Mar Biol DOI 10.1007/s00227-015-2765-y
ORIGINAL PAPER
Interannual variation in the larval development of a coral reef fish in response to temperature and associated environmental factors Ian M. McLeod1,2,3,4 · Rhondda E. Jones1 · Geoffrey P. Jones1,2 · Miwa Takahashi1,5 · Mark I. McCormick1,2
Received: 27 February 2015 / Accepted: 13 October 2015 © Springer-Verlag Berlin Heidelberg 2015
Abstract Climate change is predicted to increase ocean temperatures and influence weather patterns. Here, we examine the influence of temperature and other environmental variables on key early life traits of the coral reef damselfish, Pomacentrus moluccensis, based on ten cohorts of newly settled fish collected over 13 years from around Lizard Island (Great Barrier Reef, Australia). Pelagic larval duration (PLD), larval growth and size at settlement were estimated through otolith microstructure analysis. Multiple regression techniques were used to measure the strength of the associations between these traits and developmental temperature, rain, wind speed and solar radiation. Temperature accounted for 18.4, 26.7 and 25.0 % of the variability in PLD, growth rates and settlement size, respectively. PLDs generally declined and growth rates generally increased with increasing temperatures to ~28 °C, above which PLDs tended to increase and growth rates tended to Responsible Editior: D. Goulet. Reviewed by undisclosed experts. * Ian M. McLeod
[email protected] 1
College of Marine and Environmental Sciences, James Cook University, Townsville, QLD 4811, Australia
2
ARC Centre for Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811, Australia
3
AIMS@JCU, Australian Institute of Marine Science, Townsville, QLD 4810, Australia
4
Present Address: Centre for Tropical Water and Aquatic Ecosystem Research (TropWATER), James Cook University, Townsville, QLD 4811, Australia
5
Australian Institute of Marine Science, PMB 3, Townsville, QLD 4810, Australia
decrease. Size at settlement did not differ between ~25 and ~28 °C, but tended to decrease with increasing temperature above ~28 °C. Together rain, wind speed and solar radiation explained 6.3, 26.3 and 33.7 % of the remaining variability in PLD, growth rates and size at settlement, respectively. Higher wind speeds were generally associated with longer PLDs. Increasing wind, high rainfall and increasing solar radiation were associated with slower growth rates and smaller sizes at settlement. Overall, results suggest that ~28 °C is likely to be a thermal optimum for larval development for this species and other environmental factors associated with climate change including rainfall, wind speed and solar radiation should be considered in predictions of effects on larval fish.
Introduction The earth’s climate is changing rapidly as a result of elevated levels of atmospheric carbon dioxide (Solomon et al. 2007; IPCC 2013). The consequences for marine systems are increasing ocean temperatures (Bindoff 2007) and acidity (Doney et al. 2009). Elevated temperatures are predicted to influence patterns of rainfall and sunshine, and the frequency and magnitude of storms (Meehl 2007; Poloczanska et al. 2007; Lough and Hobday 2011; IPCC 2013). The ability of populations to persist in a changing climate will be heavily influenced by how their most vulnerable life stages respond to environmental change. For many marine fish species, it is the small pelagic larval stage that is the most vulnerable to environmental stressors (Pankhurst and Munday 2011; Pörtner and Peck 2011). Mortality rates are extremely high during this life phase (Leis 1991; Peck et al. 2012), and subtle differences in mortality rates can cause order-of-magnitude differences
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in recruitment from year to year (Houde 1989; Peck et al. 2012). Larval fishes exhibit three interrelated developmental life history traits: pelagic larval duration (PLD), larval growth and size at settlement, each of which has a bearing on larval survival, dispersal and connectivity, and influence patterns of recruitment to adult populations (O’Connor et al. 2007; Cowen and Sponaugle 2009; Munday et al. 2009). Increased growth rates can lead to reduced PLDs because there are strong correlations between growth rates and PLD, with fast-growing larvae often exhibiting shorter larval durations (Houde 1989; Sponaugle and Cowen 1996; Green and Fisher 2004). Slower growing larvae can be subject to selective mortality (Anderson 1988; Gagliano et al. 2007a; D’Alessandro et al. 2013). Moreover, the relationship between growth rates and PLD will influence size