Trophic ecology and resource partitioning of Haemulidae species along the Northeastern Brazilian continental shelf

Abstract

In the Southeastern Tropical Atlantic, Haemulidae family play an important role both environmentally, acting as a link between lower and higher trophic levels, and socioeconomically, being widely caught by artisanal fleets. This study aimed to describe the trophic ecology of three grunt species (Haemulon aurolineatum, H. plumierii and H. squamipinna) considering spatial, temporal and ontogenetic aspects, integrating stomach content and stable isotopes analysis. Sampling occurred in 26 stations along the Northeast of Brazil (04°– 09°S), in August 2015 and April 2017, using bottom trawling net. There was greater feeding intensity at night, at latitudes below 08°S and in the inner continental shelf. Higher values of δ¹⁵N were reported for H. aurolineatum and H. plumierii collected near coastline. The isotopic niche breadth indicated that H. aurolineatum has a narrower diet thanH. plumierii. For the three species, the trophic level ranged between three and four. Considering stomach content and isotopic niche, diet was similar comparing species. This trophic ecology pattern reveals a likewise use of the habitat, which may be essential for identifying priority areas for conservation on an ecosystem basis, especially in rich reef zones that are subject to several increasing pressures, such as those in Northeast Brazil.

Keywords:
Feeding; Grunts; Stable isotopes; Stomach contents; Trophic ecology

Resumo

No Atlântico Tropical Sudeste, peixes da família Haemulidae desempenham um papel importante tanto ambientalmente, atuando como um elo entre os níveis tróficos mais baixos e mais altos, quanto socioeconomicamente, sendo amplamente capturados pelas frotas artesanais. Este estudo teve como objetivo descrever a ecologia trófica de três espécies de roncadores (Haemulon aurolineatum, H. plumierii e H. squamipinna) considerando aspectos espaciais, temporais e ontogenéticos integrando conteúdo estomacal e análise de isótopos estáveis. A amostragem ocorreu em 26 estações ao longo do Nordeste do Brasil (04°– 09°S), em agosto de 2015 e abril de 2017, utilizando rede de arrasto de fundo. Houve maior intensidade de alimentação à noite, em latitudes abaixo de 08°S e na plataforma continental interna. Valores mais altos de δ¹⁵N foram reportados para H. aurolineatum e H. plumierii coletados perto da linha costeira. A amplitude do nicho isotópico indicou que o H. aurolineatum tem uma dieta mais estreita do que o H. plumierii. Para as três espécies, o nível trófico variou entre três e quatro. Considerando o conteúdo estomacal e o nicho isotópico, a dieta foi semelhante comparando as espécies. Este padrão de ecologia trófica mostra um uso semelhante do habitat, que pode ser essencial para identificar áreas prioritárias para conservação em uma base ecossistêmica, especialmente em zonas ricas de recifes que estão sob várias pressões crescentes, como as do Nordeste do Brasil.

Palavras-chave:
Alimentação; Conteúdo estomacal; Ecologia trófica; Isótopos estáveis; Roncadores

INTRODUCTION

Fishes of the Haemulidae family are extremely important for the food web balance, mainly for reef communities, and comprise the main prey of many larger fishes with great commercial value such as Lutjanidae and Carangidae (Palazón-Fernández, 2007; Frédou et al., 2009; Pereira et al., 2011; Rindone et al., 2015). The genus Haemulon is considered very abundant and rich, has great representativeness within tropical fish, encompassing 19 species from the eastern Pacific to the western Atlantic (Rocha et al., 2008).

In the Atlantic Ocean, Haemulon are restricted to the tropical regions of Brazil, from northeastern to southeastern coast (Rocha et al., 2008), inhabiting mostly coral reefs and rocky bottoms (Ilarri et al., 2008). With demersal behavior, they feed mainly of preys associated to the seabed such as the macrobenthic fauna, but is also reported on the water column, carrying on small daily migrations from the reef to sandbanks near seagrass meadows (Parrish, 1989; Rocha et al., 2008; Pereira, Ferreira, 2013; Pereira et al., 2015). There are nine species of Haemulon reported for the Brazilian coast (Rocha, Rosa, 1999; Tavera et al., 2012; Cerqueira et al., 2021) highlighting Haemulon aurolineatum Cuvier, 1830, H. plumierii (Lacepède, 1801), and H. squamipinna Rocha & Rosa, 1999, giving their high abundance and wide spatial distribution (Rocha et al., 2008; Pereira et al., 2015).

In the Northeastern Brazil, Haemulidae (grunts) are part of the bycatch of the lobster (Panulirus argus and P. laevicauda) and goatfish (Pseudupeneus maculatus) fisheries but, giving the decrease in abundance of these target species, nowadays, they are targeted in the region (Nóbrega, Lessa, 2007; Marques, Ferreira, 2010), being also relevant for the aquarium business (Rocha et al., 1998; Lessa, Nóbrega, 2000; Shinozaki-Mendes et al., 2013). Moreover, due to their wide distribution and great abundance, H. aurolineatum, H. plumierii, and H. squamipinna have a critical role to trophic dynamic of marine ecosystems in the Brazilian coastline (Rocha et al., 2008).

Studies on the trophic dynamic are essential for wildlife conservation (Gheler-Costa et al., 2018), encompassing many facets such as niche overlap and intraspecific interactions, whether in temporal or spatial realms (Esteves, Aranha, 1999), providing a better understanding of ecosystem functioning (Vieira, 2019). The traditional method to evaluate the fish diet composition is by stomach content analysis which provides an initial “snapshot” of the ecosystem trophic functions, observing each prey importance and identifying their relationship with the predator (Hahn et al., 2002). Stable isotopes composition provides diet information based on what is incorporated in the predator tissues to longer period (Fry, 2006). The stable isotopes of carbon (δ¹³C) and nitrogen (δ¹⁵N) have been widely used on studies of feeding habit of marine fishes (Gonzalez et al., 2019; Richards et al., 2019; Soares et al., 2020), providing information on energy sources (Peterson, Fry, 1987; Vander-Zanden et al., 2011) and trophic position (Bastos et al., 2017). Therefore, stable isotope analysis can provide complementary information to stomach content analyses, especially considering that nutrient assimilation varies according to prey ingested type, regardless of amount found in stomachs (Melville, Connolly, 2003).

The use of integrated techniques in trophic ecology for marine fish species is still scarce in Brazil (Freitas et al., 2011, 2017; Pimentel et al., 2018; Gonzalez et al., 2019). Although integrated approaches (stomach content and stable isotopes) for Haemulon species have been employed in Bahamas (Chittaro et al., 2004; Zhu et al., 2019), Panama Isthmus (Stuthmann, Castellanos-Galindo, 2020), Caribean Sea (Morinière et al., 2003; Nagelkerken et al., 2008) and Gulf of Mexico (Peterson et al., 2020), no such attempt has yet been made in Brazil, mainly considering a wide spatial scale and incorporating the influence of environmental factors (Pereira et al., 2015).

Therefore, even with a high social, economic, and environmental importance in Southwestern Tropical Atlantic (Pereira, Ferreira, 2013; Pereira et al., 2015; Eduardo et al., 2018; Cardoso de Melo et al., 2020), Haemulon species still does not have an extensive knowledge of many biological aspects (e.g., diet, growth, and reproduction patterns), their fishery is open access, and the management is absent. In addition, the integrated approaches of their biology and ecology are still unknown, or restricted in terms of spatial coverage. Thus, the present study aimed to describe the trophic ecology of H. aurolineatum, H. plumierii, and H. squamipinna, applying an integrative approach which combines stomach contents and carbon and nitrogen stable isotopes. We also tested the effect of the spatial (habitats, shelf position, latitudes), temporal (capture time), and biological (ontogenetic differences) factors into the feeding habits of Haemulidae in the South Atlantic. We expect that the information on the habitat use and trophic relationship between species associated to other studies, such as distribution patterns and fisheries (Eduardo et al., 2018; Cardoso de Melo et al., 2020), may be useful for future management and conservation actions, as for example, to identify priority areas for conservation (e.g., Marine Protection Areas, MPAs). This information may also be useful as input for ecosystem modelling (e.g., Ecopath).

