The effects of terrestrially-derived disturbance gradients in marine waters across coral reefs have been noted from many parts of the world (Edinger et al., 1998; Mallela et al., 2004; Fabricius et al., 2005; Lirman and Fong, 2007; Teichberg et al., 2018). Coral reefs closer to shore are generally characterized by less hard coral abundance, an increase in fleshy algae, a general loss of habitat complexity, and by a decrease in coral and fish species diversity or even complete shifts in the sets of species (Fabricius et al., 2005; Plass-Johnson et al., 2015a, 2018). Anthropogenic impacts can alter the resource availability and predator-prey relationships on a coral reef thus affecting habitat use and the trophic niche of the biotic constituents (Jones and Syms, 1998; Syms and Jones, 2000). Thus, changes in coral reef communities along disturbance gradients may be associated with a change in their trophic structure (Jennings et al., 1995). However, the trophic structure of coral reef communities is highly complex, and discerning the specific change of habitat use of any individual species can be challenging due to the high biological diversity on reefs (Fenner, 2012). Nevertheless, revealing trophodynamics of a coral reef community may allow for better interpretation of community change under varying environmental stress (Done, 1992) and help facilitate management decisions that break negative feedback loops (Glaser et al., 2018).

The trophic niche of an organism has been described as the bionomic portion of a specie's ecological niche, divisible to n dimensions based on the sum of all nutritional resource use (Hutchinson, 1978). Stable isotope ratios of a consumer are closely linked to their diet (Post, 2002) and thus are similar to the bionomic niche axis. The heavier stable nitrogen (¹⁵N) and stable carbon (¹³C) isotopes accrue in consumers with an increase in trophic level (Post, 2002). The isotopic structure of a system depends on the availability of dissolved inorganic nitrogen (DIN) and carbon (DIC) and its use by the system's primary producers (Post, 2002) which can then be reflected at higher trophic levels (Harvey and Kitchell, 2000; Post, 2002; Letourneur et al., 2013). As a result of environmental heterogeneity, seasonality and differences in physiology, primary producers may exhibit variability in isotopic signatures over space and time (Dethier et al., 2013) both within and among species. However, as long as this isotopic variability in the prey items is lower than variance resulting from dietary shifts of their consumers, which can be revealed by sampling of prey items, variance in isotopic signature of the consumers is assumed to be a robust measure of trophic niche width (Bearhop et al., 2004). Recently, multivariate, Bayesian techniques have utilized δ¹⁵N and δ¹³C data to describe the niche width of community members (Bearhop et al., 2004; Newsome et al., 2007; Jackson et al., 2011; Dromard et al., 2013).

Herbivorous fishes can remove excess macrophyte growth that might compete with corals for space and light resources (Bellwood et al., 2006; Hughes et al., 2007; Bonaldo et al., 2014), representing a group of interest with respect to variation in trophodynamics. However, herbivores are diverse in their feeding strategies, with resource preferences varying between erect macroalgae and turf algae (Choat et al., 2002, 2004). Turf algae is recognized as a potential impediment to coral reef development (Jompa and McCook, 2003; Vermeij et al., 2010; Smith et al., 2016; Ford et al., 2018) and thus, understanding how the trophic strategy of turf algae consumers responds to changing environments is important to elucidate the potential implications of environmental change for trophodynamics in reefs.

This study explores variation in the trophic niche space of two consumers of turf algae (Bay, 1999; Ledlie et al., 2007) with different trophic strategies. Individuals of the parrotfish, Chlorurus bleekeri (de Beaufort, 1940), and the farming damselfish, Dischistodus prosopotaenia (Bleeker, 1852), were collected at islands of the Spermonde Archipelago, Indonesia, representing a spatial gradient away from the urban center of Makassar. These reefs have documented variation in habitat composition with relation to disturbance (Edinger et al., 1998; Cleary and Renema, 2007), with low live coral cover and high amounts of coral rubble with increasing turf algae recruitment and abundance (Plass-Johnson et al., 2016a) at the near-shore, impacted reefs. C. bleekeri and D. prosopotaenia were both observed to persist at most of the reefs, potentially reflecting trophic variation associated with habitat structure. Species of parrotfish in the same genus as C. bleekeri have been shown to forage up to 130 m for food resources (Welsh and Bellwood, 2012) while D. prosopotaenia, a farming damselfish, continuously maintains a patch of turf algae approximately one square meter in size (Hoey and Bellwood, 2010). Both fish consume turf algae but recent work suggests that parrotfishes may not be directly targeting this source for their diet (Clements et al., 2016). The goal of the current study is not to reconstruct the diets of the two fishes, but rather to identify changes in their trophic niche, identified through stable isotopes, in association with changes in their environment. Therefore, this study examines the variation of the trophic niches of the two herbivorous fish species across an environmental gradient, assuming that variation in habitat degradation may alter their trophic niche space through modification of available benthic food items; however, it is assumed that variation in the isotopic niche will be greater in C. bleekeri than D. prosopotaenia due to the latter's predisposition to self-maintain its nutritional resources.

