Abstract
Herbivorous fishes are an important component of coral reef systems worldwide, but their nutritional ecology is poorly understood, particularly the relationships between the taxonomic composition and the nutritional composition of their diets. We compared dietary composition with % carbon, % nitrogen and C:N ratios of diet in four species of nominally herbivorous fishes from the Southwestern Atlantic and used literature values to calculate proportional contributions of dietary items to total nitrogen intake. Both Sparisoma axillare (Labridae, Scarinae) and Acanthurus chirurgus (Acanthuridae) had a diet composed mainly of detritus, with contributions of red algae. However, the diet of S. axillare displayed higher %N and a lower C:N ratio, although animal material made only a slightly greater contribution to total nitrogen intake than in A. chirurgus. Kyphosus sectatrix (Kyphosidae) ingested mainly carbon-rich corticated algae, while Diplodus argenteus (Sparidae) had a varied, omnivorous diet. These results indicate that conventional diet analysis may not reveal important interspecific differences in nutrient intake and that a reassessment of the nutrient intake of different herbivorous fishes is required to fully understand their ecology. This finding highlights the fact that foods of nominally herbivorous fishes vary greatly in nutritional quality. Moreover, conventional dietary categories such as detritus may exhibit considerable heterogeneity in taxonomic and nutritional composition, suggesting a previously unrecognised level of dietary selectivity in this fish assemblage.
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Introduction
One of the main goals of ecological research is to determine how nutrients and energy flow through ecosystems and are partitioned among different trophic levels (Paine 1996; Rooney et al. 2006; Bierwagen et al. 2018). The study of nutritional ecology is central to ecological research since it deals with the relationship between animals and their food, encompassing aspects such as food composition, acquisition and processing (Raubenheimer et al. 2009). In this sense, herbivorous animals represent an important group for nutritional research as they transfer nutrients and energy from primary producers to higher trophic levels. Our understanding of herbivory in terrestrial systems is underpinned by a vast literature on the selection and processing of nutritional resources by vertebrate groups including mammals (Van Soest 1994), lizards (Bjorndal 1997) and birds (Levey and Martínez del Rio 2001).
Nominally herbivorous fishes are recognised as an important ecological component of reef environments due to their high contribution to the total biomass of different habitats and their influence on the benthic communities (Horn 1989; Choat and Clements 1998; Ferreira et al. 2004; Cordeiro et al. 2016). Through their intense feeding activity, herbivorous fishes can influence the composition of benthic biota (Carpenter 1986; Smith et al. 2001; Burkepile and Hay 2006) and are generally regarded as one of the most important groups of fish on tropical reefs (Bellwood et al. 2004). Most of the research on herbivorous reef fishes classify them in discrete categories that can be broadly clustered into browsers/algivores and scrapers/grazers/detritivores (e.g. Burkepile & Hay 2006; Green & Bellwood 2009; Bonaldo et al. 2014; Adam et al. 2015). Nevertheless, among herbivores there are species that feed on different food sources, including macroalgae, turfing algae, cyanobacteria, detritus and zooplankton, among others (Choat et al. 2002, 2004; Ferreira and Gonçalves 2006). This variety is better demonstrated as a continuum, with macroalgivores with carbohydrate-rich diets at one end of the spectrum and detritivorous protein-scavengers at the other (Crossman et al. 2005).
Gut content analysis has been used for decades to assess diet in herbivorous fishes (e.g. Randall 1967), but since species possess different food processing modes, the extent to which this method reflects nutritional resources is likely to be variable depending on the species studied. As an example, parrotfishes (Labridae, Scarinae) possess pharyngeal jaws, which grind ingested material to very small fragments, hampering the identification of gut contents (Choat et al. 2002). Moreover, the identification of food items does not indicate their nutritional content or how they may contribute to overall nutrient intake. Many studies consider that algae represent low-quality food compared to animal material (Lobato et al. 2014), despite great variation in their nutritional composition (Montgomery and Gerking 1980; Barbarino and Lourenço 2009; Angell et al. 2015). Furthermore, interspecific variation in post-ingestive processing may influence the extent to which various species can extract nutrients from different food items. Although recent studies using stable isotope and fatty acid analyses (Piché et al. 2010; Dromard et al. 2015; McMahon et al. 2016) recognized that herbivorous fishes have distinct nutritional profiles, many studies do not consider diet beyond broad categories and fail to capture the complexity of the resource used (Clements et al. 2017). An integrative, multi-faceted approach is required that takes into account what foods are ingested, the nutritional composition of these foods and post-ingestive processing to understand the trophic ecology of this fish assemblage (Choat et al. 2004; Clements et al. 2009, 2017).
The objective of the present study was to examine the relationships between diet as quantified by traditional gut content analysis and diet as quantified by carbon and nitrogen content (as nutritional proxies). We examined four nominally herbivorous fish species from the Southwestern Atlantic that differ in food processing modes, and that are usually classified in different functional groups: one browser/algivore, two scraper/detritivores and one omnivore known to feed heavily on algae. Our main goal was to test the hypothesis that conventional methods used to characterise diet reflected interspecific differences in nutrient intake and nutritional targets among these fishes.
Materials and methods
Study area
Sampling was carried out between February and March 2013 (Austral Summer) at Arraial do Cabo (22°57′S, 42°01′W) on the southeastern coast of Brazil. This region is of great ecological and biogeographic importance as it accumulates species with both tropical and temperate affinities (Ferreira et al. 2001, 2004). Reefs in the region are predominantly rocky and covered by a rich epilithic algal community (EAC) and the zoanthid Palythoa caribaeorum, while corals and other invertebrates occupy a lesser proportion of the substratum (Ferreira et al. 1998a; Rogers et al. 2014). The richness of reef-associated fish fauna in the region is relatively high (within the Brazilian province), with the occurrence of at least 13 species of nominally herbivorous fishes (Cordeiro et al. 2016). Although local upwelling brings up waters colder than 18 °C (Valentin 1984), the study sites are protected from this upwelling and generally experience temperatures between 18 and 25 °C.