MATERIAL AND METHODS

Study area and sampling procedures. Biological samples were collected during the project Acoustic Along Brazilian Coast (ABRACOS), composed of two scientific expeditions (Bertrand, 2017, 2015) carried out in August 2015 and April 2017, both on board the research ship R/V ANTEA. The study area (Fig. 1) comprised the Northeast Brazilian continental shelf, between the states of Rio Grande do Norte (RN) and Alagoas (AL) (04°– 09°S). Fishes were sampled at 26 stations, between 15 and 65 m deep. This region is considered of high diversity (Eduardo et al., 2018), encompassing several Marine Protected Area (e.g., “Costa dos Corais”, “Guadalupe”, “Santa Cruz”, “APA Barra de Mamanguape”) (Ferreira, Maida, 2007; Pereira et al., 2021). The region’s continental shelf average width is approximately 40 km, almost all covered by carbonate sediments with an average depth between 40 and 80 m (Vital et al., 2010). Fishing was carried out for five minutes in average using a bottom trawling net (mesh: 40 mm; cod mesh: 25 mm; mouth dimensions: 28 x 10 m), during night and day.

Diet was described considering the following factors: habitat type, latitude, distance from the coast, period of the day and ontogeny. Habitats were classified according to Eduardo et al., (2018): I – Sand; II – Algae; III – SWCR (substrate with rocks, coralline formations and sponges). Latitudes were divided into five strata according to Eduardo et al., (2018): A (all points above 5°S), B (05° to 06°S), C (06° to 07°S), D (07° to 08°S), and E (all points below 08°S). Given the average width of the continental shelf of 40 km, the distance from the coast was classified as inner (< 20 km) and outer (> 20 km) continental shelf. For the period of the day, samplings carried out from 9 AM to 6 PM were considered diurnal and from 6 PM to midnight as nocturnal. Adults and juveniles were classified according to the mean size at first maturity of each species (Cardoso de Melo et al., 2020).

On board, for the 26 stations (no replicates for each station), 30 individuals were randomly sub-sampled, labelled, and frozen. For all species, it was not possible to use the entirely collected individuals for simultaneous diet and stable isotope studies, given the poor preservation condition of some stomachs. In the laboratory, individuals were measured for standard length (SL, cm), weighted (g), and dissected for the stomach removal procedure. Removed stomachs were fixed in a formaldehyde solution (4%) and then transferred to 70% alcohol for further contents analysis. Each stomach content item was identified to the lowest possible taxonomic level, counted, and weighed.

FIGURE 1 |
Study area and sample points along the continental shelf of the northeast coast of Brazil. Red dots indicate samples for inner position (≤ 20 km) and black dots for outer (> 20 km).

Diet and feeding habits. Vacuity index (Vi) was estimated as the proportion of empty stomachs over the total sample size. Fulness index (Fi) was defined as a proxy of the feeding intensity indicator (Zavala-Camin, 1996). Differences on Fi were tested through the non-parametric test of Kruskal-Wallis, as the data did not follow the assumptions for a parametric test. Diet was described by three quantitative indices: frequency of occurrence (%FO), numerical frequency (%N), and relative weight (%W) (Hyslop, 1980; Bowen, 1996). Subsequently, two importance indices were calculated: Index of Relative Importance (Pinkas et al., 1971) and Alimentary Index (Kawakami, Vazzoler, 1980) adapted by Oliveira et al., (2004). The IRI uses frequency of occurrence, weight, and quantity of each item, while IAi is based on frequency of occurrence and volume of each item, which was replaced by the weight (Oliveira et al., 2004).

Feeding strategy was assessed through the modified Costello diagram (Amundsen et al., 1996), which is a representation of the degree of diet variability of a predator by plotting prey-specific abundance (Pi) vs the frequency of occurrence (%Fo) of each prey taxon. Niche breadth (Bi) was estimated using standardized Levins’ index (Hurlbert, 1978), which ranges from 0, when the species consumed only one type of food, to 1, when the species equally consumed all types of food items analyzed. Bi ≤ 0.3 are considered narrow; 0.6 ≥ Bi > 0.3 are moderate and Bi > 0.6 are considered a wide trophic niche breadth. For both, diet overlap and trophic niche breadth, percentual values were used. For diet overlap (Oi), the Pianka’s index (Pianka, 1973) was used. This index ranges from 0 to 1, where 0 means the niches do not overlap and 1 means the total niche overlap.

Stable Isotopes and trophic position. For stable isotope analysis (SIA), at least ten individuals of each species and the zooplankton were obtained for each sampling point. From these, samples of the dorsal muscular tissue of fish were collected, cleaned with distilled water to remove scales and remaining bones, and dried in an oven at 60° C for 48h. Subsequently, the tissue was ground to a powder with a tamper and pestle. Isotope analysis of zooplankton samples were made in duplicate: part of them was selected to remove carbonate (CaCO₃), by adding hydrochloric acid (HCl) and were used for the analysis of carbon isotopes (Fry, 1988); the rest of the samples (non-acidified) were used for nitrogen. Both subsamples were placed in an oven at 60°C for 24 hours and ground to a powder. Stable isotope analysis for carbon and nitrogen were run on a mass spectrometer (Thermo Delta V +) together with an element analyzer (Thermo Flash 2000, ConFio IV interface) on the Ocean Spectrometry Platform (IUEM, France). The isotopic ratios are expressed using the delta (δ) notation in parts per thousand (Peterson, Fry, 1987) and derived from the formula

$\delta X=\left[\left(\frac{Rsample}{Rs\tan dard}\right)-1\right]x{10}^3$

where δX corresponds to δ¹³C or δ¹⁵N and R to the ¹³C/¹²C or ¹⁵N/¹⁴N ratios of the sample and a known standard, for carbon or nitrogen, respectively. The standards used for δ¹³C and δ¹⁵N were the PeeDee Belemnite (PDB) limestone and atmospheric nitrogen, respectively. The analytical precision of the analysis was monitored through the analysis of an internal standard (Thermo – Acétanilide) every six samples, resulting in an accuracy of 0.10‰ and 0.07 ‰ for carbon and nitrogen isotopes, respectively.

Resource assimilated by consumers was first assessed by visualizing biplots (δ¹³C x δ¹⁵N) of consumer and zooplankton values. The mean δ¹³C and δ¹⁵N values were calculated considering spatial (habitats, shelf position, latitudes), temporal (capture time) and biological (ontogenetic differences) factors. Significant differences between these factors were tested, within and between species, using the Kruskal-Wallis tests. The trophic position of each species was estimated based on Post, (2002) methodology and considering a trophic discrimination factor (TDF) of 2.54‰ (Vanderklift, Ponsard, 2003).

Finally, the isotopic niche of the three species was assessed using the standard ellipses area (SEA). This method allows to quantify the space occupied by a species in a bi-dimensional plane (δ¹³C vs. δ¹⁵N) and is less sensitive to differences in sample size than other isotopic metrics (Jackson et al., 2011). However, both the position and width of a species isotopic niche is equally dependent to the isotopic composition of their prey and the organic matter sources sustaining the food web (Ben-David, Flaherty, 2012). Therefore, the isotopic niches of Haemulidae species were used to quantify the extent to which they may use available food sources. The overlap in their SEA’s area was considered to reflect the degree that they may rely on similar food resources. It was estimated through pairwise comparisons of the overlapping area between species and by using a Bayesian approach to assess the mean and 95% credible intervals (CI95) (Jackson et al., 2011). Zooplankton from the second size class was assumed the best primary consumer to be the baseline source due its trust of distribution and its homogeneity, composed mainly by copepods (Figueiredo et al., 2020). All analyses were performed by using the R program with the packages tRrophicPosition (Quezada-Romegialli et al., 2018) and SIBER (“Stable Isotope Bayesian Ellipses in R” (Jackson et al., 2011). In all analyses a significant level of 95% was considered.

RESULTS

A total of 229 individuals were analyzed for stomach content analysis (SCA), in which 143 of them were Haemulon aurolineatum (9.2–18.0 cm SL), 68 of H. plumierii (10.7–22.5 cm SL), and 20 H. squamipinna (12.6–14.5 cm SL). For stable isotope analysis (SIA), 257 individuals were analyzed: 112 H. aurolineatum, 85 H. plumierii, and 60 H. squamipinna. The description of the diet by the SCA was performed only for H. aurolineatum and for H. plumierii. Haemulon squamipinna did not present enough stomachs with food content to perform a reliable description of its diet. However, SIA were performed for the three species.

Diet composition and feeding habits. In general, a similar proportion of full and empty stomachs was found for H. plumierii (Vi=54.4%) and for H. aurolineatum (Vi=59.4%). However, the majority of the empty stomachs were collected at daytime for both species (H. plumierii=67.6%; H. aurolineatum=58.8%).

