Elsevier

Marine Pollution Bulletin

Volume 105, Issue 2, 30 April 2016, Pages 566-574
Marine Pollution Bulletin

Productivity and sea surface temperature are correlated with the pelagic larval duration of damselfishes in the Red Sea

https://doi.org/10.1016/j.marpolbul.2015.11.045Get rights and content

Highlights

  • Pelagic larval durations (PLDs) of damselfishes in the Red Sea

  • Higher productivity & temperature correlate with shorter PLDs of Dascyllus.

  • Dascyllus may be an ideal group to study variations in PLD and biogeography.

  • First PLD measurements from the Red Sea for D. trimaculatus and D. aruanus

  • First spatially wide-ranging PLD assessment for the endemic D. marginatus

Abstract

We examined the variation of pelagic larval durations (PLDs) among three damselfishes, Dascyllus aruanus, D. marginatus, and D. trimaculatus, which live under the influence of an environmental gradient in the Red Sea. PLDs were significantly correlated with latitude, sea surface temperature (SST), and primary production (CHLA; chlorophyll a concentrations). We find a consistent decrease in PLDs with increasing SST and primary production (CHLA) towards the southern Red Sea among all species. This trend is likely related to higher food availability and increased metabolic rates in that region. We suggest that food availability is a potentially stronger driver of variation in PLD than temperature, especially in highly oligotrophic regions. Additionally, variations in PLDs were particularly high among specimens of D. marginatus, suggesting a stronger response to local environmental differences for endemic species. We also report the first average PLD for this species over a broad geographic range (19.82 ± 2.92 days).

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

References (65)

  • V.N. Biktashev et al.

    Phytoplankton blooms and fish recruitment rate: effects of spatial distribution

    J. Plankton Res.

    (2003)
  • B. Bjørnsson et al.

    Optimal temperature for growth and feed conversion of immature cod (Gadus morhua L.)

    ICES J. Mar. Sci.

    (2001)
  • D.J. Booth et al.

    Pelagic larval duration is similar across 23° of latitude for two species of butterflyfish (Chaetodontidae) in eastern Australia

    Coral Reefs

    (2011)
  • R.K. Cowen et al.

    Relationships between early life history traits and recruitment among coral reef fishes

  • D.H. Cushing et al.

    The growth and death of fish larvae

    J. Plankton Res.

    (1994)
  • J.D. DiBattista et al.

    On the origin of endemic species in the Red Sea

    J. Biogeogr.

    (2015)
  • J.D. DiBattista et al.

    A review of contemporary patterns of endemism for shallow water reef fauna in the Red Sea

    J. Biogeogr.

    (2015)
  • A. Duputié et al.

    An empiricist's guide to theoretical predictions on the evolution of dispersal

    Interface Focus

    (2013)
  • J. Fontes et al.

    Temporal variability of larval growth, size, stage duration and recruitment of a wrasse, Coris julis (Pisces: labridae), from the Azores

    Sci. Mar.

    (2010)
  • T.J. Froukh et al.

    Genetic population structure of the endemic fourline wrasse (Larabicus quadrilineatus) suggests limited larval dispersal distances in the Red Sea

    Mol. Ecol.

    (2007)
  • E.C. Giles et al.

    Exploring seascape genetics and kinship in the reef sponge Stylissa carteri in the Red Sea

    Ecol. Evol.

    (2015)
  • K. Grorud-Colvert et al.

    Variability in water temperature affects trait-mediated survival of a newly settled coral reef fish

    Oecologia

    (2011)
  • S.K. Heinz et al.

    Speciation and the evolution of dispersal along environmental gradients

    Evol. Ecol.

    (2009)
  • E.D. Houde

    Comparative growth, mortality, and energetics of marine fish larvae: temperature and implied latitudinal effects

    Fish. Bull.

    (1989)
  • E.D. Houde et al.

    Fish early life dynamics and recruitment variability

    Am. Fish. Soc. Symp.

    (1987)
  • E.D. Houde et al.

    Ecosystem- and taxon-specific dynamic and energetics properties of larval fish assemblages

    Bull. Mar. Sci.

    (1993)
  • I. Hunt et al.

    Effects of temperature on morphological landmarks critical to growth and survival in larval Atlantic cod (Gadus morhua)

    Mar. Biol.

    (1996)
  • M.F. Landaeta et al.

    Larval distribution and growth of the rockfish, Sebastes capensis (Sebastidae, Pisces), in the fjords of southern Chile

    ICES J. Mar. Sci.

    (2006)
  • S.E. Lester et al.

    The relationship between pelagic larval duration and range size in tropical reef fishes: a synthetic analysis

    Proc. Biol. Sci.

    (2005)
  • A. Lo-Yat et al.

    Extreme climatic events reduce ocean productivity and larval supply in a tropical reef ecosystem

    Glob. Chang. Biol.

    (2011)
  • D.F. Lozano-Cortés et al.

    Colony size-frequency distribution of pocilloporid juvenile corals along a natural environmental gradient in the Red Sea

    Mar. Pollut. Bull.

    (2015)
  • O.J. Luiz et al.

    Adult and larval traits as determinants of geographic range size among tropical reef fishes

    PNAS

    (2013)
  • Cited by (0)

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