Study species
The Southwestern Atlantic has a depauperate fish fauna compared to other biogeographical regions such as the Indo-Pacific and the Caribbean (Kulbicki et al. 2013), and this is reflected in the number of herbivorous fishes in this area. Fish herbivory is restricted to a few families, most importantly Kyphosidae, Acanthuridae, Labridae (Scarinae) and Pomacentridae (Ferreira et al. 2004; Floeter et al. 2005), with contributions from omnivorous species belonging to the families Sparidae, Monacanthidae and Pomacanthidae (Ferreira et al. 2004; Dubiaski-Silva and Masunari 2006; Mendes et al. 2015). Four species were selected as they represent different feeding modes and phylogenetic affinities: the macroalgivore Kyphosus sectatrix (Kyphosidae), the detritivore-herbivores Sparisoma axillare (Labridae, Scarinae) and Acanthurus chirurgus (Acanthuridae), and the omnivore Diplodus argenteus (Sparidae). Previous work on the diets of these study species identified K. sectatrix as eating mainly brown macroalgae (Ferreira and Gonçalves 2006), S. axillare and A. chirurgus ingesting mainly detritus and filamentous algae (Ferreira and Gonçalves 2006) and D. argenteus as an omnivore that ingests a broad range of food items (Dubiaski-Silva and Masunari 2006). All these species are known to ingest algae to some extent and are abundant throughout the study area (Cordeiro et al. 2016).
Adult fish were collected with a speargun at different sites throughout the study area (Table 1) with all collections restricted to the afternoon, when feeding rates of most herbivorous fishes attain their peak and guts are full (Ferreira et al. 1998b; Zemke-White et al. 2002; Choat et al. 2004). The number of individuals sampled varied among species in accordance to their availability during sampling (22 K. sectatrix, 10 S. axillare, 18 A. chirurgus, 13 D. argenteus). Sample size was tested to ensure that the diet of each species was accurately represented (Fig ESM1). Once collected, specimens were removed from water, killed by pithing (when necessary) and placed on ice prior to transportation to the laboratory where they were measured (fork length), weighed (in grammes) and had their alimentary tracts removed (see Table 1). In species with a distinct stomach (K. sectatrix, A. chirurgus and D. argentus) just the stomach content was stored, but in S. axillare, which lacks a distinct stomach (Clements and Choat 2018), the proximal unsacculated region of the intestine was sampled. Gut contents were divided in two equivalent subsamples: one used to identify dietary items (gut content analysis) and the other for nutritional analysis. The former subsample was frozen (− 20 °C) until analysis, and the latter immediately placed in liquid nitrogen, then freeze-dried to constant mass and stored in a freezer (− 20 °C). Handling time between collection and processing was as short as possible to prevent changes in nutrient concentration (following Crossman et al. 2005).
Dietary analysis
Material for diet analysis was thawed at the laboratory before analysis. The subsample of gut content material for dietary analysis from each individual was evenly spread on a Petri dish positioned over a grid with 50 marked points. The items over each point were recorded and counted under a stereoscopic microscope (50 × magnification). Dietary items were identified to the lowest taxonomic category and sorted into groups (Table 2) according to taxonomy and morphological structure (Steneck and Dethier 1994). Although detritus can be defined as “dead and decaying primary producer material, which normally becomes detached from the primary producer after senescence” (Lartigue and Cebrian 2012; Hundt and Simons 2018), it is often difficult to visually discriminate living components such as bacteria, diatoms and cyanobacteria from the non-living component (Wilson et al. 2003). We thus applied this term broadly and identified detritus in the dietary analyses as any amorphic organic material found.
Nutritional analysis
Freeze-dried samples used in nutritional analysis were homogenised on a Retsch MM301 ball and mill homogenizer at 25 repetitions/second for 15 s. Immediately before grinding, samples were bathed in liquid nitrogen to avoid over-heating, which can change nutrient content. Measurements of percentage values for carbon, hydrogen and nitrogen were assessed in duplicate using an elemental analyser Exeter CE-440 located at the Auckland University of Technology (AUT). Nitrogen content is usually related to protein, which represents an important nutrient for fishes (Weber and Haman 1996). Likewise, diets with high concentration of carbon are usually associated with the ingestion of carbohydrate-rich plant material (Crossman et al. 2005). From the values of nitrogen and carbon, the C:N ratios for each individual diet were obtained. The C:N ratio is widely used in ecology as a proxy for the relative nutritional value of a food type, with lower values generally thought to indicate more nutritious dietary sources of protein (Wilson et al. 2003). Thus, nitrogen and carbon measurements from the gut contents, along with C:N ratios, were used here as proxies for the nutritional value of the foods ingested by the study species.
We also estimated the proportional contribution to total nitrogen intake of each of the major food categories in the four study fish species by combining: (1) the dietary proportions of food categories from gut content analysis, (2) the total nitrogen content of the diet in each of the four species and (3) literature data on nitrogen concentration in each of the main food categories in the fish diets. This was done as follows. First, we surveyed the literature for the nitrogen content of each of the most important food item categories found in our gut content analysis. Second, we took the proportional contribution made by each food item to the total diet of each fish species and divided these values by the total nitrogen content of the diet for each study fish species. Third, we multiplied this value by the nitrogen content of each food item as follows: NIi = (Di/N) × FNi, where NIi is the nitrogen intake of the item i to the diet of a given species, Di is the contribution of the item i to the diet of a given species, N is the amount of dietary nitrogen and FNi is the value of nitrogen content of each food type i. This value was finally turned into a percentage to give the relative contribution made by each dietary food category to total nitrogen intake for each of the study fish species.