Feeding intensity (Fi) of H. aurolineatum is significantly higher at night (Kruskal-Wallis; chi-squared=7.1632; p=0.0074). Feeding intensity was also significantly different (Kruskal-Wallis; chi-squared=11.99; p=0.0074) among latitude strata, specifically between areas A and B (p=0.025), and A and E (p=0.017). Fi also significantly varied among shelf positions (Kruskal-Wallis; chi-squared=10.31; p=0.0013), with individuals collected close to the coast having higher Fi values than those from the shelf break areas. Juveniles also had significantly higher Fi than adults (Kruskal-Wallis; chi-squared=4.3077; p=0.0379). There was no significant difference of Fi between habitats. For H. plumierii the analysis by ontogeny could not be carried out, given the low number of juveniles, and no significant differences of Fi was recorded for any other factor considered (Fig. 2).

FIGURE 2 |
Feeding intensity indicator (Fi) of Haemulon aurolineatum and H. plumierii in different habitats, latitude gradient, shelf position, ontogeny and period of the day. The black horizontal line and box represent the median value and the interquartile range, while the vertical lines represent the upper and lower limits. Outliers were not included in the plot. Different symbols (* and **) represent significant difference.

The diet of the Haemulidae were mainly composed by crustaceans and polychaetas (Tab. 1). For H. aurolineatum, crustaceans, mainly decapods, carideans, and brachyurans, were generally the main source of food. The most frequent item was non-identified crustaceans (%FO=31), followed by polychaetas (%FO=20) and decapods (%FO=15). The same pattern was observed for numerical frequency (%N) and for relative weight (%W). Echinoderms were also one of the most consumed items, but with minor importance when compared to the aforementioned (Tab. 2).

TABLE 1 |
Contribution of each item of prey to the Haemulon aurolineatum and H. plumierii diets in the Southtern Atlantic considering the frequency of occurrence (%FO), number (%N), weight (%W) and respective relative importance (IRI) and food intensity (%IAI) (UI: unidentified).

Prey items		Haemulon aurolineatum					Haemulon plumierii
		%FO	%N	%W	%IRI	%IAI	%FO	%N	%W	%IRI	%IAI
Algae
		-	-	-	-	-	3.22	1.47	0.00	0.15	0.00
Cnidaria
	Hydrozoa	-	-	-	-	-	3.22	1.47	0.00	0.15	0.00
Echinodermata
	Echinoidea	10.34	9.78	5.89	4.89	3.65	25.80	11.76	16.39	22.67	24.73
	Holothuroidea	1.72	1.09	0.97	0.11	0.10	-	-	-	-	-
Polychaeta
	Amphinomidae	0.94	0.65	10.90	13.60	13.49	1.08	0.43	11.44	12.95	15.10
	Dorvilleidae	0.94	0.65	0.05	0.06	0.06	1.08	0.43	0.05	0.06	0.07
	Eunicidae	4.70	3.26	0.87	1.09	1.08	5.38	2.14	0.92	1.04	1.21
	Nereididae	2.82	1.96	1.66	2.07	2.05	3.23	1.29	1.74	1.97	2.30
	Onuphidae	1.88	1.30	0.29	0.37	0.36	1.08	0.43	0.17	0.19	0.22
	UI Polychaeta	9.40	8.48	2.50	3.13	3.10	10.75	5.58	2.63	2.98	3.47
Crustacea
	Anomura	1.72	1.09	0.96	0.11	0.10	6.45	4.41	4.12	1.71	1.55
	Amphipoda	5.17	3.26	2.95	0.97	0.91	6.45	8.82	1.13	2.00	0.42
	Brachyura	8.62	5.43	8.06	3.51	4.16	22.58	13.23	14.70	19.68	19.41
	Caridea	13.79	13.04	9.94	9.55	8.20	6.45	2.94	1.65	0.92	0.62
	Decapoda	15.52	11.96	12.71	11.54	11.80	9.68	5.88	3.01	2.68	1.70
	Isopoda	1.72	1.09	1.72	0.15	0.18	-	-	-	-	-
	Malacostraca	3.45	2.17	2.48	0.48	0.51	-	-	-	-	-
	Stomatopoda	6.90	4.35	5.42	2.03	2.23	3.22	1.47	1.82	0.33	0.34
	Thanaidacea	-	-	-	-	-	6.45	2.94	2.22	1.04	0.84
	UI Crustacea	31.03	21.74	24.35	43.11	45.19	16.12	17.65	9.10	13.46	8.58
Mollusca
	Cephalopoda	-	-	-	-	-	3.22	1.47	3.22	0.47	0.60
	Gastropoda	1.72	1.09	1.72	0.15	0.18	7.89	2.94	5.96	1.79	2.25
	UI Mollusca	8.62	6.52	4.81	2.94	2.48	6.45	5.88	3.55	1.90	1.34
Chordata
	Teleostei	1.72	1.09	1.72	0.15	0.18	16.12	7.35	16.12	11.81	15.20

TABLE 2 |
Ranking of importance of each category of prey item identified in the stomach content of Haemulon aurolineatum and H. plumierii according to each importance index (UI, unidentified).

Rank	Haemulon aurolineatum		Haemulon plumierii
	IRI	IAI	IRI	IAI
1	UI Crustacea	UI Crustacea	Echinoidea	Echinoidea
2	Polychaeta	Polychaeta	Brachyura	Polychaeta
3	Decapoda	Decapoda	Polychaeta	Brachyura
4	Caridea	Caridea	UI Crustacea	Teleostei
5	Echinoidea	Brachyura	Teleostei	UI Crustacea

Haumulon plumierii mainly based its diet on echinoderms, polychaetas, and crustaceans and teleost fishes (Tab. 1). The most frequent items were echinoderms (%FO=26), polychaetas and crustaceans, especially brachyurans. Teleost fishes were also one of the most frequent groups. In number, the most abundant item was non-identified crustaceans (%N=17), brachyurans (%N=13) and echinoids (%N=11). Polychaetas were the most numerically frequent food item (%N=17), followed by echinoderms and teleosts (both %N=16). Crustaceans also had high biomass, with non-identified crustaceans and brachyurans (Tab. 2).

The niche breadth of H. plumierii was very wide (Levin’s index: 63%). On the other hand, H. aurolineatum tends to feed on a smaller diversity of prey (50%). There was moderate dietary overlap between H. plumierii and H. aurolineatum (Oi > 84%).

According to the Costello diagram (Fig. 3), no specific food item was preferred by any Haemulidae species. Instead, for all species, items were generally placed in the left side of the plot, characterizing the fishes as mostly generalist predators. For H. aurolineatum specifically, even though most items had low frequency of occurrence, these items, when present, were very important in weight (Fig. 3).

FIGURE 3 |
Modified Costello diagram (Pi, prey specific abundance; Fo, frequency of occurence), a scatterplot containing all prey items, showing the feeding strategy of Haemulon aurolineatum and H. plumierii captured along the northeast coast of Brazil.

Stable isotopes. The isotopic ratios for H. plumierii were very wide for δ¹⁵N (7.40 to 13.44 ‰) but not for δ¹³C (-17.01 to -13.92 ‰). For H. aurolineatum ratios varied between -17.01 to -13.22 ‰ and 7.53 to 13.23 ‰ for δ¹³C and δ¹⁵N, respectively. Haemulon squamipinna had the narrowest ranges: -16.88 to -14.91 ‰ for δ¹³C and 7.76 to 11.24 ‰ for δ¹⁵N. For both H. plumierii and H. aurolineatum, there were no significant differences for these ratios among habitats (Tab. 3; Fig. 4). Haemulon squamipinna had significantly higher mean δ¹⁵N and δ¹³C ratio in sand than in SWCR. No individuals of H. squamipinna were reported on Algae. All species had higher mean δ¹⁵N ratio in the inner platform (Tab. 3; Fig. 4).

TABLE 3 |
Statistic differences in δ¹⁵N and δ¹³C values by habitat type, shelf position, latitude strata and ontogeny for Haemulon aurolineatum, H. plumierii, and H. squamipinna caught in Northeast Brazilian continental shelf. All caught specimens of H. squamipinna were considered adults, not allowing ontogenetic analysis. Significant values are identified by *.

