Productivity and sea surface temperature are correlated with the pelagic larval duration of damselfishes in the Red Sea
Introduction
The time a fish larva spends in the plankton before recruiting onto a reef, known as its pelagic larval duration (PLD), is a valuable source of information on how ecological and oceanographic processes affect a fish's early life. Such information can help to better understand organisms with complex life cycles, such as many coral reef inhabitants; subsequently, this fundamental life history information can be used to improve management of marine ecosystems and their natural resources. PLDs of coral reef fishes are known to exhibit variation driven by a wide range of intrinsic and extrinsic factors (McCormick and Molony, 1995, Searcy and Sponaugle, 2000, Sponaugle, 2010, Wellington and Victor, 1992, Wilson and Meekan, 2002). Two of the most relevant extrinsic factors that cause intraspecific variations in larval growth and development are temperature and food availability (Heath, 1992, Houde and Zastrow, 1993, Mcleod et al., 2011, Takahashi and Watanabe, 2005), which can be estimated from remote sensing satellite data on sea surface temperature (SST) and chlorophyll a (CHLA) concentrations respectively. Warmer temperatures increase metabolic rate and growth rates (Green and Fisher, 2004, Meekan et al., 2003, Sponaugle et al., 2006), which can lead to shorter PLDs (Bergenius et al., 2005, Green and Fisher, 2004, Grorud-Colvert and Sponaugle, 2011, McCormick and Molony, 1995, Sponaugle et al., 2006). Similarly, higher food availability can increase larval growth (Biktashev et al., 2003, Fontes et al., 2010, Houde and Hoyt, 1987, Houde, 1989, Landaeta and Castro, 2006, Sponaugle, 2009, Sponaugle, 2010) and potentially decrease the time a fish larva spends in the pelagic before recruiting onto a coral reef (Sponaugle and Grorud-Colvert, 2006). Variations in PLDs can be indicative of differences in dispersal potential, growth rates, and survival of fish larvae. Furthermore, the conditions a fish larva experiences during its PLD seem to even influence success, fitness, and growth in later life stages as juvenile and adult fish (Cushing and Horwood, 1994, Houde and Hoyt, 1987, Houde, 1989, Rankin and Sponaugle, 2011, Sponaugle and Grorud-Colvert, 2006, Sponaugle et al., 2011). However, most studies that have assessed the influence of temperature and food availability on the larval stage of fishes have focused on larval growth rate (Mcleod et al., 2015), size at settlement (McCormick and Molony, 1995), or recruitment cohort size (Lo-Yat et al., 2011) rather than on the length of PLDs in the standing population, and still fewer of these studies target coral reef fishes. In our study we focus specifically on PLD variations within the standing populations (i.e., post-settlement and adult fishes, as opposed to recruitment cohorts) of three congeneric coral reef damselfishes present in the Red Sea.
The Red Sea is an ideal location to study the effect of a variety of environmental parameters on coral reefs (Berumen et al., 2013). The Red Sea harbors thriving and continuous coral reefs along both sides of its narrow basin. Due to its shape, location, and only a single shallow and narrow connection to the Indian Ocean, it displays a unique environmental gradient of temperature, salinity, productivity, turbidity, and essentially reef-scape (Racault et al., 2015, Raitsos et al., 2013). These physical and environmental characteristics have made the Red Sea a natural location to assess the environmental impact on several coral reef organisms (e.g., Froukh and Kochzius, 2007, Giles et al., 2015, Lozano-Cortés and Berumen, 2015, Nanninga et al., 2014, Ngugi et al., 2012, Roberts et al., 1992, Robitzch et al., 2015, Sawall et al., 2014a, Sawall et al., 2014b).
Here, we focus on the two seemingly major parameters that may drive PLD variations in the environmental gradient of the Red Sea: temperature and food availability. For this purpose we use the three Dascyllus species that live in the Red Sea (D. aruanus, D. marginatus, and D. trimaculatus). These species serve as a good model group to study PLD variations in coral reef fishes for several reasons. They are biologically similar, small in size, and commonly present along the entire environmental gradient of the Red Sea at overlapping depth ranges. They are zooplanktivorous, demersal spawners, and have relatively similar recruitment periods and larval development times (PLD). However, they have subtly different ecological preferences, which make them an interesting group to study the effect of the environment on early life history traits in the context of ecological specialization. We consider D. trimaculatus as the most ecologically versatile species within this group. It can be found on exposed reef walls, sheltered backside-reefs, and lagoons; it is not dependent on live coral; and it only uses reef structure for shelter, recruitment, and as spawning habitat. While D. trimaculatus mostly recruits onto anemones in the Red Sea, it can also recruit into branching corals, sea urchins, and other microhabitats. Once they reach juvenile stages, D. trimaculatus leave their settlement substrate, range throughout the entire reef structure, and spend most of their lifetime foraging in the water column. Intermediate on the ecological specialization ranking is D. aruanus. This species shows stronger habitat preferences, only recruiting to and living its entire life in branching live corals that are located in sheltered sandy reefs and lagoons. Dascyllus aruanus and our third species, D. marginatus, both show similar habitat preferences and occasionally even co-inhabit the same coral colony. However, the degree of ecological specialization is stronger in D. marginatus, which cannot be found on very shallow reef-tops and lagoons, nor can it be found on offshore reefs in most of the Red Sea. Therefore, we refer to D. marginatus as the most ecologically specialized species in our group.