Data analysis
Because our data did not meet parametric assumptions of normality and homogeneity of variances, we performed a one-way permutation-based Analysis of Variance (ANOVA) to compare the contribution of the different food items for each one of the four study species using the package ‘lmPerm’(Wheeler and Torchiano 2016), followed by a Tukey HSD post hoc test to assess the differences. In order to visualise the similarities and differences in the diets of the four fish species, a Principal Components Analysis (PCA) was applied to gut content analysis data using the package ‘vegan’ (Oksanen et al. 2017). We used the Schoener index (Wallace 1981) to assess dietary overlap between each pair of species using the package ‘spaa’ (Zhang 2016). This index varies between 0 and 1 with higher values indicating higher overlap. We also used a one-way permutation-based ANOVA for each nutrient (%C, %N and C:N ratio) with Tukey HSD post hoc test to compare nutrient concentrations among species using a similar aforementioned approach. All analyses were performed using the software R (R Core Team 2017).
Results
Thirty-four different food items were identified in the diet of the four study fish species (Table 2), and these were grouped into 15 categories. The species with the most diverse diet was A. chirurgus with 30 food items, followed by D. argenteus (23), K. sectatrix (16) and S. axillare (14). Of the 34 food items identified, only eight were present in the diet of all four fish species (i.e. Cyanobacteria, Polysiphonia spp., Jania spp., Gelidiella acerosa, Gelidium pusillum, Cladophora sp., Bryopsis sp. and Sphacelaria sp.), and only A. chirurgus and D. argenteus ingested exclusive food items not found in other species (three and four, respectively) (Table 2).
We detected a large variation in the diets of all four study species (Table ESM1). The most abundant food item in the diet of A. chirurgus (F = 87.56, P < 0.001) was detritus, with four groups of algae having secondary importance (i.e. articulated calcareous, filamentous and corticated red algae, and green filamentous categories). Other items such as brown algae, bryozoans and arthropods were also present in very small quantities (Fig. 1, Table ESM2). Detritus was also the dominant food item in S. axillare (F = 68.22, P < 0.001), followed by both articulated calcareous and filamentous red algae. Cyanobacteria, red corticated algae and arthropods were also abundant in gut contents, while others items such as green and brown filamentous algae were present in lower amounts (Fig. 1, Table ESM3). The diet of K. sectatrix (F = 66.51, P < 0.001) was dominated by brown and red corticated algae, with other algae (mainly filamentous) composing a small fraction (Fig. 1, Table ESM4). D. argenteus (F = 4.25, P < 0.001) exhibited the most variable diet among the study species, with no obvious dominant component. While arthropods, echinoderms and molluscs were the most important items of animal origin, green corticated, red calcareous, and corticated composed the bulk of algal categories (Fig. 1, Table ESM5).
The PCA with data from diet composition highlighted differences and similarities among the nutritional strategies of the four study fish species (Fig. 2). The diet of Kyphosus sectatrix was positively related to red and brown corticated algae with negative values along the first component axis. S. axillare and A. chirurgus overlapped in diet and had positive values along the first component axis being related to detritus, red and calcareous filamentous algae. Among the study species, D. argenteus has the most variable diet, with data scattered on both axis and spread positively along the second component axis. It was related to different animal material such as Arthropoda, Echinodermata and Mollusca (Fig. 2). Dietary overlap was the highest between A. chirurgus and S. axillare (Schoener index = 0.81). Kyphosus sectatrix presented the most dissimilar diet when comparing with S. axillare (0.30), A. chirurgus (0.23) and D. argenteus (0.28) (Table 3).
Carbon content differed significantly between all fish species (F = 53.05, P < 0.001), with the highest values in the diet for S. axillare followed by K. sectatrix, while D. argenteus exhibited the greatest variation and A. chirurgus the lowest (Fig. 3a, Table ESM6). S. axillare exhibited the highest %N, followed by both D. argenteus and K. sectatrix (F = 55.28, P < 0.001), with A. chirurgus displaying the most nitrogen-poor diet (Fig. 3b, Table ESM6). C:N ratio was highest in A. chirurgus and lowest in S. axillare (F = 15.44, P < 0.001), with both K. sectatrix and D. argenteus exhibiting intermediate and similar ratios (Fig. 3c, Table ESM6).
The calculations of proportional nitrogen intake from each dietary food category indicated that detritus was the main source of dietary nitrogen in both A. chirurgus and S. axillare, contributing 36% and 37.8% of total nitrogen intake, respectively (Table 4). Large filamentous cyanobacteria were also a significant contributor to total nitrogen intake in S. axillare at 11.1%. The contribution of animal material to total dietary nitrogen intake was highest in D. argenteus (76.5%), intermediate in S. axillare (16.6%) and A. chirurgus (13.2%) and lowest in K. sectatrix (0.2%) (Table 4). The main components of this animal material differed between the fish species: arthropods, molluscs and echinoderms in D. argenteus, arthropods in S. axillare, bryozoans and arthropods in A. chirurgus and bryozoans in K. sectatrix (Table 4). Brown and red corticated algae were the main source of nitrogen for K. sectatrix, and although having a very varied diet, D. argenteus acquired most of its total nitrogen intake (76.5%) from invertebrates (Table 4).
Discussion
In this study, we present data on gut content analyses and dietary nutrient concentration of four nominally herbivorous fish species from the Southwestern Atlantic. The four fish species analysed had distinct diets in relation to the percentage contribution of the different food categories, with the greatest overlap between A. chirurgus and S. axillare. While K. sectatrix had a diet dominated by corticated algae with intermediate levels of carbon and nitrogen, and D. argenteus the most variable diet and nutrient concentration, the diets of both A. chirurgus and S. axillare included high proportions of detritus in addition to red algae. Despite the apparent similarity in the diets of A. chirurgus and S. axillare, they had very distinct nutritional dietary profiles with the former containing roughly four times the nitrogen and double the carbon content of the latter.