	H. aurolineatum	H. plumierii	H. squamipinna
Habitat type	δ15N chi-squared=0.4423; p=0.8016 δ13Cchi-squared=5.8939; p=0.0525	δ15N chi-squared=6.3978; p=0.0938 δ13C chi-squared=5.8939; p=0.0773	δ15N chi-squared=13.079; p=0.0057* δ13C chi-squared=22.923; p=0.0006*
Shelf position	δ15N chi-squared=29.035; p=0.0001* δ13C chi-squared=18.775; p=0.0001*	δ15N chi-squared=4.1876; p=0.0407* δ13C chi-squared=7.9109; p=0.0049*	δ15N chi-squared=21.229; p=0.0001* δ13C chi-squared=0.0419; p=0.8376
Latitude strata	δ15N chi-squared=36.754; p=0.0001* δ13C chi-squared=20.840; p=0.0003*	δ15N chi-squared=14.904; p=0.0049* δ13C chi-squared=9.4218; p=0.0514	δ15N chi-squared=1.8005; p=0.1797 δ13C chi-squared=0.0244; p=0.8757
Ontogeny	δ15N chi-squared=1.5287; p=0.2100 δ13C chi-squared=1.9023; p=0.1600	δ15N chi-squared=0.0156; p=0.9005 δ13C chi-squared=0.9541; p=0.3287	-

FIGURE 4 |
Isotopic ratios of carbon (δ¹³C) and nitrogen (δ¹⁵N) of Haemulon plumierii, H. aurolineatum, and H. squamipinna in different habitats and shelf position captured along the northeast coast of Brazil. The black horizontal line and box represent the median value and the interquartile range, while the vertical lines represent the upper and lower limits. Outliers were not included in the plot. Different symbols (* and **) represent significant difference.

Significantly higher values of δ¹⁵N ratio were measured in H. plumierii in latitude A than in latitudes C, D and E (Tab. 3; Fig. 5). The values of δ¹⁵N ratio in H. aurolineatum varied significantly between strata A and B, A and D, A and E, B and D, and B and E. For both species, the highest values were measured in the southernmost zones (Tab. 3; Fig. 5). Unlike the other two species, H. squamipinna, was only sampled in latitudes D and E and no significant difference between of δ¹⁵N. No significant differences of δ¹⁵N were recorded between adults and juveniles for any species (Tab. 3; Fig. 5).

FIGURE 5 |
Isotopic ratios of carbon (δ¹³C) and nitrogen (δ¹⁵N) of Haemulon plumierii, H. aurolineatum and H. squamipinna in different latitude gradient and ontogeny captured along the northeast coast of Brazil. The black horizontal line and box represent the median value and the interquartile range, while the vertical lines represent the upper and lower limits. Outliers were not included in the plot. *All caught specimens of H. squamipinna were considered adults, not allowing ontogenetic analysis. Different symbols (*, ** and **) represent significant difference. Ontogeny* - All caught specimens of H. squamipinna were considered adults, not allowing ontogenetic analysis.

The trophic level was similar for all species, between the 3^rd and 4^th trophic position, classifying all species as carnivore predators. The trophic level was not significantly affected by any abiotic factor (Tab. 4).

All species had generally significant differences in mean δ¹³C ratio (Kruskal-Wallis; chi-squared=35.822; p=0.0001, Kruskal-Wallis) but not in δ¹⁵N (Kruskal-Wallis; chi-squared=3.6714; p=0.160). These differences were partly reflected in the isotopic niche of Haemulidae since H. aurolineatum (2.57 ‰; CI95 2.1–3.0 ‰) and H. plumierii (2.33 ‰; CI95 1.8–2.8 ‰) had similar SEAs (Fig. 6A). These later comprehended more than two folds of the area occupied by H. squamipina (1.02 ‰; CI95 0.7–1.3 ‰). Although only 9.6% of the total area occupied by them (3.51 ‰) was shared by the three species, the percentage of overlap between their isotopic niches varied according to each pairing of species (Fig. 6B). Particularly, H. aurolineatum occupied considerable part of the SEAs of both H. plumierii (71.2%; CI95 45.9–94.8%) and H. squamipina (68.9%; CI95 37.2–99.8%). The opposite was only true for H. plumierii, which shared 64.3% (CI95 41.6–87.6%) of H. aurolineatum isotopic niche. Haumulon squamipina and H. plumierii shared smaller percentages of their areas with each other (Fig. 6B). In turn, overlaps in their total SEAs were higher between H. aurolineatum - H. plumierii (51.6%; CI95 28.4–75.3%) than H. aurolineatum - H. squamipina (24.7%; CI95 9.7–40.0%), and H. plumierii - H. squamipina (12.1%; CI95 0–24.8%).

TABLE 4 |
Trophic position of Haemulon species estimated based on the stable isotopes analysis (TP_SIA), its upper and lower limits, based on α=95%, and its standard deviation.

Species	Mean trophic position	Lower limit	Upper limit	Standard deviation
H. aurolineatum	3.74	3.56	3.92	0.090
H. plumierii	3.81	3.63	4.00	0.094
H. squamipinna	3.71	3.56	3.89	0.085

FIGURE 6 |
A. Scaled isotopic niches and B. Isotopic overlap of Haemulon aurolineatum, H. plumierii and H. squamipina captured along the northeast coast of Brazil.

DISCUSSION

Haemulidae play a crucial role in the tropical Brazilian marine food web as they act as a linkage between lower trophic levels and the top predators. We analyzed the feeding habits and trophic ecology of three important Haemulidae species on the coast of the Northeast Brazil. It is important to mention that this is the first study about Haemulon genus on a large spatial scale (tropical Brazilian continental shelf), encompassing the feeding habits of three species applying a combination of approaches (stomach content and isotopic analysis).

Haemulon aurolineatum and H. plumierii were classified as nocturnal feeders, since most individuals with no food content were caught at daytime. It is recorded that Haemulidae are observed schooling during the day when the risk of predation is greater (Burke, 1995; Coxey, 2008). This behavior is related to the predator scape behavior (Danilowicz, Sale, 1999). However, Pereira, Ferreira, (2013) also found a high frequency of foraging during the daytime for species of the family Haemulidae. In addition, they observed that juveniles preferred feeding in the water column, while adults foraged mainly in sand and bare rock (Pereira, Ferreira, 2013). The formation of schools for Haemulidae fishes may be related to the protective function and anti-predation mechanism (Ward et al., 2002; Braga et al., 2009), but also, with increased efficiency in foraging (Pereira, Ferreira, 2013).

Feeding intensity, described by the Fi index, can be affected by availability and type of prey, size and season (Mondal, Mitra, 2016; Perelman et al., 2017). At latitudes below 08° S, specifically, in areas where the abundance of Haemulidae species is well-known to be very high (Eduardo et al., 2018; Cardoso de Melo et al., 2020) were found higher values of Fi. The very abundant populations of Haemulidae in this area are supported by extensive coral reefs, supported by the existence of two Marine Protected Areas (“Costa dos Corais” and “Guadalupe”) (Pereira et al., 2021), which help to maintain the environmental stability providing better conditions for the biodiversity. In addition, small resurgence processes have been reported close to these locations, which increase the supply of nutrients from the deepest layer to the surface, generating primary production, attracting prey and thus increasing food availability for the fish assemblages (MMA, 2006). Feeding intensity also differed among shelf position, with fish caught near the coast presenting higher Fi values than fish from the deeper areas, and higher Fi values reported for juveniles rather than adults. Just as for ontogeny, with higher values for juveniles than adults. As observed in our study, in the Caribbean (Verweij et al., 2006), and other Brazilian areas (Pereira, Ferreira, 2013), life phase and schooling patterns have direct effects on the foraging behaviour of coral-reef fishes from the genus Haemulon. Adults and juveniles of Haemulon genus have different foraging behaviour, where juveniles had higher Fi than adults, which have less active diurnal feeding rate than juveniles (Verweij et al., 2006).

All species preyed on a wide variety of items, mainly epibenthic organisms, such as polychaetas, crustaceans, and echinoderms. Fishes were also especially important on the diet of H. plumierii. This fact, together with the moderate/high spectrum of prey and the results of the feeding strategy analyses, suggested that H. plumierii may be considered as generalist predators. Haemulon species seem to have a wide trophic plasticity, feeding on preys directly associated to reef environments. For example, crustaceans and, in a smaller proportion, mollusks, echinoderms, polychaetas, and teleosts are prey items often found in the diet of these species on the reefs of Santa Marta, Colombia (Estrada, 1986), Panamá Channel (Heck, Weinstein, 1989), Rio Grande do Norte, Brazil (Silva et al., 2018) and Bahamas (Layman, Silliman, 2002), indicating that they have a similar feeding pattern regardless of its distribution (Pereira et al., 2015).

