Human-induced environmental change has directly and indirectly affected ecosystems on a global scale, altering the behavior, ecology, and evolutionary trajectories of various species. Fishing of marine top predators and the cascading effects this may have on marine ecosystems is of critical concern. Predators are thought to be an important reason for why fish form schools, thus, a reduction in predator populations could alter schooling behavior for prey fish. Here, we investigate the indirect effects of fishing out predators on the schooling behavior of coral reef fishes. We compared the tendency to school for three fish species between two Pacific coral reefs: Palmyra Atoll (USA), an unfished reef with high predator abundance, and Moorea (French Polynesia), a fished reef with low predator abundance. We also specifically characterize movement and foraging-associated behaviors of one of these fishes, the convict surgeonfish (Acanthurus triostegus), in this same comparative context.   

Study sites

The study was conducted on the Pacific coral reefs of Palmyra Atoll (5°53’N, 162°5’W;) and Moorea Island (17°32’S 149°50’W). Palmyra Atoll (USA) is a remote uninhabited island that forms part of the northern Line Islands archipelago in the Central Pacific. Moorea (French Polynesia) is an inhabited island (population 17,816 in 2017) that forms part of the Society Islands archipelago in the South Pacific (INSEE 2017). Schooling surveys and focal follows (described below) were conducted at four sites on the backreef of Palmyra Atoll and four sites on the backreef of Moorea.

Palmyra Sites

WT: 5.882234, -162.123690

LL: 5.877881, -162.114265

RP: 5.875142, -162.120279

PS: 5.870679, -162.109125

SIB: 5.875445, -162.107227

Moorea Sites

TIAHURA: -17.485822, -149.890088

TEMAE: -17.508686, -149.763688

TIKI: -17.543092, -149.900736

PUBLIC: -17.523421, -149.917574

HILTON: -17.482513, -149.845671

 Schooling behavior surveys

We conducted 30-min roving diver surveys (Rassweiler et al., 2020; Schmitt et al., 2002) to compare the prevalence of schooling behavior across both islands. An observer snorkeled in a random pattern for 30 minutes and recorded any focal species individuals observed. For, A. triostegus, C. spilurus , and M. flavolineatus, we counted every individual, as schooling tendency could be a result of conspecific (Okubo, 1986) and assessed whether the fish were in a school (and noted school size) or solitary. School sizes were approximated to the number of individuals when possible, and approximated in bins of 5, 10, or 50 in larger or fast-moving schools. For this study, schooling refers to three or more fish exhibiting organized group behavior, and may include synchronized and parallel swimming behaviors (as defined by T. J. Pitcher, 1983), but we did not include any spawning aggregation behavior.

Some species of herbivorous fish that form schools are known to use their numbers to overwhelm territorial herbivores to force access into their guarded territories (Choat & Bellwood, 1985; Eurich et al., 2018; Foster, 1985). Thus, to control for the potential of variation in the numbers of territorial herbivores affecting schooling behavior differentially among islands, we also surveyed the abundance of these territorial herbivores (i.e. Acanthurus lineatus, Acanthurus nigricans, and Stegastes nigricans on Palmyra Atoll and Acanthurus nigrofuscus and Stegastes nigricans on Moorea). 

Acanthurus triostegus behavioral observations

We conducted 30-60min focal follows on A. triostegus to evaluate movement and behavior of schooling and solitary fish subject to different predator abundances. We assessed three metrics of fish behavior for defined portions of these focal follows: proportion of time spent non-vigilant, distance travelled, and area covered via calculation of a 95% kernel utilization distribution (KUD). 

Snorkeling observers (four observers on Palmyra Atoll, two on Moorea, lead observer (ASG) was present on both islands) followed solitary or schooling A. triostegus while towing a GPS device that recorded location every 60s. Initial follows were conducted at both islands to assess appropriate distance for following fish that would not impact normal foraging nor initiate a flight response. Every 60s, the observer would note school size (if applicable), and whether the focal individual(s) was exhibiting non-vigilant grazing behavior, a position in which the fish had their body oriented towards the substrate in a nose-down grazing position at time of observation, or vigilant behavior with an upright body orientation whether the fish was swimming or stationary. This behavior was classified as non-vigilant grazing as these nose-down grazing positions can reduce a prey fish’s ability to visually scan for predators (Krause & Godin, 1996). Observations on schools were done by recording behavioral information based on the behavior of 50% or more of the individuals in the school (e.g., school was recorded as ‘non-vigilant grazing’ if at least half of the school was in a nose-down position at the 60s mark). If a school was widely dispersed or in a line formation, the observer followed the last 1/3 for the school and recorded the information for that subset of the school. If an observer lost sight of a solitary fish or school of fish, they were able to search for the fish for up to two minutes. If after two minutes the fish were not located, the focal follow would be terminated. 

References:

Choat JH, Bellwood DR (1985) Interactions amongst herbivorous fishes on a coral reef: influence of spatial variation. Mar Biol 89:221–234. doi: 10.1007/BF00393655

Eurich JG, Shomaker SM, McCormick MI, Jones GP (2018) Experimental evaluation of the effect of a territorial damselfish on foraging behaviour of roving herbivores on coral reefs. Journal of Experimental Marine Biology and Ecology 506:155–162. doi: 10.1016/j.jembe.2018.06.009

Foster SA (1985) Group foraging by a coral reef fish: a mechanism for gaining access to defended resources. Animal Behaviour 33:782–792. doi: 10.1016/S0003-3472(85)80011-7

Institut national de la satistique et des études économiques (2017) Populations légales des communes et des communes associées de Polynésie française en 2017.

Krause J, Godin J-GJ (1996) Influence of prey foraging posture on flight behavior and predation risk: predators take advantage of unwary prey. Behav Ecol 7:264–271. doi: 10.1093/beheco/7.3.264

Okubo A (1986) Dynamical aspects of animal grouping: Swarms, schools, flocks, and herds. Advances in Biophysics 22:1–94. doi: 10.1016/0065-227X(86)90003-1

Pitcher TJ (1983) Heuristic definitions of fish shoaling behaviour. Animal Behaviour 31:611–613. doi: 10.1016/S0003-3472(83)80087-6

Rassweiler A, Dubel AK, Hernan G, Kushner DJ, Caselle JE, Sprague JL, Kui L, Lamy T, Lester SE, Miller RJ (2020b) Roving Divers Surveying Fish in Fixed Areas Capture Similar Patterns in Biogeography but Different Estimates of Density When Compared With Belt Transects. Front Mar Sci. doi: 10.3389/fmars.2020.00272

Schmitt E, Sluka R, Sullivan-Sealey K (2002) Evaluating the use of roving diver and transect surveys to assess the coral reef fish assemblage off southeastern Hispaniola. Coral Reefs 21:216–223. doi: 10.1007/s00338-002-0216-y

All file metada can be found in metada_reef_fish_schooling.rtf