at settlement (Sponaugle and Grorud-Colvert 2006), which is important because a larger size at settlement is often associated with increased growth and survival after settlement (Sogard 1997; McCormick and Hoey 2004). The growth and development of larval fishes is affected by genetic and non-genetic contributions from their parents, extrinsic environmental factors and the interplay between their genes and the environment (Peck et al. 2012; Politis et al. 2014). Temperature is one of the most relevant environmental factors influencing growth and development in fishes (Houde 1989; Munday et al. 2008). Typically the tolerance levels of species to temperature are represented as skewed dome-shaped relationships, where rates increase with temperature up to an optimal level and then decrease rapidly with further increases in temperature (Pörtner and Peck 2011). However, whether or not such models explain long-term temporal variation in the response of larval fish to environmental temperature is unknown. A number of studies have examined the effects of seasonal temperature variation (over several months to a few years) on the larval development of reef fishes. These studies have commonly found negative linear relationships between temperature and PLD and positive linear relationships between temperature and larval growth (e.g. McCormick and Molony 1995; Radtke et al. 2001; Green and Fisher 2004; Bergenius et al. 2005; Sponaugle and Grorud-Colvert 2006; Takahashi et al. 2012). Size at settlement has also commonly been found to be negatively correlated with developmental temperature (McCormick and Molony 1995; Radtke et al. 2001; Green and Fisher 2004; Sponaugle and GrorudColvert, 2006). These results have been supported by experimental studies (e.g. Green and Fisher 2004; Gagliano et al. 2007b; McLeod et al. 2013; Munday et al. 2013) and by meta-analysis of field and laboratory studies (Laurel and Bradbury 2006; O’Connor et al. 2007). However, the effects of climate change may only become apparent over
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Mar Biol
longer time scales, with a multitude of factors contributing to normal interannual variation in demographic processes. Some authors have extrapolated from the linear relationships between current-day temperatures and larval development to predict faster larval growth and shorter PLDs in a warmer future, with important effects on larval survival and dispersal (Munday et al. 2009; Kendall et al. 2013). These predications may be valid but have not been tested in the context of long-term observations at one site. Studies of population traits over broad latitudinal ranges can also be informative as to how fishes respond to longterm temperature change. In one of the broadest latitudinal studies to date, McLeod et al. (2015) showed that up to ~28–29 °C the effects of developmental temperature on two reef fishes were similar to those found in temporal studies (faster growth rates and shorter PLDs with increasing temperature), but this trend slowed or reversed in the warmest waters at low latitudes. Whether the relationship between temperature and larval development is similar between temporal and spatial gradients is largely unknown. Comparisons between long-term temporal scales and broad spatial scales (e.g. McLeod et al. 2015) over a similar temperature range will let us know whether ‘snap shot’ studies (studies completed over a short time scale) over geographic scales, with differing temperature ranges, can inform us about temporal changes, with important implications for climate change predictions. In addition to temperature, there are a multitude of other direct and indirect environmental influences on larval development. Other climate-related factors, such as wind speed, rainfall and solar radiation, are also likely to influence early life history traits through larval food intake. Wind speed and rainfall determine small-scale turbulence in coastal waters and may indirectly be an important influence on rates at which larval fish encounter and capture prey (Utne-Palm 2004; Bergenius et al. 2005), which would likely impact growth rates and survival. For example, windinduced turbulence explained 25 % of the variability in larval supply of two species of tropical lizardfishes in Panama (Lemberget et al. 2009). Theoretically, increasing turbulence initially increases prey encounters, then past a certain threshold, decreases prey capture success for predators, and this yields a dome-shaped relationship between larval food consumption rates and turbulence (MacKenzie and Kiorboe 1995; Gallego et al. 1996). Solar radiation may either aid feeding directly by increasing the visibility of prey, or indirectly through its impact on secondary production. Light intensity may also affect vertical distribution, enabling larvae to feed over a range of depths where prey may be concentrated (Kouwenberg et al. 1999). However, solar radiation may directly reduce larval growth rates and survival through the damaging effects of ultraviolet radiation