The Dascyllus model also seems suitable to study variation in PLDs in the context of biogeography of coral reef associated fishes. Of the three species that occur in the Red Sea, D. marginatus is an Arabian endemic while D. trimaculatus and D. aruanus are both widespread species, common in most of the Indo-Pacific. In general, pomacentrid species with restricted distributions have shorter PLDs than wide-ranging species (Cowen and Sponaugle, 1997, Wellington and Victor, 1989), although the opposite is observed for labrids (Cowen and Sponaugle, 1997, Victor, 1986). The expected trend is that endemic or geographically-constrained species have shorter PLDs potentially restricting dispersal (Lester and Ruttenberg, 2005, Macpherson and Raventos, 2006, Mora et al., 2003). However, in endemic pomacentrid species the PLDs seem to have a rather non-linear relationship with range size (Thresher et al., 1989). Similarly, most studies assessing correlations between PLDs and biogeographic ranges over a number of species find no link between the two (Macpherson and Raventos, 2006, Victor and Wellington, 2000, Zapata and Herrón, 2002). The exact nature of PLD vs. biogeography remains an open question.
Thus, the objectives of our study are to use the model species-group of D. marginatus, D. aruanus, and D. trimaculatus to 1) assess the influence of environmental parameters such as SST and CHLA on the PLDs of coral reef associated damselfishes with different degrees of ecological specialization in a natural environment inside the Red Sea; 2) investigate variations in PLDs related to differences in biogeographic ranges among closely related species; 3) provide the first PLD-measurements for D. trimaculatus and D. aruanus from the Red Sea and additional measurements from two sites outside the Red Sea as well as 4) provide the first PLD-measurements the first PLDs for D. marginatus from a wide geographic range.
Section snippets
Fish sampling
Clove oil, tweezers, hand nets, and spears were used to collect juvenile and adult specimen from the three Dascyllus species (D. aruanus, D. marginatus, and D. trimaculatus) present in the Red Sea (RS) (Fig. 1). Fishes of different sizes (Fig. 2) and/or from different sampling years (Table 1) were collected for PLD assessment to cover potential temporal variations as much as possible. These were caught at 18 reef sites off the Saudi Arabian coastline and at two sites outside the RS (Indian
Within the Red Sea
The total mean PLDs of all three species differed significantly from each other (F(2144) = 50.453, p < 0.001, Fig. 3). Overall, D. trimaculatus showed the highest mean PLD (24.33 ± 2.02), followed by D. aruanus (23.09 ± 1.92), while D. marginatus exhibited the lowest (19.82 ± 2.92) (Table 2). Significant interspecific differences in PLDs were found among regions (F(3144) = 31.723, p < 0.001, Fig. 5) and intraspecific differences among all three species: between sampling regions (F(3144) = 31.723, p < 0.001, Fig.
Discussion and conclusions
Our study shows that there is a significant link between the pelagic larval duration (PLD) of Dascyllus species and environmental parameters such as mean sea surface temperature (SST) and chlorophyll a (CHLA) content in the Red Sea. In all three study species, we found a gradual and consistent decrease in mean PLD with decreasing latitude along the environmental gradient. Moreover, intra-specific differences in PLD between sampling regions along this gradient were higher in D. marginatus than
Acknowledgments
We would like to thank fieldwork and logistic support provided by KAUST Coastal and Marine Resources Core Lab. For assistance acquiring samples, we thank A. Gusti, M. Roberts, R. Gatins, A. Kattan, G. Bernardi, M. Erdmann, and J.-P. Hobbs. For support with environmental data, we thank D. Raitsos and D. Dreano. We also thank two anonymous referees and S. Agrawal for comments and feedback, as well as J. S. Berdahl for formatting the artwork. Financial support came from KAUST baseline research
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