Localized disturbances to coral reef ecosystems can involve important alterations to the habitat, and consequently, to the ecological niches of the associated fish communities. Our results agree with previous studies in the Spermonde Archipelago (Edinger et al., 1998, 2000; Sawall et al., 2012; Plass-Johnson et al., 2015a, 2016a,b), where the three sites closer to shore were characterized by low coral cover, higher rubble and higher abundances of turf algae. Cross-shelf variation in these benthic components are related to isotopic metrics of the parrotfish, Chlorurus bleekeri. A positive relationship between rubble and SEA_c and δNR, and a negative relationship with δCR suggest change in resource use and the trophic niche for C. bleekeri while little change in isotopic metrics was observed for the damselfish Dischistodus prosopotaenia.

Given the many sources of variation in isotope values, an increase in δCR of a consumer could be due to the consumption of more food sources across a range of distinct ¹³C values or it could be due to increasing variation in the ¹³C values of each of the food sources. Here, we show that the variability in the δ¹³C values of individual food sources (turf algae and detritus) and other benthic constituents (Padina sp.) do not differ significantly among sites. With the exception of BO, these three groups do differ from each other within sites. This among-site similarity within food, and within-site difference among foods, suggests that the increased δCR is most likely a product of an increasingly diverse diet. Further differences in trophic responses of the two fishes are reflected in the size of their trophic niche (SEA_c) with D. prosopotaenia's being half the size of C. bleekeri. Smaller SEA_c, δCR and δNR indicate the damselfish had a much more restricted diet than the parrotfish.

Although parrotfishes are known to feed from turf algae, their diet also includes detritus, endolithic algae and invertebrates (Choat et al., 2002; Plass-Johnson et al., 2013; Dromard et al., 2014; Clements et al., 2016). Our results indicate that C. bleekeri is assimilating foods with ¹³C values closer to that of Padina sp. (Figure 5). While the exact food source cannot be determined, the significant relationship between δCR, SEA_C, δNR and rubble composition suggests that the alternate source may be indirectly linked to rubble. Because C. bleekeri's δCR becomes narrower, its δNR becomes wider, and the SEA_C gets larger as rubble content increases, it seems that an increase in rubble reduces the number of food sources, but C. bleekeri begins to eat across a broader range of trophic levels. Clements et al. (2016) recently identified parrotfishes as microphages, getting their protein from cyanobacteria and other microorganisms that are (a) living either on or in calcareous substrates, (b) epiphytic on algae or (c) endosymbionts of sessile invertebrates. Nonetheless, the strong relationship between the metrics and rubble indicates that the fish is altering its diet, perhaps toward cyanobacteria and/or microorganisms associated with rubble and away from hard substrate associated biota, suggesting a degree of trophic plasticity based on changes in the habitat structure (Bellwood, 1995; Bonaldo and Bellwood, 2009). Given the reduction in the δCR at SA, it would seem that they become more focused on foods associated with rubble.

In the case of the damselfish, D. prosopotaenia, there was little consistent change in its trophic niche in relation to the environment or distance from shore. Furthermore, there were no significant relationships between benthic components and the Layman's metrics of the damselfish. The farming damselfish feed on their cultivated algae but also on the invertebrate communities and detritus that become established within the algal mat (Wilson and Bellwood, 1997; Dromard et al., 2013), suggesting two possible sources of variability; the invertebrate community and the algae. Recent studies have shown that in the Spermonde Archipelago there is significant variation in invertebrate recruitment in relation to distance from shore (Plass-Johnson et al., 2016a). Undoubtedly variation in invertebrate composition may contribute to some differences in the damselfish values (i.e., BO), however, differences in the species composition of the turf algae among farmed territories may also contribute to variability. Although the sampling for this study attempted to isolate sources of variability in the values of the consumers, further explanation of D. prosopotaenia's trophic niche may need to include a more specific investigation that integrates dietary and behavioral variation (Helfman, 1989).