Mar Biol Table 1 Mean (±SEM) pelagic larval durations, growth rates and settlement sizes of each cohort of Pomacentrus moluccensis from Lizard Island, and mean water temperature, solar radiation, wind speed and rainfall during their individual larval development PLD (days)
Growth rate (mm day−1)
Settlement Water temp. size (mm TL) (°C)
Solar radiation (MJ m−2)
Wind (km h−1)
16 Light traps
18.8 (±0.5) AB
0.60 (±0.02) BCD
13.6 (±0.2) BC
29.0 (±0.01)
24.7 (±0.1)
13.5 (±0.1)
4.5 (±0.1)
Dec 2006
21 Light traps
18.4 (±0.3) AB
0.58 (±0.01) BC
13.2 (±0.2)B
26.7 (±0.03)
27.6 (±0.2)
24.1 (±0.4)
0.3 (±0.1)
Jan 2008
20 Hand nets
17.6 (±0.3) A
0.61 (±0.02) CD
13.1 (±0.2)B
28.6 (±0.03)
26.6 (±0.2)
18.4 (±0.2)
1.2 (±0.6)
Oct 2009
17 Light traps
21.5 (±0.3)C 0.55 (±0.01) AB
14.4 (±0.2) DE
25.5 (±0.01)
25.6 (±0.1)
20.4 (±0.3)
0.01 (±0.01)
Nov 2009
33 Light traps
19.1 (±0.2)B 0.61 (±0.01) BCD
14.0 (±0.1) CDE
25.7 (±0.01)
24.2 (±0.1)
28.7 (±0.3)
0.9 (±0.03)
Dec 2009
22 Light traps
18.8 (±0.2) AB
0.64 (±0.01) DE
14.5 (±0.2) EF
27.8 (±0.03)
25.1 (±0.03)
23.6 (±0.1)
1.7 (±0.03)
Feb 2010
15 Light traps
18.1 (±0.3) AB
0.69 (±0.01) E
15.0 (±0.1)F
29.0 (±0.01)
20.5 (±0.1)
18.2 (±0.1)
3.5 (±0.02)
Oct 2010
14 Light traps
18.6 (±0.3) AB
0.63 (±0.01) CD
14.2 (±0.1) CD
27.2 (±0.003)
23.3 (±.1)
27.0 (±0.1)
0.8 (±0.1)
Jan 2011
27 Hand nets
19.2 (±0.2)B 0.50 (±0.01) A
12.1 (±0.1)A
29.6 (±0.02)
20.7 (±0.1)
20.7 (±0.2)
12.4 (±0.3)
Oct 2011
22 Light traps
18.2 (±0.3) AB
13.7 (±0.1) BCD
26.9 (±0.05)
24.3 (±0.2)
27.4 (±0.4)
3.4 (±0.1)
Sampling month
N
Dec 1998
Capture method
0.62 (±0.02) CD
on nucleic acids, through epidermal damage (Zagarese and Williamson 2001), or reduce survival by making larvae more visible to their predators. The aim of the present study was to examine the longterm effects of a temperature gradient and other environmental factors on key early life history traits of a common damselfish, Pomacentrus moluccensis, based on collections of juveniles collected over 13 years at Lizard Island, Great Barrier Reef (GBR), Australia. Otolith microstructure analysis was undertaken to estimate PLD, average larval growth and size at settlement. Regression analyses were applied to determine the influence of water temperature and other associated environmental factors (wind speed, rainfall and solar radiation) on these life history traits.
Methods Study site and species This study was undertaken at the Lizard Island Group (14°40′S, 145°27′E), a mid-shelf reef, situated 30 km from the Australian mainland in the northern GBR. The species investigated was the lemon damselfish, Pomacentrus moluccensis (Pomacentridae: Bleeker, 1853), a common, coral-associated species on shallow coral reefs in the western Pacific (Randall et al. 1990). Pomacentrus moluccensis
Rainfall (mm day−1)
lay demersal eggs during a reproductive season from October to March on the GBR (Randall et al. 1990) that hatch into free-swimming larvae that develop in the pelagic environment for 15–23 days (Milicich et al. 1992; Booth et al. 2000). Sample collection To investigate variation in larval traits in relation to water temperature, larvae were either collected using an array of light traps (see Meekan et al. 2001, for design) set 100 m off the reef on the western side of Lizard Island or newly settled individuals (8.5 mm day−1) or low (20 km h−1). There was an interaction between wind speed and solar radiation. At low wind speeds (20 km h−1), increasing solar radiation tended to be associated with decreasing growth rates, but at higher wind speeds (>20 km h−1) increasing solar radiation had no effect. Additionally, when rainfall was low, increasing solar radiation was associated with a decrease in growth rate, but at high rainfall the effect of solar radiation was reduced (Figs. 2, 3). Rain and solar radiation were identified as having strong negative influences on size at settlement (Table 3). There were also significant interactions between rain and solar radiation, and wind and solar radiation (Table 3). The patterns of influence of wind, rain and solar radiation on size at settlement closely mirror the influence of these factors on growth. For example, at low solar radiation (