High nitrogen concentration is usually associated with protein-rich food items, especially from animal origin. Organic detritus associated with algal turfs in reef systems can also have high levels of nitrogen and protein (Crossman et al. 2001; Wilson et al. 2003; Clements and Choat 2018), but this fact alone would not explain the discrepancy between S. axillare and A. chirurgus diets in C:N ratio since the dietary contribution of detritus was similar in both species. Endogenous mucus produced from the pharynx, which is considerable in parrotfishes, can also elevate nitrogen content of material in the anterior gut (Holley et al. 2015), but not sufficiently to explain the magnitude of differences seen here. Rather, our data indicate that detritus as identified by gut content analysis in this study does not represent a homogeneous category. The high taxonomic and nutritional heterogeneity of detritus in algal turfs (Crossman et al. 2001; Wilson et al. 2003; Crossman et al. 2005), combined with the mechanical processing of ingested material by the pharyngeal mill in parrotfishes (Choat et al. 2002; Carr et al. 2006), clearly complicate accurate assessment of diet by traditional gut content analysis in some of these fishes.
Despite the similarities in the proportions of food categories in gut contents, the differences between S. axillare and A. chirurgus in dietary nutritional profiles suggest that these two species have distinct feeding strategies that result in profound differences in the nutritional composition of their diets. Although both S. axillare and A. chirurgus actively select algal turf substrata when feeding (Bonaldo et al. 2006; Francini-Filho et al. 2010), our results suggest that they feed selectively on different components of this resource. Sparisoma axillare obviously selects material with a higher proportion of protein (e.g. large filamentous cyanobacteria), whereas A. chirurgus ingests material with higher carbon content. This supports the view that parrotfishes do not actively select macroalgae as their primary food source (Clements et al. 2017; Clements and Choat 2018). This view is reinforced by the fact that another Brazilian parrotfish, Scarus trispinosus, apparently has little or no capacity to digest macroalgae, since a large number of algae species survived the entire digestive process and were viable in culture from fish faeces (Tâmega et al. 2016). Indeed, recent advances in parrotfish nutritional ecology suggest that these fishes are best described as microphages targeting protein-rich cyanobacteria and other endolithic and epilithic autotrophic microorganisms (Clements et al. 2017; Clements and Choat 2018). The high nitrogen concentration and C:N ratios found on the diet of S. axillare at least partly reflect the presence of these microorganisms in the detrital component of their diets. Although microscopic endolithic and epilithic cyanobacteria were not assessed in our gut content analyses, large filamentous cyanobacteria were a frequent food item in S. axillare (being registered in eight out of ten individual analysed), but were identified in the guts of only two (out of 18) A. chirurgus. This reinforces the idea that S. axillare targets protein-rich autotrophs as their main food. The detritus in A. chirurgus appears to be of a different origin. The dominant monounsaturated fatty acid in A. chirurgus is 16:1n-7 palmitoleic acid (Phleger and Laub 1989), which is a biomarker for diatoms (Kelly and Scheibling 2012). This indicates that the detritus in A. chirurgus is rich in diatoms and likely also in dead algal material colonised by heterotrophic bacteria.
The differences observed in dietary nutritional composition of S. axillare and A. chirurgus reflect distinct levels of selectivity by these fishes within the same habitat and highlight the low redundancy in their feeding ecology. Such a pattern of selectivity would be similar to that seen between grazing ruminants and equids (Duncan et al. 1990, Edwards 1991) and between wallabies and kangaroos (Freudenberger et al. 1989, Hume 1999). In the former example the higher intake requirements of equids forces them to be less selective of forage quality than grazing ruminants, which are more efficient at digesting forage of intermediate quality than equids, and thus require lower daily food intake rates. In the latter example, kangaroos are able to subsist on a diet with higher fibre content than wallabies by having lower intake rates which enable lengthy retention times, thus facilitating efficient digestion of forage through fermentation by microoganisms in the tubiform forestomach. Alimentary morphology in A. chirurgus and S. axillare resembles that of related “detritivorous” acanthurid and scarine taxa, which appear to be largely reliant on endogenous digestive mechanisms (Choat et al. 2004, Crossman et al. 2005). In terms of their feeding behaviour, A. chirurgus has a feeding rate consistently higher than S. axillare (Francini-Filho et al. 2010), a pattern that resembles the aforementioned mammal examples. Similarly, in the same study region, Ferreira et al. (1998b) found that Acanthurus bahianus has a feeding rate up to five times higher and ingestion by weight higher than Sparisoma tuiupiranga, reinforcing the discrepancies between surgeonfishes and parrotfishes. A. chirurgus would thus require higher intake rates than S. axillare to fulfil its nutritional requirements, especially in terms of protein intake.
The higher %C in the diet of S. axillare compared to A. chirurgus is likely to include inorganic carbon from articulated calcareous algae such as Jania spp. and Amphiroa spp. These algae are the most important components in the turf communities in the sampling region and are ingested by a number of grazing species (Ferreira et al. 1998a; Mendes et al. 2009). Although articulated calcareous algae comprised similar proportions of the diet in both S. axillare and A. chirurgus, the dietary proportion of these algae are more likely to be underestimated by visual examination in S. axillare due to the action of the pharyngeal mill. The inclusion of inorganic carbon from calcareous algae in S. axillare is likely to mean that the differences we note between this species and A. chirurgus in both C:N ratio and %N intake are actually underestimates in terms of nutrient intake.
