1. Introduction
Reef building, scleractinian (“hard”) corals have specific environmental tolerances (Kleypas et al. 1999 [
1]), such that individual demography, population dynamics and community structure vary markedly along environmental gradients (e.g., Done 1982 [
2]; Harriot 1999 [
3]; Anderson et al. 2017 [
4]). Most notably, there are clear and well-defined latitudinal limits to growth and abundance of scleractinian corals and therefore, reef accretion (Buddemeier and Kinzie 1976 [
5]; Kleypas et al. 1999 [
1]; Muir et al. 2015 [
6]), which are constrained at high latitudes by lower temperature, aragonite saturation and light levels. Even within the latitudinal limits of coral reef accretion, there are declines in diversity of coral assemblages with increasing latitude (Bellwood and Hughes, 2001 [
7]). For those coral species that are distributed over a wide latitudinal extent, there are also differences in demography linked to differences in local environmental conditions (e.g., Anderson et al. 2015 [
8]). In general, corals grow more slowly at high latitude locations, which is largely attributed to thermal constraints on coral growth (e.g., Harriot, 1999 [
3], Anderson et al. 2015 [
8], Pratchett et al. 2015 [
9]) and this may in turn, lead to lower population turnover and reduced resilience (Hoey et al. 2011 [
10]).
Despite considerable research on large-scale (biogeographical) patterns in coral assemblages and the various factors that contribute to these patterns (Bellwood and Hughes, 2001 [
7]; Connolly et al. 2003 [
11]; Keith et al. 2013 [
12]), variation in coral populations and communities is often very pronounced even at relatively small spatial scales (e.g., with depth, aspect and distance from shore), associated with steep gradients in environmental conditions (Done 1982 [
2]; Cleary et al. 2005 [
13]). Cross-shelf variation in the abundance, biodiversity and composition of benthic reef assemblages is particularly pronounced (e.g., Done 1982 [
2]; Wilkinson and Cheshire 1989 [
14]; Fabricius and De’Ath 2001 [
15], Wismer et al. 2009 [
16]). In general, near shore (or inshore) reef habitats have higher abundance of fleshy macroalgae and coral assemblages are dominated by stress-tolerant species, whereas offshore reef habitats have higher cover of crustose coralline algae and higher diversity of corals (but see Lirman and Fong 2007 [
17]). There are also marked differences in the abundance and composition of fish assemblages between inshore and offshore reefs (e.g., Williams 1982 [
18]; Williams and Hatcher 1983 [
19]; Russ 1984 [
20]; Hoey and Bellwood 2008 [
21]; Emslie et al. 2010 [
22]), with possible consequences for the structure and functioning of reef ecosystems.
Cross-shelf variation in the abundance, biodiversity and composition of coral reef organisms may be ascribed to natural and inherent gradients in environmental conditions, such as depth and wave exposure (Bellwood and Wainwright 2001 [
23]). However, anthropogenic transformation of coastal environments, involving land clearing, coastal development and dredging, are causing increasing sedimentation, eutrophication and pollution (Hughes et al. 2015 [
24]; Kroon et al. 2016 [
25]), which have disproportionate impacts on near shore systems. Increasing levels of both suspended sediment and sediment deposition have generally negative consequences for corals (Loya, 1976 [
26]; Riegl and Branch 1995 [
27]; Fabricius 2005 [
28]; Weber et al. 2012 [
29]), causing light attenuation and reduced photosynthesis versus tissue abrasion and smothering, respectively. Some coral species are capable of withstanding increased exposure to sedimentation by actively feeding on particulate matter (Anthony & Fabricius, 2000 [
30]), though increased levels of sedimentation often have catastrophic impacts on established coral assemblages (Dodge & Vaisnys, 1977 [
31]) if not sublethal effects such as suppressed coral growth (Fabricius 2005 [
28]).
The purpose of this study was to quantify cross-shelf variation in annual linear extension (ALE) for three different taxa of branching corals;
Acropora nasuta,
Pocillopora spp. and
Stylophora pistillata. The focus on branching corals was intended to complement previous studies (e.g., Lough and Barnes 2000 [
32], Carricart-Ganivet & Merino, 2001 [
33]) that have explored spatial variation (at a wide range of different scales) in growth of massive corals, for which growth can be retrospectively measured from skeletal features (Pratchett et al. 2015 [
9]). Estimating growth of branching corals meanwhile, requires real time measurements of changes in weight or external dimensions. Branching corals also make disproportionate contributions to the structure and topographic complexity of reef habitats, which supports high abundance and diversity of reef organisms (Messmer et al. 2011 [
34]). Moreover, branching corals are amongst the fastest growing corals (Pratchett et al. 2014 [
9]) but are also very susceptible to environmental change (Hughes et al. 2018 [
35]). Given the sustained and ongoing degradation of near shore environments (Kroon et al. 2016 [
25]), as well as the sensitivity of branching corals to sedimentation (Fabricius 2005 [
28]; Weber et al. 2012 [
29]), we expected to find markedly lower growth rates on inshore reefs (located within 20 km of the coastline) compared to corals growing at reefs located up to >35 km offshore.