For both species, H. aurolineatum and H. plumierii, a large percentage of digested organic matter was recorded. Similarly, other studies reported a large amount of unidentified organic matter and invertebrates was observed in most stomachs of Haemulon (Hammerschlag et al., 2010). Due to the high degree of digestion (Aguiar, Filomeno, 1995; Pereira et al., 2015; Hornbeck, 2017; Medeiros et al., 2017), most stomachs found during the day are in final digestion process, often with only small exoskeletons parts, while at night, where foraging is observed, items are still in the initial digestion process (Hammerschlag et al., 2010).

Isotopic analysis indicated higher values of δ¹⁵N in H. aurolineatum and H. plumierii for specimens collected in the inner platform, which may be related to the continental contribution of human sources as fertilizers and sewage that could assimilate in preys (Weber, 1992; Noriega et al., 2005; Guimarães, Mello, 2006). Nitrogen from wastewater generally has higher values of δ¹⁵N than inorganic nitrogen from the marine environment, due to its human or animal origin and also isotopic discrimination during remineralization processes (volatilization of ¹⁴N-ammonium during ammonification), with higher δ¹⁵N values in coastal areas (Lepoint et al., 2004). Haemulidae, may change their isotopic composition along ontogeny, the adults are more generalists and can feed on larger preys compared to juveniles that have more specialized diets (Pereira, Ferreira, 2013). However, it was not observed for any species in this study.

Overall, the species were classified as tertiary carnivorous consumer, with trophic position ranging between 3 and 4. On the eastern Pacific and Caribbean coast of Panama in Central America, trophic level obtained for three Haemulidae species, two of Haemulon genus, showed results similar to those obtained in this study, remaining in same range, characterizing them as secondary predators, with a predominant zoobenthivorous habit (Stuthmann, Castellanos-Galindo, 2020). The common species in both studies (H. plumierii) had values close to those found here, although baseline choices were different.

Haemulidae tend to be generalists, with no specific preference, preying on what is more abundant or available in the environment (Flores-Ortega et al., 2014). Although with similar values of the niche breadth, H. plumierii seemed to be more generalist than H. aurolineatum, which might be explained by the fact that the former species is naturally of larger size. Larger individuals usually had larger digestive and oral apparatus, being able to capture a greater variety of prey size (Restrepo-Gómez, Mancera-Rodríguez, 2014; Pereira et al., 2015). Also, larger individuals are generally more efficient at chasing and capturing preys (Gerking, 1994; Cardoso et al., 2019).

Haemulon aurolineatum and H. plumierii had high diet overlapping, meaning they share more than three quarters of their prey items. Although H. aurolineatum and H. squamipinna often have similar high habitat affinity, population size and body shape (Pereira et al., 2015, 2021), according to Cardoso et al., (2019), in our study area with the same data base, H. squamipinna was not found at latitudes lower than 07°S. Meanwhile, H. aurolineatum and H. plumierii were jointly observed throughout the entire area. In addition, H. aurolineatum and H. plumierii displayed high affinity with the habitats of Sand With Coral and Rocks (SWCR), Sandy and Algae, while H. squamipinna was associated with sand and SWCR bottoms (Eduardo et al., 2018; Cardoso et al., 2019). Therefore, the higher similarity in the habitat uses among H. aurolineatum and H. plumierii, may have led to a greater prey sharing, resulting in a high diet overlapping. This was already reported in different regions, such as in Paraíba, Northeast Brazil (Medeiros et al., 2017) and Curaçao Island (Morinière et al., 2003), indicating that these species have been always partitioning resources in the different ecosystems they inhabit. However, given the diversity of preys there is no indication of competition.

The integrate techniques (stomach content and stable isotopes analysis) have been successfully implemented to understand spatial and ontogenetic factors for many fish species such as omnivores, benthivores, herbivores and for big predators (Nagelkerken et al., 2008; Rosende-Pereiro et al., 2019; Zhu et al., 2019) and showed complementary responses in the present study. The Haemulidae trophic ecology patterns found in this portion of the South Atlantic, carnivorous predator with trophic position varying between 3 and 4, resemble different locations around the globe.

Haemulidae fishes are considered of high socioeconomical importance, especially for the artisanal fleet, but management and conservative strategies are still lacking in the Brazilian coast, since these species exploitation is, currently, of open access. Moreover, although the effort to conserve reef ecosystems and species have increased overtime, they are still insufficient to mitigate or reverse the increasing anthropogenic impacts in this area, despite the relatively high number of Marine Protected Areas (MPA), which are not necessarily managed and/or enforced given the absence of information. Increasing knowledge about the fish biology and their respective relationships with their habitats and other species is essential for identifying priority areas for conservation in an ecosystem basis, especially in rich reef zones that are under several increasing pressures, as those in Northeast Brazil, also considered as an EBSA (Ecologically or Biologically Significant; CBD, 2014).

ACKNOWLEDGEMENTS

We acknowledge the French oceanographic fleet and IRD for sponsoring and guiding the research and every member of R/V Antea for their support. This study was partially sponsored by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) though a scholarship granted to Ádamo Limeira and Conselho Nacioanl de Desenvolvimento Científico e Tecnológico (CNPq), through a productivity research grant to FLF and TF. This work is a contribution to the LMI TAPIOCA and program CAPES/COFECUB (88881.142689/2017–01).