The diet of K. sectatrix was largely dominated by brown and red corticated algae. Most Kyphosus species worldwide eat brown algae (Clements and Choat 1997; Ferreira and Gonçalves 2006), which possess highly refractory carbohydrates (Littler et al. 1983; White et al. 2010). Herbivorous Kyphosus species arguably display the most effective mechanisms for algal processing and digestion seen among marine herbivorous fishes, relying on both endogenous and exogenous strategies for nutrient acquisition (Mountfort et al. 2002, Crossman et al. 2005). The large, acidic stomach lyses macroalgal cell walls, allowing digestive enzymes access to cell contents (Zemke-White et al. 2000), while the hindgut microbiota converts refractory carbohydrates into short-chain fatty acids that are assimilated by the fish for energy and lipid synthesis (Mountfort et al. 2002; Fidopiastis et al. 2006). These strategies allow K. sectatrix to extract energy from corticated algae that most other fish species cannot process effectively. The nature of their food and the lack of significant mechanical digestion mean that conventional gut content analysis is a reliable indicator of diet in Kyphosus spp.
The omnivorous D. argenteus ingested a great variety of food items, with some individuals ingesting almost exclusively algae while others ingested mainly animal material as previously described for this species in the Southwestern Atlantic (Dubiaski-Silva and Masunari 2006). Most species from the family Sparidae are considered omnivores and display considerable trophic plasticity (e.g. Dubiaski-Silva and Masunari 2006; Soares et al. 2012; Sheaves et al. 2014). The genus Diplodus is characterised by a relatively small acidic stomach followed by a long intestine and produce a range of digestive enzymes enabling the utilisation of both animal and plant matter (Tramati et al. 2005). Although little information is available about the drivers of selectivity on highly omnivorous fishes, other sparid species show differences in amylase activity which are related to their diets, suggesting a high physiological plasticity (Fernández et al. 2001). Whether this plasticity is solely related to opportunity or is triggered by sex or developmental stage is yet to be determined.
It is important to note that all the sampling for this work was carried out in summer, and thus our results do not incorporate seasonal variation. Seasonal dietary variation in the study fish species is likely to occur in the study area due to seasonal variation in food availability (Ferreira et al. 1998b). For example, throughout the entire study area brown algae (mainly Sargassum and Dictyota) are much more abundant during spring and summer than autumn and winter, when Sargassum retains only its holdfast and almost disappears (Guimaraes and Coutinho 1996; Villaça et al. 2008). Thus, in winter K. sectatrix in particular would need to either spend more time foraging or explore different food sources. Similarly, nothing is known about the seasonal dynamics of algal turf communities and its components, or how its composition and nutritional properties vary over time. It is possible that D. argenteus modulates the intake between animal and plant material seasonally depending on availability, reproductive period or nutritional composition of their food.
In summary, the four herbivorous fish species studied displayed diets that were broadly consistent with previously used dietary categories: macroalgae (K. sectatrix), omnivory (D. argenteus) and detritivory (S. axillare and A. chirurgus) (Longo et al. 2014; Cordeiro et al. 2016). However, the dietary nutritional analysis presented here clearly shows that the latter two species have distinct diets, and thus their trophic ecology requires reassessment. It is likely that they represent distinct functional groups, with S. axillare acting as microphage targeting protein-rich autotrophic microorganisms (such as cyanobacteria) and A. chirurgus ingesting larger quantities of dead algal material colonised by bacteria and diatoms. In this sense, the present study reinforces the view that conventional gut content analysis is not sufficient to identify the diet of some herbivorous species. More detailed information on the nutritional composition of foods and how different nutrients are utilised by herbivorous species is still required to understand the nutritional ecology of this important group of fishes on reefs worldwide. These four species represent only a fraction of the relatively species-poor fauna of reef fishes that occur in Brazil. Little is known about how herbivorous fishes in the Atlantic process ingested foods, since by far most of the work on nutritional ecology of herbivorous fishes has been performed in the Pacific (Choat et al. 2002, 2004; Crossman et al. 2005). The high diversity of endemic herbivorous genera restricted to the Atlantic (like Sparisoma) provides great potential for comparative study of food processing modes and the description of novel nutritional strategies within this assemblage.
Change history
27 November 2018
The authors would like to correct the error in the publication of the original article. The corrected details are given below for your reading.
References
Adam TC, Burkepile DE, Ruttenberg BI, Paddack MJ (2015) Herbivory and the resilience of Caribbean coral reefs: knowledge gaps and implications for management. Mar Ecol Prog Ser 520:1–20. https://doi.org/10.3354/meps11170
