue
 for individuals to identify competitors. Body size differences were
 calculated from the species level trait maximum body length downloaded
 from Fishbase [39], which is appropriate because Chaetodontids achieve
 68-92% of their full adult body size in the first year and do not differ
 perceptibly as adults [40]. Conspecifics were excluded to ensure the
 result could be interpreted as a nuanced representation and was not
 overwhelmed by zeros (i.e., for phylogenetic distance). We generated
 separate regression models for mean proximity, signalling proportion and
 variation in chase distance as dependent variables (species pairs: n = 107
 proximity; n = 24 signalling; n = 16 for chase variation) and checked QQ
 plots to ensure assumptions were met for proximity and attack intensity.
 Signalling was modelled using a binomial GLM to account for proportional
 dependent data, and McFadden’s R2 index was used to assess predictive
 ability.