Lunar rhythms in growth of larval fish

Abstract

Growth and survival of larval fishes is highly variable and unpredictable. Our limited understanding of this variation constrains our ability to forecast population dynamics and effectively manage fisheries. Here we show that daily growth rates of a coral reef fish (the sixbar wrasse, Thalassoma hardwicke) are strongly lunar-periodic and predicted by the timing of nocturnal brightness: growth was maximized when the first half of the night was dark and the second half of the night was bright. Cloud cover that obscured moonlight facilitated a 'natural experiment', and confirmed the effect of moonlight on growth. We suggest that lunar-periodic growth may be attributable to light-mediated suppression of diel vertical migrations of predators and prey. Accounting for such effects will improve our capacity to predict the future dynamics of marine populations, especially in response to climate-driven changes in nocturnal cloud cover and intensification of artificial light, which could lead to population declines by reducing larval survival and growth.

Keywords: developmental history; larval growth; lunar periodicity; reef fish; trophic connectivity.

Figure 1.

Lunar cohorts of larval sixbar wrasse and their residual growth trajectories. (a) Frequencies of sampled larvae (n = 411) born on each LD. Colour identifies ‘lunar cohort’ determined by birthdate on a lunar calendar (estimated from otoliths). Birthdates from LD ∼ 26 to LD 3 = ‘new moon’; 4 ≤ LD ≤ ∼11 = ‘first quarter’; approximately 12 ≤ LD ≤ 18 = ‘full moon’; 19 ≤ LD ≤ ∼25 = ‘last quarter’ (note that variation assignments at day 11 and 26 is owing to uneven durations of lunar months). (b) Residual (i.e. age-independent) growth trajectories of larvae assigned to four lunar cohorts. Given are mean ± 1 s.e. residual growth per day (points are offset for presentation) and fitted lines are predicted by a GAM (span = 3). Dashed line indicates average growth. Symbols indicate the timing of the last quarter moons (top) and first quarter moons (bottom) for each lunar cohort (i.e. for median lunar birthdates of each lunar cohort). (Online version in colour.)

Figure 2.

Lunar pattern of (a) nocturnal brightness and (b) residual growth of larval sixbar wrasse. Nocturnal brightness is expressed as intensity (i.e. proportion of lunar disc illuminated: greyscale, black = 0, white = 1) and timing (moonrise and moonset, averaged over the sampled months, rounded to the nearest hour) of moonlight across lunar nights. Residual (i.e. age-independent) growth is mean ± 1 s.e., fit by periodic regression (note our formal analyses included a set of random effects not represented by this fitted line). y-axis in panel (a) ranges from 18.00 (approx. dusk, y-axis maximum) to 6.00 the following morning (approx. dawn, y-axis minimum). x-axis of both panels is date expressed on a 29.5 d lunar cycle (0 = new moon, 14 = full moon, etc.).

Figure 3.

Predicted residual growth of larval sixbar wrasse as a function of nocturnal cloud cover, conditional on lunar parameters set to (a) the new moon, (b) the first quarter moon, (c) the full moon, and (d) the last quarter moon. Given are predicted values (black lines) ± 95% CI (shaded envelopes). X-axis is the proportion of night sky (in a 3° latitude × 3° longitude region centred on Mo'orea) shrouded in cloud, back-transformed to the original scale (0 = clear night, 1 = fully cloudy night). Predictions falling above the dashed line indicate better-than-average growth; values below the dashed line indicate worse-than-average growth.

Figure 4.

A schematic hypothesis of how nocturnal illumination may shape larval growth of a reef fish. The lunar cycle is represented as four discrete panels for simplicity: (a) new moon, (b) first quarter moon, (c) full moon, and (d) last quarter moon. Each panel shows a cross section of the atmosphere (white = moon above horizon; grey shading = moon below horizon) and the water column (light blue line = sea level, depth gradient from epipelagic to mesopelagic) through time (from dusk to dawn). Moon phase, moonrise and moonset times create variation in nocturnal illumination that affects the water column. Larval sixbar wrasse (shown in yellow) remain in surface waters; their prey (copepod icons/brown shading) and their predators (myctophid icons/red shading) undergo diel vertical migrations that are sensitive to nocturnal illumination. Prey can respond quickly to changes in light; predators migrate from deeper depths and therefore respond with a time lag. (Online version in colour.)