The mechanisms of species co-existence in highly diverse systems at a small spatial scale are generally maintained via fine-scale niche partitioning by resource specialization (Dobzhansky, 1950). Interestingly, there was never an overlap in the isotopic niche space between the two species at any site. Farming damselfish aggressively defend their territory from other herbivores (Ceccarelli et al., 2005) including parrotfish (Ceccarelli et al., 2011), and the lack of isotopic overlap between D. prosopotaenia over C. bleekeri suggests that the latter may not feed often within the territory of the damselfish. This is further supported by the ~3‰ difference between the fishes in their ¹³C values indicating they may be assimilating completely different foods associated with their diets which is also in line with parrotfishes as microphages (Clements et al., 2016). In nearly every instance however, at any site, the Layman's metrics of the parrotfish were greater than those of the damselfish, likely reflecting their contrasting trophic strategies and also evolutionary history. For instance, the capacity of the parrotfish to forage at greater distances may enable them to target a diversity of resources that is only limited by their home range (Welsh and Bellwood, 2012). While wider foraging ranges may conversely result from reliance on specific, rare resources, their robust jaw morphology (Bellwood, 1994) and a gut able to process high sediment loads (Choat et al., 2002) support the first interpretation, as they allow the fish to process more foods with differing isotopic values. In contrast, farming damselfish actively select the composition of their 1m² territories (Hata and Kato, 2004; Ceccarelli et al., 2005) which counterintuitively can also lead to higher diversity via intermediate disurbance (Gochfeld, 2010). Their restricted niche values suggest that they are reduced in the number of food sources that they assimilate in comparison to the parrotfish. As a result, the SEA_C values and the isotopic ranges (δCR and δNR) of the parrotfish were ~10× and ~1.5-2×, respectively, greater than those of the damselfish. Furthermore, the mean values of the parrotfish were nearly two trophic levels (one trophic level = 3.4‰; Post, 2002) higher for ¹⁵N and 2–3‰ for ¹³C than the damselfish. Thus, although D. prosopotaenia and C. bleekeri are similar in their diets, morphological and behavioral specialization allow them to occupy distinctive dietary niches while coexisting (Cowman et al., 2009).

The occurrence of local and global disturbance to coral reefs is increasing because of climate change and human resource use (Burke et al., 2011). These disturbances result in modifications of the coral reef habitat, and this will have important effects on the associated fish species. In the worst case scenarios, a coral-dominated reef can transition to macroalgal, sponge or other non-coral dominance (Norström et al., 2009). The maintenance of micro—habitat by D. prosopotaenia, a fish that selects specific groups of algae and invertebrates (Hoey and Bellwood, 2010), guarantees resource availability despite a change in the greater environment. In contrast, the ability of C. bleekeri to vary resource utilization across differing habitat compositions is a different response allowing persistence in the face of environmental change. The ability to adapt resource utilization according to a changing habitat seems particularly important given that the species may actively avoid some altered coral reef conditions (Hoey and Bellwood, 2011; Welsh and Bellwood, 2015). Understanding species-specific responses to changed habitat will allow to better predict changes in community due to local and global disturbances.

The analysis of stable isotopes in coral reef food webs offers a powerful tool in elucidating trophic variation among consumers (Cocheret de la Moriniere et al., 2003; Carassou et al., 2008; Kolasinski et al., 2009; Greenwood et al., 2010; Dromard et al., 2013, 2014; Plass-Johnson et al., 2013, 2015b), however further clarification of sources of variability is needed to successfully apply this method within highly diverse systems. In our study, turf algae was more abundant at the degraded sites, however, the parrotfish C. bleekeri may have altered its feeding behavior because of specific structural (rubble) preferences for finding foods with ¹³C values closer to Padina sp. This is further supported by a recent study that identifies cyanobacteria and microorganisms as their target food sources (Clements et al., 2016). Nonetheless, the trophodynamics of parrotfish are still being uncovered (Plass-Johnson et al., 2014; Clements et al., 2016) and the description of the actual feeding capacity of any species will likely take much more work. For parrotfishes, revealing specific diets through isotopes will require the isolation and sampling of endolithic organisms. At the same sites, the farming damselfish D. prosopotaenia was able to maintain its trophic niche, suggesting successful defense of its algal community-related resources. These findings help understand both the intra- and inter-specific capacity of two coral reef fishes to change or maintain their trophic relationship within the context of a changing environment. As the effect of environmental degradation on the trophic strategies still remains poorly understood for many species, the current study helps to identify the capacity of some fishes to respond to habitat loss by employing different trophic niches.

All authors listed, have made substantial, direct and intellectual contribution to the work, and approved it for publication.