REFERENCES

• Aguiar JBS, Filomeno MJB Hábitos alimentares de Orthopristis ruber (Cuvier, 1830), (Osteichthyes – Haemulidae) na Lagoa de Conceição – SC, Brasil. Biotemas. 1995; 8(2):41–49.
• Amundsen PA, Gabler HM, Staldvik FJ. A new approach to graphical analysis of feeding strategy from stomach contents data - modification of the Costello (1990) method. J Fish Biol. 1996; 48(4):607–14. https://doi.org/10.1111/j.1095-8649.1996.tb01455.x
  » https://doi.org/10.1111/j.1095-8649.1996.tb01455.x
• Bastos RF, Corrêa F, Winemiller KO, Garcia AM. Are you what you eat? Effects of trophic discrimination factors on estimates of food assimilation and trophic position with a new estimation method. Ecological Indicators. 2017; 75:234–41. https://doi.org/10.1016/J.ECOLIND.2016.12.007
  » https://doi.org/10.1016/J.ECOLIND.2016.12.007
• Ben-David M, Flaherty EA Stable isotopes in mammalian research: A beginner’s guide. J Mammal. 2012; 93(2):312–28. https://doi.org/10.1644/11-MAMM-S-166.1
  » https://doi.org/10.1644/11-MAMM-S-166.1
• Bertrand A. ABRACOS 2 cruise, R/V Antea. 2017. https://doi.org/10.17600/17004100
  » https://doi.org/10.17600/17004100
• Bertrand A. ABRACOS cruise, R/V Antea. 2015. https://doi.org/10.17600/15005600
  » https://doi.org/10.17600/15005600
• Bowen SH. Quantitative description of the diet. Fisheries Techniques. 1996.
• Braga MR, Braga RR, Aranha JMR. Registro de cardume misto de espécies da família Haemulidae nas Ilhas Itacolomis, Santa Catarina, Brasil. Estud Biol. 2009; 31(73/75). https://doi.org/10.7213/REB.V31I73/75.22854
  » https://doi.org/10.7213/REB.V31I73/75.22854
• Burke NC. Nocturnal foraging habitats of French and bluestriped grunts, Haemulon flavolineatum and H. sciurus, at Tobacco Caye, Belize. Environ Biol Fish. 1995; 42(4):365–74. https://doi.org/10.1007/BF00001467
  » https://doi.org/10.1007/BF00001467
• Cardoso DC, Dehart P, Freitas CEC, Siqueira-Souza FK. Diet and ecomorphology of predator fish species of the Amazonian floodplain lakes. Biota Neotrop. 2019; 19(3):20180678. https://doi.org/10.1590/1676-0611-BN-2018-0678
  » https://doi.org/10.1590/1676-0611-BN-2018-0678
• Cardoso de Melo C, Soares APC, Pelage L, Eduardo LN, Frédou T, Lira AS et al Haemulidae distribution patterns along the Northeastern Brazilian continental shelf and size at first maturity of the most abundant species. Reg Stud Mar Sci. 2020; 35:101226. https://doi.org/10.1016/j.rsma.2020.101226
  » https://doi.org/10.1016/j.rsma.2020.101226
• Convention on Biological Diversity (CBD). Wider Caribbean and Western Mid-Atlantic Region, Ecologically or Biologically Significant Marine Areas (EBSAs). Special places in the world’s oceans. 2014; Vol 2.
• Cerqueira NNCD, Rotundo MM, Marceniuk AP, Cruz VP, Foresti F, Oliveira C. Molecular identification of Brachygenys and Haemulon species (Perciformes: Haemulidae) from the Brazilian coast. Neotrop Ichthyol. 2021; 19(2):e200109. https://doi.org/10.1590/1982-0224-2020-0109
  » https://doi.org/10.1590/1982-0224-2020-0109
• Chittaro PM, Fryer BJ, Sale PF. Discrimination of French grunts (Haemulon flavolineatum, Desmarest, 1823) from mangrove and coral reef habitats using otolith microchemistry. J Exp Mar Biol Ecol. 2004; 308(2):169–83. https://doi.org/10.1016/J.JEMBE.2004.02.021
  » https://doi.org/10.1016/J.JEMBE.2004.02.021
• Coxey MSGS. Biological diversity and community structure of the ichthyofauna on Vessel Reefs in the Coast of Recife (PE)-Brazil. [Master Dissertation]. Faro: Universidade do Algarve; 2008. Available from: http://hdl.handle.net/10400.1/7115
  » http://hdl.handle.net/10400.1/7115
• Danilowicz BS, Sale PF. Relative intensity of predation on the French grunt, Haemulon flavolineatum, during diurnal, dusk, and nocturnal periods on a coral reef. Mar Biol. 1999; 133:337–43. https://doi.org/10.1007/S002270050472
  » https://doi.org/10.1007/S002270050472
• Eduardo LN, Frédou T, Lira AS, Ferreira BP, Bertrand A, Ménard F et al Identifying key habitat and spatial patterns of fish biodiversity in the tropical Brazilian continental shelf. Cont Shelf Res. 2018; 166:108–18. https://doi.org/10.1016/j.csr.2018.07.002
  » https://doi.org/10.1016/j.csr.2018.07.002
• Esteves KE, Aranha JMR. Ecologia trófica de peixes de riachos. Oecol. 1999; 6(1):157–82. https://doi.org/10.4257/oeco.1999.0601.05
  » https://doi.org/10.4257/oeco.1999.0601.05
• Estrada MR. Habitos alimentarios de los Peces del genero Haemulon (Pisces: Haemulidae) de los arrecifes de la region de Santa Marta, Colombia. Bol Investig Mar Costeras. 1986; 15:49–66. https://doi.org/10.25268/BIMC.INVEMAR.1986.15.0.464
  » https://doi.org/10.25268/BIMC.INVEMAR.1986.15.0.464
• Frédou T, Ferreira BP, Letourneur Y. Assessing the stocks of the primary snappers caught in Northeastern Brazilian reef sys- tems. 1: Traditional modelling approaches. Fish Res. 2009; 99(2):90–96. https://doi.org/10.1016/j.fishres.2009.05.008
  » https://doi.org/10.1016/j.fishres.2009.05.008
• Ferreira BP, Maida M. Características e perspectivas para o manejo da pesca na area de proteção ambiental marinha Costa dos Corais. In: Blanc D, editor. Áreas aquaticas protegidas como instrumento de gestão pesqueira. Brasília: Ministério do Meio Ambiente; 2007. p.41–51.
• Figueiredo GGAA de, Schwamborn R, Bertrand A, Munaron J-M, Le Loc’h F. Body size and stable isotope composition of zooplankton in the western tropical Atlantic. J Mar Syst. 2020; 212:103449. https://doi.org/10.1016/J.JMARSYS.2020.103449
  » https://doi.org/10.1016/J.JMARSYS.2020.103449
• Flores-Ortega JR, Avila-Castro E, Haro-Preciado HJ, Godínez-Domínguez E. Hábitos alimentarios e interacciones tróficas de Anisotremus interruptus (Pisces: Haemulidae) y Lutjanus argentiventris (Pisces: Lutjanidae) en el Pacífico Central Mexicano. Lat Am J Aquat Res. 2014; 42(1):276–82.
• Freitas MO, Abilhoa V, Costa e Silva GH. Feeding ecology of Lutjanus analis (Teleostei: Lutjanidae) from Abrolhos Bank, Eastern Brazil. Neotrop Ichthyol. 2011; 9(2):411–18. https://doi.org/10.1590/S1679-62252011005000022
  » https://doi.org/10.1590/S1679-62252011005000022
• Freitas MO, Abilhoa V, Spach HL, Minte-Vera CV, Francini-Filho RB, Kaufman L et al Feeding ecology of two sympatric species of large-sized groupers (Perciformes: Epinephelidae) on Southwestern Atlantic coralline reefs. Neotrop Ichthyol. 2017; 15(2):160047. https://doi.org/10.1590/1982-0224-20160047
  » https://doi.org/10.1590/1982-0224-20160047
• Fry B. Stable Isotope Ecology. New York: Springer; 2006.
• Fry B. Food web structure on Georges Bank from stable C, N and S isotopic composition. Am Soc Limnol Oceanogr. 1988; 33(5):1182–90.
• Gerking SD. Feeding ecology of fish. San Diego: Academic Press; 1994.
• Gheler-Costa C, Botero GP, Reia L, Cassia Gilli L, Comin FH, Verdade LM. Ecologia trófica de onça-parda (Puma concolor) em paisagem agrícola. Rev Agronegócio Meio Ambiente. 2018; 11(1):203–25. https://doi.org/10.17765/2176-9168.2018V11N1P203-225
  » https://doi.org/10.17765/2176-9168.2018V11N1P203-225
• Gonzalez JG, Ménard F, le Loc’h F, Andrade HA, Viana AP, Ferreira V et al Trophic resource partitioning of two snook fish species (Centropomidae) in tropical estuaries in Brazil as evidenced by stable isotope analysis. Estuar Coast Shelf Sci. 2019; 226:106287. https://doi.org/10.1016/J.ECSS.2019.106287
  » https://doi.org/10.1016/J.ECSS.2019.106287
• Guimarães GP, Mello WZ. Estimativa do fluxo de amônia na interface ar-mar na Baía de Guanabara: estudo preliminar. Quím Nova. 2006; 29(1):54–60. https://doi.org/10.1590/S0100-40422006000100012