Angell AR, Mata L, de Nys R, Paul NA (2015) The protein content of seaweeds: a universal nitrogen-to-protein conversion factor of five. J Appl Phycol 28:511–524. https://doi.org/10.1007/s10811-015-0650-1
Barbarino E, Lourenço SO (2009) Comparison of CHN analysis and Hach acid digestion to quantify total nitrogen in marine organisms. Limnol Oceanogr Methods 7:751–760. https://doi.org/10.4319/lom.2009.7.751
Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833. https://doi.org/10.1038/nature02691
Bierwagen SL, Heupel MR, Chin A, Simpfendorfer CA (2018) Trophodynamics as a tool for understanding coral reef ecosystems. Front Mar Sci 5:24. https://doi.org/10.3389/fmars.2018.00024
Bjorndal KA (1997) Fermentation in reptiles and amphibians. In: Mackie RI, White BA (eds) Gastrointestinal microbiology, vol 1. Gastrointestinal ecosystems and fermentations. Chapman & Hall, New York, pp 199–230
Bonaldo RM, Krajewski JP, Sazima C, Sazima I (2006) Foraging activity and resource use by three parrotfish species at Fernando de Noronha Archipelago, tropical West Atlantic. Mar Biol 149:423–433. https://doi.org/10.1007/s00227-005-0233-9
Bonaldo RM, Hoey AS, Bellwood DR (2014) The ecosystem roles of parrotfishes on tropical reefs. Oceanogr Mar Biol Annu Rev 52:81–132
Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139. https://doi.org/10.1890/0012-9658(2006)87%5b3128:HVNCOM%5d2.0.CO;2
Burkholder PD, Burkholder LM, Almodovar LR (1971) Nutritive constituents of some Caribbean marine algae. Bot Mar 14:132–135. https://doi.org/10.1515/botm.1971.14.2.132
Carpenter RC (1986) Partitioning herbivory and its effects on coral reef algal communities. Ecol Monogr 56:345–364
Carr A, Tibbetts IR, Kemp A, Truss R, Drennan J (2006) Inferring parrotfish (Teleostei: Scaridae) pharyngeal mill function from dental morphology, wear, and microstructure. J Morph 267:1147–1156. https://doi.org/10.1002/jmor.10457
Choat JH, Clements KD (1998) Vertebrate herbivory in marine and terrestrial environments: a nutritional ecology perspective. Annu Rev Ecol Syst 29:375–403. https://doi.org/10.1146/annurev.ecolsys.29.1.375
Choat JH, Clements KD, Robbins WD (2002) The trophic status of herbivorous fishes on coral reefs 1: dietary analyses. Mar Biol 140:613–623. https://doi.org/10.1007/s00227-001-0715-3
Choat JH, Robbins WD, Clements KD (2004) The trophic status of herbivorous fishes on coral reefs. II. Food processing modes and trophodynamics. Mar Biol 145:445–454. https://doi.org/10.1007/s00227-004-1341-7
Clements KD, Choat JH (1997) Comparison of herbivory in the closely-related marine fish genera Girella and Kyphosus. Mar Biol 127:579–586. https://doi.org/10.1007/s002270050048
Clements KD, Choat JH (2018) Nutritional ecology of parrotfishes (Scarinae, Labridae). In: Hoey AS, Bonaldo RM (eds) The biology and ecology of parrotfishes. CRC, Boca Raton, pp 42–68
Clements KD, Raubenheimer D, Choat JH (2009) Nutritional ecology of marine herbivorous fishes: ten years on. Funct Ecol 23:79–92. https://doi.org/10.1111/j.1365-2435.2008.01524.x
Clements KD, German DP, Piché J, Tribollet A, Choat JH (2017) Integrating ecological roles and trophic diversification on coral reefs: multiple lines of evidence identify parrotfishes as microphages. Biol J Linnean Soc 120:729–751. https://doi.org/10.1111/bij.12914
Cordeiro CAMM, Mendes TC, Harborne AR, Ferreira CEL (2016) Spatial distribution of nominally herbivorous fishes across environmental gradients on Brazilian rocky reefs. J Fish Biol 89:939–958. https://doi.org/10.1111/jfb.12849
Crossman DJ, Choat JH, Clements KD et al (2001) Detritus as food for grazing fishes on coral reefs. Limnol Oceanogr 46:1596–1605. https://doi.org/10.4319/lo.2001.46.7.1596
Crossman DJ, Choat JH, Clements KD (2005) Nutritional ecology of nominally herbivorous fishes on coral reefs. Mar Ecol Prog Ser 296:129–142. https://doi.org/10.3354/meps296129
Diniz GS, Barbarino E, Lourenço SO (2012) On the chemical profile of marine organisms from coastal subtropical environments: gross composition and nitrogen-to-protein conversion factors. In: Marcelli M (ed) Oceanography. InTech, Zagreb, pp 297–320
Diniz GS, Barbarino E, Oiano-Neto J et al (2014) Proximate composition of marine invertebrates from tropical coastal waters, with emphasis on the relationship between nitrogen and protein contents. Lat Am J Aquat Res 42:332–352. https://doi.org/10.3856/vol42-issue2-fulltext-5
Dromard CR, Bouchon-Navaro Y, Harmelin-Vivien M, Bouchon C (2015) Diversity of trophic niches among herbivorous fishes on a Caribbean reef (Guadeloupe, Lesser Antilles), evidenced by stable isotope and gut content analyses. J Sea Res 95:124–131. https://doi.org/10.1016/j.seares.2014.07.014
Dubiaski-Silva J, Masunari S (2006) Ontogenetic and seasonal variation in the diet of Marimbá, Diplodus argenteus (Valenciennes, 1830) (Pisces, Sparidae) associated with the beds of Sargassum cymosum C. Agardh, 1820 (Phaeophyta) at Ponta das Garoupas, Bombinhas, Santa Catarina. J Coast Res SI 39:1190–1192
Duncan P, Foose TJ, Gordon IJ, Gakahu CG, Lloyd M (1990) Comparative nutrient extraction from forages by grazing bovids and equids: a test of the nutritional model of equid/bovid competition and coexistence. Oecologia 84:411–418
Edwards PB (1991) Seasonal variation in the dung of African grazing mammals, and its consequences for coprophagous insects. Func Ecol 5:617–628