4. Discussion
Growth rates of corals vary taxonomically, spatially and temporally and have an important role in structuring coral assemblages and reef habitats (Pratchett et al. 2015 [
9]). Average ALE recorded for scleractinain corals ranges from <2 mm·y
−1 for
Siderastrea spp. up to 172 mm·y
−1 for
Acropora pulchra and is generally higher for branching versus massive corals (Pratchett et al. 2015 [
9]). In this study, average ALE was highest (23.56 mm·y
-1 ± 0.86 SE) for
Pocillopora spp. Though we were not certain of the taxonomic identity of these corals, nor whether there were possibly more than one species considered within this complex (Schmidt-Roach et al. 2014 [
36]), our growth rates correspond with growth rates recorded previously for colonies nominally considered to be
P. damicornis (Anderson et al. 2015 [
8]) that used the same techniques. Notably, growth rates recorded for
Pocillopora colonies exceeded that of
A. nasuta. In general,
Acropora corals exhibit the highest growth rates and previous estimates of ALE for
A. nasuta (39.2–52.8 mm·y
−1) are much higher than were recorded herein (Pratchett et al. 2015 [
9]), even within reef habitats (shallow, obliquely exposed, reef crests on mid-shelf and outermost reefs) where these corals predominate. Similarly, published growth rates for
S. pistillata are generally much higher (15.05–24.61 mm·y
−1; Pratchett et al. 2015 [
9]) than were recorded in this study (11.81 mm·y
−1 ± 0.73 SE). Intraspecific variation in the growth rates of corals, especially among widely separated geographic locations, is often attributed to differences in environmental conditions and especially temperature (Carricart-Ganivet 2004 [
41]; Lough 2008 [
42]). In particular, growth rates of corals may be constrained at both low and high temperatures (Pratchett et al. 2015 [
9]). Low rates of ALE recorded in this study, relative to growth rates reported for the same species in other locations, may reflect higher than normal temperatures that occurred across much of the GBR in 2016 (Hughes et al. 2017 [
43]). During the course of this study, corals were exposed to DHW values of 2–6 °C-weeks (
Figure 1) and moderate levels of bleaching were recorded, especially on offshore reefs in this region (Hughes et al. 2017 [
43]). However, reef specific DHW did not account for observed differences in growth rates (
Table 2). Elevated temperatures may have accounted for the poor survival of
A. nasuta and
S. pistillata at mid-shelf sites, though heat stress experienced at these locations was lower than for offshore locations. More importantly, differential heat stress throughout the entire study period (though not measured here) may have contributed to observed spatial patterns of coral growth (Anderson et al. 2018 [
44]), potentially suppressing coral growth and calcification at offshore locations more so than at other locations.
Although species-specific growth rates recorded in this study are lower than reported previously, there were no apparent differences in ALE between inshore, mid-shelf and outer-shelf sites. Many studies have reported comparatively low rates of coral growth or calcification in near shore environments linked to high or elevated levels of suspended sediments (e.g., Tomascik & Sander 1985 [
45]; Guzmán et al. 2008 [
46]; Sowa et al. 2014 [
47]). We had expected, therefore, that coral growth would be highest at offshore locations, which are furthest removed from land-based sources of sediment, nutrients and other pollutants. However, the few studies that have explicitly studied cross-shelf variation in growth rates of select coral species (massive
Porites; Scoffin et al. 1992 [
48], Lough and Barnes 2000 [
32] and
Orbicella (formerly
Montastraea)
annularis; Carricart-Ganivet & Merino, 2001 [
33] Manzello et al. 2015 [
49]), show decreasing ALE with distance from shore. All we can really conclude in this study is that growth rates of all three branching coral taxa were not any lower at sites on inshore reefs (Orpheus and Pelorus Islands), compared to sites at mid-shelf (Bramble and Trunk Reefs) and outer-shelf reefs (Pith and Unnamed Reefs). One possible explanation is that elevated temperatures on outer-shelf reefs (where corals were exposed to greater cumulative heat stress than at mid-shelf or inshore locations) suppressed coral growth and calcification, such that overall growth rates were similar to that of corals on the high continental islands that had conspicuously higher levels of sedimentation and turbidity.