  » https://doi.org/10.1590/S0100-40422006000100012
• Hahn NS, Fugi R, Peretti D, Russo MR, Loureiro-Crippa VE. Estrutura trófica da ictiofauna da planície de inundação do alto rio Paraná. In: Agostinho AA, Thomaz SM, Rodrigues L, Gomes LC, editors. A planície de inundação do Alto rio Paraná. Maringá: Area de Pesquisas Ecológicas de Longa Duração, Núcleo de Pesquisas em Limnologia, Ictiologia e Aqüicultura-Nupelia, Universidade Estadual de Maringá. Maringá: Universidade Estadual de Maringá; 2002. p.123–26.
• Hammerschlag N, Ovando D, Serafy JE. Seasonal diet and feeding habits of juvenile fishes foraging along a subtropical marine ecotone. Aquatic Biol. 2010; 9(3):279–90. https://doi.org/10.3354/AB00251
  » https://doi.org/10.3354/AB00251
• Heck KL, Weinstein MP. Feeding habits of juvenile reef fishes associated with panamanian seagrass meadows. Bull Mar Sci. 1989; 45(3):629–36.
• Hornbeck JR. A comparison of the ichthyofaunal trophic ecology at selected limestone artificial reef sites and adjacent natural reef sites. [Master Dissertation]. Florida: Nova Southeastern University. 2017. Available from: https://nsuworks.nova.edu/occ_stuetd/438/
  » https://nsuworks.nova.edu/occ_stuetd/438/
• Hurlbert SH. The measurement of niche overlap and some relatives. Ecology. 1978; 59(1):67–77. https://doi.org/10.2307/1936632
  » https://doi.org/10.2307/1936632
• Hyslop EJ. Stomach contents analysis-a review of methods and their application. J Fish Biol. 1980; 17(4):411–29. https://doi.org/10.1111/j.1095-8649.1980.tb02775.x
  » https://doi.org/10.1111/j.1095-8649.1980.tb02775.x
• Ilarri MDI, Souza AT, Medeiros PR, Grempel RG, Lucena Rosa IM. Effects of tourist visitation and supplementary feeding on fish assemblage composition on a tropical reef in the Southwestern Atlantic. Neotrop Ichthyol. 2008; 6(4):651–56. https://doi.org/10.1590/S1679-62252008000400014
  » https://doi.org/10.1590/S1679-62252008000400014
• Jackson AL, Inger R, Parnell AC, Bearhop S. Comparing isotopic niche widths among and within communities: SIBER – Stable Isotope Bayesian Ellipses in R. J Anim Ecol. 2011; 80(3):595–602. https://doi.org/10.1111/J.1365-2656.2011.01806.X
  » https://doi.org/10.1111/J.1365-2656.2011.01806.X
• Kawakami E, Vazzoler G. Método gráfico e estimatica de índice alimentar aplicado no estudo de alimentação de peixes. Bol Inst Oceanogr. 1980; 29(2):205–07. https://doi.org/10.1590/S0373-55241980000200043
  » https://doi.org/10.1590/S0373-55241980000200043
• Layman CA, Silliman BR. Preliminary survey and diet analysis of juvenile fishes of an estuarine creek on Andros Island, Bahamas. Bull Mar Sci. 2002; 70(1):199–210. Available from: https://craiglayman.com/wp-content/uploads/Layman-and-Silliman-2002.pdf
  » https://craiglayman.com/wp-content/uploads/Layman-and-Silliman-2002.pdf
• Lepoint G, Dauby P, Gobert S. Applications of C and N stable isotopes to ecological and environmental studies in seagrass ecosystems. Mar Pollut Bull. 2004; 49(11–12):887–91. https://doi.org/10.1016/J.MARPOLBUL.2004.07.005
  » https://doi.org/10.1016/J.MARPOLBUL.2004.07.005
• Lessa R, Nóbrega MF. Guia de identificação de peixes marinhos da região Nordeste. Programa REVIZEE/SCORE-NE. Recife: DIMAR; 2000. Available from: https://www.pesca.pet/wp-content/uploads/2018/10/Lessa_Nobrega_2000.pdf
  » https://www.pesca.pet/wp-content/uploads/2018/10/Lessa_Nobrega_2000.pdf
• Marques S, Ferreira BP. Composição e características da pesca de armadilhas no litoral norte de Pernambuco - Brasil. Bol Téc Cient CEPENE. 2010; 18(1):49–60.
• Medeiros APM, Xavier JHA, Rosa IML. Diet and trophic organization of the fish assemblage from the Mamanguape River Estuary, Brazil. Lat Am J Aquat Res. 2017; 45(5):879–90. http://dx.doi.org/10.3856/vol45-issue5-fulltext-2
  » http://dx.doi.org/10.3856/vol45-issue5-fulltext-2
• Melville AJ, Connolly RM. Spatial analysis of stable isotope data to determine primary sources of nutrition for fish. Oecologia. 2003; 136:499–507. https://doi.org/10.1007/S00442-003-1302-8
  » https://doi.org/10.1007/S00442-003-1302-8
• Ministerio do Meio Ambiente (MMA). Programa REVIZEE. Avaliação do potencial sustentavel de recursos vivos na zona economica exclusiva. Brasília - DF: Ministério do Meio Ambiente; 2006.
• Mondal A, Mitra A. Growth, food and feeding habit with prey preference of long whiskered catfish, Mystus gulio (Hamilton, 1822) in brackishwater traditional impoundments of Sundarban, India. Int J Fish Aquat Stud. 2016; 4(6):49–58. Available from: https://www.fisheriesjournal.com/archives/2016/vol4issue6/PartA/4-5-80-765.pdf
  » https://www.fisheriesjournal.com/archives/2016/vol4issue6/PartA/4-5-80-765.pdf
• Morinière EC de la, Pollux BJA, Nagelkerken I, van der Velde G. Diet shifts of Caribbean grunts (Haemulidae) and snappers (Lutjanidae) and the relation with nursery-to-coral reef migrations. Estuar Coast Shelf Sci. 2003; 57(5–6):1079–89. https://doi.org/10.1016/S0272-7714(03)00011-8
  » https://doi.org/10.1016/S0272-7714(03)00011-8
• Nagelkerken I, Bothwell J, Nemeth RS, Pitt JM, van der Velde G. Interlinkage between Caribbean coral reefs and seagrass beds through feeding migrations by grunts (Haemulidae) depends on habitat accessibility. Mar Ecol Prog Ser. 2008; 368:155–64. https://doi.org/10.3354/MEPS07528
  » https://doi.org/10.3354/MEPS07528
• Nóbrega MF de, Lessa R. Descrição e composição das capturas da frota pesqueira artesanal da região Nordeste do Brasil. Arq Ciênc Mar. 2007; 40(2):64–74. Available from: http://www.repositorio.ufc.br/handle/riufc/53821
  » http://www.repositorio.ufc.br/handle/riufc/53821
• Noriega CD, Muniz K, Araújo MC, Travassos RK, Neumann-Leitão S. Fluxos de nutrientes inorgânicos dissolvidos em um estuário tropical – Barra das Jangadas – PE, Brasil. Trop Oceanogr. 2005; 33(2):133–45. https://doi.org/10.5914/TROPOCEAN.V33I2.5057
  » https://doi.org/10.5914/TROPOCEAN.V33I2.5057
• Oliveira AK, Alvim MCC, Peret AC, Alves CBM. Diet shifts related to body size of the pirambeba Serrasalmus brandtii Lütken, 1875 (Osteichthyes, Serrasalminae) in the Cajuru Reservoir, São Francisco River Basin, Brazil. Braz J Biol. 2004; 64(1):117–24. https://doi.org/10.1590/S1519-69842004000100013
  » https://doi.org/10.1590/S1519-69842004000100013
• Palazón-Fernández JL. Reproduction of the white grunt, Haemulon plumieri (Lacépede, 1802) (Pisces: Haemulidae) from Margarita Island, Venezuela. Sci Mar. 2007; 71(3):429–40. https://doi.org/10.3989/SCIMAR.2007.71N3429
  » https://doi.org/10.3989/SCIMAR.2007.71N3429
• Parrish JD. Fish communities of interacting shallow-water habitats in tropical oceanic regions. Mar Ecol Prog Ser. 1989; 58:143–60. https://doi.org/10.3354/MEPS058143
  » https://doi.org/10.3354/MEPS058143
• Pereira PHC, Feitosa JLL, Ferreira BP Mixed-species schooling behaviour and protective mimicry involving coral reef fish from the genus Haemulon Neotrop Ichthyol. 2011. 9(4):741–46. https://doi.org/10.1590/S1679-62252011005000037
  » https://doi.org/10.1590/S1679-62252011005000037
• Pereira PHC, Barros B, Zemoi R, Ferreira BP. Ontogenetic diet changes and food partitioning of Haemulon spp. coral reef fishes, with a review of the genus diet. Rev Fish Biol Fish. 2015; 25(1):245–60. https://doi.org/10.1007/s11160-014-9378-2
  » https://doi.org/10.1007/s11160-014-9378-2
• Pereira PHC, Ferreira BP. Effects of life phase and schooling patterns on the foraging behaviour of coral-reef fishes from the genus Haemulon J Fish Biol. 2013; 82(4):1226–38. https://doi.org/10.1111/JFB.12054