Fernández I, Moyano FJ, Díaz M, Martínez T (2001) Characterization of & α-amylase activity in five species of Mediterranean sparid fishes (Sparidae, Teleostei). J Exp Mar Biol Ecol 262:1–12
Ferreira CEL, Gonçalves JEA (2006) Community structure and diet of roving herbivorous reef fishes in the Abrolhos Archipelago, south-western Atlantic. J Fish Biol 69:1533–1551. https://doi.org/10.1111/j.1095-8649.2006.01220.x
Ferreira CEL, Gonçalves JEA, Coutinho R, Peret AC (1998a) Herbivory by the dusky damselfish Stegastes fuscus (Cuvier, 1830) in a tropical rocky shore: effects on the benthic community. J Exp Mar Bio Ecol 229:241–264. https://doi.org/10.1016/S0022-0981(98)00056-2
Ferreira CEL, Peret AC, Coutinho R (1998b) Seasonal grazing rates and food processing by tropical herbivorous fishes. J Fish Biol 53:222–235. https://doi.org/10.1111/j.1095-8649.1998.tb01029.x
Ferreira CEL, Gonçalves JEA, Coutinho R (2001) Community structure of fishes and habitat complexity on a tropical rocky shore. Environ Biol Fishes 61:353–369. https://doi.org/10.1023/A:1011609617330
Ferreira CEL, Floeter SR, Gasparini JL et al (2004) Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison. J Biogeogr 31:1093–1106. https://doi.org/10.1111/j.1365-2699.2004.01044.x
Fidopiastis PM, Bezdek DJ, Horn MH, Kandel JS (2006) Characterizing the resident, fermentative microbial consortium in the hindgut of the temperate-zone herbivorous fish, Hermosilla azurea (Teleostei: Kyphosidae). Mar Biol 148:631–642. https://doi.org/10.1007/s00227-005-0106-2
Floeter SR, Behrens MD, Ferreira CEL et al (2005) Geographical gradients of marine herbivorous fishes: patterns and processes. Mar Biol 147:1435–1447. https://doi.org/10.1007/s00227-005-0027-0
Francini-Filho RB, Ferreira CM, Coni EOC, Moura RL, Kaufman L (2010) Foraging activity of roving herbivorous reef fish (Acanthuridae and Scaridae) in eastern Brazil: influence of resource availability and interference competition. J Mar Biol Assoc UK 90:481–492. https://doi.org/10.1017/S0025315409991147
Freudenberger DO, Walli IR, Hume ID (1989) Digestive adaptations of kangaroos, wallabies and rat-kangaroos. In: Grigg G, Jarman P, Hume ID (eds) Kangaroos, wallabies and rat-kangaroos. Surrey Beatty & Sons Pty Ltd, New South Wales, pp 179–187
Green AL, Bellwood DR (2009) Monitoring functional groups of herbivorous fishes as indicators for coral reef resilience. In: IUCN working group on climate change and coral reefs
Guimaraes MA, Coutinho R (1996) Spatial and temporal variation of benthic marine algae at the Cabo Frio upwelling region, Rio de Janeiro, Brazil. Aquat Bot 52:283–299. https://doi.org/10.1016/0304-3770(95)00511-0
Holley LL, Heidman MK, Chambers RM, Sanderson SL (2015) Mucous contribution to gut nutrient content in American gizzard shad Dorosoma cepedianum. J Fish Biol 86:1457–1470. https://doi.org/10.1111/jfb.12656
Horn MH (1989) Biology of marine herbivorous fishes. Oceanogr Mar Biol 27:167–272
Hume ID (1999) Marsupial nutrition. Cambridge University Press, Cambridge, p 450
Hundt PJ, Simons AM (2018) Extreme dentition does not prevent diet and tooth diversification within combtooth blennies (ovalentaria: Blenniidae). Evolution. https://doi.org/10.1011/evo.13453
Kelly JR, Scheibling RE (2012) Fatty acids as dietary tracers in benthic food webs. Mar Ecol Prog Ser 466:1–22. https://doi.org/10.3354/meps09559
Kulbicki M, Parravicini V, Bellwood DR et al (2013) Global biogeography of reef fishes: a hierarchical quantitative delineation of regions. PLoS One 8:e81847. https://doi.org/10.1371/journal.pone.0081847
Lartigue J, Cebrian J (2012) Ecosystem productivity and carbon flows: patterns across ecosystems. In: Levin SA, Carpenter SR, Godfray HCJ (eds) The Princeton guide to ecology. Princeton University Press, Princeton, pp 320–329
Levey DJ, Martínez del Rio C (2001) It takes guts (and more) to eat fruit: lessons from avian nutritional ecology. Auk 118:819–831. https://doi.org/10.2307/4089834
Littler MM, Taylor PR, Littler DS (1983) Algal resistance to herbivory on a Caribbean barrier reef. Coral Reefs 2:111–118
Lobato FL, Barneche DR, Siqueira AC et al (2014) Diet and diversification in the evolution of coral reef fishes. PLoS One 9:e102094. https://doi.org/10.1371/journal.pone.0102094
Longo GO, Ferreira CEL, Floeter SR (2014) Herbivory drives large-scale spatial variation in reef fish trophic interaction. Ecol Evol 4:4553–4566. https://doi.org/10.1002/ece3.1310
McDermid KJ, Stuercke B, Balazs GH (2007) Nutritional composition of marine plants in the diet of the green sea turtle (Chelonia mydas) in the Hawaiian Islands. Bull Mar Sci 81:55–71
McMahon KW, Thorrold SR, Houghton LA, Berumen LM (2016) Tracing carbon flow through coral reef food webs using a compound-specific stable isotope approach. Oecol 180:809–821
Mendes TC, Villaça RC, Ferreira CEL (2009) Diet and trophic plasticity of an herbivorous blenny Scartella cristata of subtropical rocky shores. J Fish Biol 75:1816–1830. https://doi.org/10.1111/j.1095-8649.2009.02434.x
Mendes TC, Cordeiro CAMM, Ferreira CEL (2015) An experimental evaluation of macroalgal consumption and selectivity by nominally herbivorous fishes on subtropical rocky reefs. J Exp Mar Biol Ecol 471:146–152. https://doi.org/10.1016/j.jembe.2015.06.001
Montgomery WL, Gerking SD (1980) Marine macroalgae as food for fishes: an evaluation of potential food quality. Environ Biol Fish 5:143–153