Environmental constraints on coral growth and calcification are not always manifest as changes in ALE (Brown et al. 1990 [
50]). Scleractinian corals are indeed capable of maintaining or increasing linear extension, despite reductions in calcification, by sacrificing skeletal density (Carricart-Ganivet & Merino 2001 [
33]; Hoegh-Guldberg et al. 2007 [
51]), which presumably impacts on skeletal integrity and resistance to physical disturbances. When comparing cross-shelf variation in growth process, both Lough and Barnes (2000 [
32]) and Carricart-Ganivet & Merino (2001 [
33]) found that skeletal density increased with distance from shore. This may be a necessary response to increase skeletal integrity and persistence in the face of increased wave exposure and hydrodynamic forcing. Conversely, lower levels of wave action on inshore reefs may allow corals to persist with comparably lower skeletal densities, allowing for faster rates of linear extension. Risk and Sammarco (1991 [
52]) suggested that the low densities of
Porites corals at inshore sites on the GBR reflect inhibition of calcification by elevated nutrients, though overall rates of calcification for massive
Porites are actually higher on inshore reefs (Lough & Barnes 1992 [
53]), which combined with reduced skeletal density, result in higher rates of ALE. As with previous studies, we found differences in the skeletal density of corals growing on different reefs, which were related to shelf position. However, skeletal density was higher on inshore, rather than offshore reefs (
Figure 3). As such, differences in skeletal densities do not account for (but compound upon) differences in linear extension. This suggests that overall rates of calcification for the branching corals considered in this study (
A. nasuta,
Pocillopora spp. and
S. pistillata) may actually be higher at sites on the inshore reefs, compared to colonies growing at sites on mid- and outer-shelf reefs.
It is incontrovertible that elevated sedimentation and eutrophication can have adverse effects on the growth, reproduction and demography of scleractinian corals, as shown in experimental studies (Humphrey et al. 2008 [
54]) as well as highly perturbed environments (Dodge & Vaisnys, 1977 [
31]). However, most experimental studies use extreme levels of sedimentation that poorly reflect predominant conditions that occur even on fringing coastal reefs (Jones et al. 2016 [
55]). These extreme treatment levels were justified based on early erroneous estimates of sedimentation in the field (Jones et al. 2016 [
55]) that failed to account for sediment resuspension and flux. While sedimentation is a prominent feature of nearshore reefs and one of the major factors that differentiates inshore reefs from offshore systems (Wolanski et al. 2005 [
56]), extreme levels of sediment resuspension and turbidity are often short-lived (Browne et al. 2013 [
57]). Moreover, high levels of sedimentation are restricted to specific habitats, where coral assemblages are dominated by species (e.g.,
Goniopora and
Turbinara) that are predominantly heterotrophic and can withstand prolonged turbidity and sediment deposition (Browne et al. 2012 [
57]). Ultimately, fine-scale heterogeneity in environmental conditions enables branching corals (e.g.,
Acropora) to grow at some sites (Browne et al. 2013 [
56]), even if this is more restrictive than occurs on reefs further offshore. In this study, for example, we compared growth rates of corals in very shallow environments (1–3 m), where we found highest abundance of the specific study species. It is likely however, that these corals might be much more restricted in their depth distribution on near shore reefs due to higher levels of turbidity and light attenuation.
The results and conclusions of this study are limited by inherent constraints in the method used to measure coral growth. Although ALE is among the most commonly used metric to measure coral growth and is broadly comparable across different types of corals (Pratchett et al. 2015 [
9]), it does not fully account for complexities in the way that corals (especially, branching corals species) actually deposit calcium carbonate, which is the main rate limiting process for coral growth. This study also used the vital stain (Alizarin Red), requiring corals to be sacrificed to record change in physical dimensions, which provides only a single time-averaged estimate of coral growth across the period between staining and subsequent collection (Morgan & Kench 2012 [
58]). Recent advances in underwater photogrammetry enable 3D reconstructions from images of individual coral colonies which, when compared over time, can provide much more holistic, precise and higher resolution measures of growth (Ferrari et al. 2017 [
58]). Moreover, 3D photogrammetry does not require that corals be manipulated or ultimately collected (Ferrari et al. 2017 [
59]), which otherwise imposes considerable risks and inherent constraints on the sample size and design. This study provides the first test of cross-shelf variation in growth rates of branching corals, though much more expansive sampling (making use of new methods to better represent the size and shape of individual coral colonies) is still warranted.