Mountfort DO, Campbell J, Clements KD (2002) Hindgut fermentation in three species of marine herbivorous fish. Appl Environ Microbiol 68:1374–1380. https://doi.org/10.1128/AEM.68.3.1374-1380.2002
Munda IK, Gubenšek F (1976) The amino acid composition of some common marine algae from Iceland. Bot Mar 19:85–92
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens HH, Szoecs E, Wagner H (2017) vegan: community ecology package. R package version 2.4-5. https://CRAN.R-project.org/package=vegan
Paine R (1996) Food web complexity and community dynamics. Am Nat 100:65–75
Phleger CF, Laub RJ (1989) Skeletal fatty acids in fish from different depths off Jamaica. Comp Biochem Physiol B Biochem Mol Biol 94:329–334
Piché J, Iverson SJ, Parrish FA, Dollar R (2010) Characterization of forage fish and invertebrates in the Northwestern Hawaiian Islands using fatty acids signatures: species and ecological groups. Mar Ecol Prog Ser 418:1–15
Randall JE (1967) Food habits of reef fishes of the West Indies. Stud Trop Oceanogr 5:665–847
Raubenheimer D, Simpson SJ, Mayntz D (2009) Nutrition, ecology and nutritional ecology: toward an intergrated framework. Funct Ecol 23:4–16. https://doi.org/10.1111/j.1365-2435.2008.01522.x
Rogers R, Correal G, Oliveira TC et al (2014) Coral health rapid assessment in marginal reef sites. Mar Biol Res 10:612–624. https://doi.org/10.1080/17451000.2013.841944
Rooney N, McCann K, Gellner G, Moore JC (2006) Structural asymmetry and the stability of diverse food webs. Nature 442:265–269. https://doi.org/10.1038/nature04887
Sheaves M, Sheaves J, Stegemann K, Molony B (2014) Resources partitioning and habitat-specific dietary plasticity of two estuarine sparid fishes increases food-web complexity. Mar Freshw Res 65:114–123
Smith JE, Smith CM, Hunter CL (2001) An experimental analysis of the effects of herbivory and nutrient enrichment on benthic community dynamics on a Hawaiian reef. Coral Reefs 19:332–342. https://doi.org/10.1007/s003380000124
Soares F, Freitas R, Soares J, Leitão F, Cristo M (2012) Feeding ecology and morphometric relationships of white seabream, Diplodus sargus lineatus (Sparidae), endemic species of Cape Verde. Cybium 36:461–472
Steneck RS, Dethier MN (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498. https://doi.org/10.2307/3545860
Tâmega FTS, Figueiredo MAO, Ferreira CEL, Bonaldo RM (2016) Seaweed survival after consumption by the greenbeak parrotfish Scarus trispinosus. Coral Reefs 35:329–334
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Tramati C, Savona B, Mazzola A (2005) A study of the pattern of digestive enzymes in Diplodus puntazzo (Cetti, 1777) (Osteichthyes, Sparidae): evidence for the definition of nutritional protocols. Aquacult Int 13:89–95
Valentin JL (1984) Analyse des paramètres hydrobiologiques dans la remontée de Cabo Frio (Brésil). Mar Biol 82:259–276. https://doi.org/10.1007/BF00392407
Van Soest P (1994) Nutritional ecology of the ruminants, 2nd edn. Cornell Press, Ithaca
Villaça R, Yoneshigue-Valentin Y, Boudouresque CF (2008) Estrutura da comunidade de macroalgas do infralitoral do lado exposto da ilha de Cabo Frio (Arraial Do Cabo, RJ). Oecol Bras 12:206–221
Wallace RK (1981) An assessment of diet-overlap indexes. Trans Am Fish Soc 110:72–76
Weber JM, Haman G (1996) Pathways for metabolic fuels and oxygen in high performance fish. Com Biochem Physiol 113:33–38
Wheeler B, Torchiano M (2016) lmPerm: permutation tests for linear models. R package version 2.1.0. https://CRAN.R-project.org/package=lmPerm
White WL, Coveny AH, Robertson J, Clements KD (2010) Utilisation of mannitol by temperate marine herbivorous fishes. J Exp Mar Biol Ecol 391:50–56. https://doi.org/10.1016/j.jembe.2010.06.007
Wilson SK, Bellwood DR, Choat JH, Furnas MJ (2003) Detritus in the epilithic algal matrix and its use by coral reef fishes. Oceanogr Mar Biol Annu Rev 41:279–309
Yamamuro M (1999) Importance of epiphytic cyanobacteria as food sources for heterotrophs in a tropical seagrass bed. Coral Reefs 18:263–271. https://doi.org/10.1007/s003380050191
Zemke-White WL, Clements KD, Harris PJ (2000) Acid lysis of macroalgae by marine herbivorous fishes: effects of acid pH on cell wall porosity. J Exp Mar Biol Ecol 245:57–68. https://doi.org/10.1016/S0022-0981(99)00151-3
Zemke-White WL, Choat JH, Clements KD (2002) A re-evaluation of the diel feeding hypothesis for marine herbivorous fishes. Mar Biol 141:571–579. https://doi.org/10.1007/s00227-002-0849-y
Zhang J (2016) spaa: SPecies Association Analysis. R package version 0.2.2. https://CRAN.R-project.org/package=spaa
Acknowledgements
We thank Cesar Cordeiro who helped collecting the fishes; and Howard Choat, Roberta Bonaldo and Cesar Cordeiro for helpful discussions. We also thank three anonymous reviewers and the handling editor for valuable comments on this paper.
Funding
Financial support was given by FAPERJ (through a visiting professor grant to KDC—APV#E-26/111.654/2012), CNPq (with a Sanduíche Scholarship to TCM—# 246840/2012-9), Fundação O Boticário de Proteção à Natureza (Grant #0898/20111) and ECOHUB that provides continuous support to LECAR activities.
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Mendes, T.C., Ferreira, C.E.L. & Clements, K.D. Discordance between diet analysis and dietary macronutrient content in four nominally herbivorous fishes from the Southwestern Atlantic. Mar Biol 165, 180 (2018). https://doi.org/10.1007/s00227-018-3438-4
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DOI: https://doi.org/10.1007/s00227-018-3438-4