  » https://doi.org/10.1111/JFB.12054
• Pereira PHC, Côrtes LGF, Lima GV, Gomes E, Pontes AVF, Mattos F et al Reef fishes biodiversity and conservation at the largest Brazilian coastal Marine Protected Area (MPA Costa dos Corais). Neotrop Ichthyol. 2021; 19(4):e210071. https://doi.org/10.1590/1982-0224-2021-0071
  » https://doi.org/10.1590/1982-0224-2021-0071
• Perelman JN, Schmidt KN, Haro I, Tibbetts IR, Zischke MT. Feeding dynamics, consumption rates and daily ration of wahoo Acanthocybium solandri in Indo-Pacific waters. J Fish Biol. 2017; 90(5):1842–60. https://doi.org/10.1111/jfb.13270
  » https://doi.org/10.1111/jfb.13270
• Peterson BJ, Fry B. Stable isotopes in ecosystem studies. Annu Rev Ecol Syst. 1987; 18:293–320. https://doi.org/10.1146/annurev.es.18.110187.001453
  » https://doi.org/10.1146/annurev.es.18.110187.001453
• Peterson CT, Grubbs RD, Mickle A. Trophic ecology of elasmobranch and teleost fishes in a large subtropical seagrass ecosystem (Florida Big Bend) determined by stable isotope analysis. Environ Biol Fish. 2020; 103:683–701. https://doi.org/10.1007/S10641-020-00976-7
  » https://doi.org/10.1007/S10641-020-00976-7
• Pianka ER. The structure of lizard communities. Ann Rev Ecol Syst. 1973; 4:53–77. http://dx.doi.org/10.1146/annurev.es.04.110173.000413
  » http://dx.doi.org/10.1146/annurev.es.04.110173.000413
• Pimentel CR, Soares LSH, Macieira RM, Joyeux J-C. Trophic relationships in tidepool fish assemblages of the tropical Southwestern Atlantic. Mar Ecol. 2018; 39(2):e12496. https://doi.org/10.1111/MAEC.12496
  » https://doi.org/10.1111/MAEC.12496
• Pinkas L, Oliphant MS, Iverson ILK. Fish Bulletin 152. Food habits of albacore, bluefin tuna, and bonito in California waters. Calif Dept Fish and Game Fish Bull. 1971.
• Post DM. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology. 2002; 83(3):703–18. https://doi.org/10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2
  » https://doi.org/10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2
• Quezada-Romegialli C, Jackson AL, Hayden B, Kahilainen KK, Lopes C, Harrod C. tRophicPosition, an r package for the Bayesian estimation of trophic position from consumer stable isotope ratios. Methods Ecol Evol. 2018; 9(6):1592–99. https://doi.org/10.1111/2041-210X.13009
  » https://doi.org/10.1111/2041-210X.13009
• Restrepo-Gómez A, Mancera-Rodríguez N. Trophic ecology of Saccodon dariensis (Pisces: Parodontidae) in Guatapé River tributaries, Magdalena River basin, Colombia. Rev MVZ Córdoba. 2014; 19(1):3930–43. https://doi.org/10.21897/RMVZ.113
  » https://doi.org/10.21897/RMVZ.113
• Richards TM, Gipson EE, Cook A, Sutton TT, Wells RJD. Trophic ecology of meso- and bathypelagic predatory fishes in the Gulf of Mexico. ICES J Mar Sci. 2019; 76(3):662–72. https://doi.org/10.1093/ICESJMS/FSY074
  » https://doi.org/10.1093/ICESJMS/FSY074
• Rindone RR, Kellison GT, Bortone SA. Data Availability for Red Snapper in Gulf of Mexico and Southeastern U.S. Atlantic Ocean Waters. N Am J Fish Manag. 2015; 35(2):191–204.https://doi.org/10.1080/02755947.2014.992559
  » https://doi.org/10.1080/02755947.2014.992559
• Rocha LA, Lindeman KC, Rocha CR, Lessios HA. Historical biogeography and speciation in the reef fish genus Haemulon (Teleostei: Haemulidae). Mol Phylogenet Evol. 2008; 48(3):918–28. https://doi.org/10.1016/J.YMPEV.2008.05.024
  » https://doi.org/10.1016/J.YMPEV.2008.05.024
• Rocha LA, Rosa IL. New species of Haemulon (Teleostei: Haemulidae) from the northeastern Brazilian coast. Copeia. 1999(2):447–52. https://doi.org/10.2307/1447491
  » https://doi.org/10.2307/1447491
• Rocha LA, Rosa IL, Rosa RS. Peixes recifais da costa da Paraíba, Brasil. Rev Bras Zool. 1998; 15(2):553–66. https://doi.org/10.1590/S0101-81751998000200017
  » https://doi.org/10.1590/S0101-81751998000200017
• Rosende-Pereiro A, Flores-Ortega JR, González-Sansón G, Corgos A. Stomach content and stable isotopes reveal an ontogenetic dietary shift of young-of-the-year scalloped hammerhead sharks (Sphyrna lewini) inhabiting coastal nursery areas. Environ Biol Fish. 2019; 103(1):49–65. https://doi.org/10.1007/S10641-019-00932-0
  » https://doi.org/10.1007/S10641-019-00932-0
• Shinozaki-Mendes RA, Santander-Neto J, Silva JRF, Hazin FHV. Reproductive biology of Haemulon plumieri (Teleostei: Haemulidae) in Ceará state, Northeastern Brazil. Braz J Biol. 2013; 73(2):391–96. https://doi.org/10.1590/S1519-69842013000200020
  » https://doi.org/10.1590/S1519-69842013000200020
• Silva JDB, Barletta M, Lima ARA, Ferreira GVB. Use of resources and microplastic contamination throughout the life cycle of grunts (Haemulidae) in a tropical estuary. Environ Pollut. 2018; 242:1010–21. https://doi.org/10.1016/J.ENVPOL.2018.07.038
  » https://doi.org/10.1016/J.ENVPOL.2018.07.038
• Soares A, Lira AS, Gonzalez JG, Eduardo LN, Lucena-Frédou F, le Loc’H F et al Feeding habits and population aspects of the spotted goatfish, Pseudupeneus maculatus (Perciformes: Mullidae), on the continental shelf of northeast Brazil. Sci Mar. 2020; 84(2):119–31.
• Stuthmann LE, Castellanos-Galindo GA. Trophic position and isotopic niche of mangrove fish assemblages at both sides of the Isthmus of Panama. Bull Mar Sci. 2020; 96(3):449–67. https://doi.org/10.5343/BMS.2019.0025
  » https://doi.org/10.5343/BMS.2019.0025
• Tavera JJ, Acero P A, Balart EF, Bernardi G. Molecular phylogeny of grunts (Teleostei, Haemulidae), with an emphasis on the ecology, evolution, and speciation history of New World species. BMC Evol Biol. 2012; 12(57):1–16. https://doi.org/10.1186/1471-2148-12-57
  » https://doi.org/10.1186/1471-2148-12-57
• Vanderklift MA, Ponsard S. Sources of variation in consumer-diet δ15N enrichment: A meta-analysis. Oecologia. 2003; 136:169–82. https://doi.org/10.1007/s00442-003-1270-z
  » https://doi.org/10.1007/s00442-003-1270-z
• Vander-Zanden MJ, Cabana G, Rasmussen JB. Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Can J Fish Aquat Sci. 2011; 54(5):1142–58. https://doi.org/10.1139/F97-016
  » https://doi.org/10.1139/F97-016
• Verweij MC, Nagelkerken I, Wartenbergh SLJ, Pen IR, van der Velde G. Caribbean mangroves and seagrass beds as daytime feeding habitats for juvenile French grunts, Haemulon flavolineatum Mar Biol. 2006; 149:1291–99. https://doi.org/10.1007/S00227-006-0305-5
  » https://doi.org/10.1007/S00227-006-0305-5
• Vieira CCRT. Ecologia trófica do carapau-negrão e da cavala na região da Madeira. [Master Dissertation]. Lisboa: Universidade de Lisboa; 2019.
• Vital H, Gomes MP, Tabosa WF, Frazão EP, Santos CLA, Plácido Júnior JS. Characterization of the Brazilian continental shelf adjacent to Rio Grande do Norte State, NE Brazil. Braz J Oceanogr. 2010; 58(526):43–54. Available from: https://www.scielo.br/j/bjoce/a/fGXsDMsp7cQGRZnbhZHBXhc/?format=pdf⟨=en
  » https://www.scielo.br/j/bjoce/a/fGXsDMsp7cQGRZnbhZHBXhc/?format=pdf⟨=en
• Ward AJ, Axford S, Krause J. Mixed-species shoaling in fish: the sensory mechanisms and costs of shoal choice. Behav Ecol Sociobiol. 2002; 52:182–87. https://doi.org/10.1007/S00265-002-0505-Z
  » https://doi.org/10.1007/S00265-002-0505-Z
• Weber R. Sistemas costeiros e oceânicos. Quím Nova. 1992; 15(2):137–43. Available from: http://static.sites.sbq.org.br/quimicanova.sbq.org.br/pdf/Vol15No2_137_v15_n2_%284%29.pdf
  » http://static.sites.sbq.org.br/quimicanova.sbq.org.br/pdf/Vol15No2_137_v15_n2_%284%29.pdf
• Zavala-Camin LA. Introdução aos estudos sobre alimentação natural em peixes. 1st ed. Maringá: Editora da Universidade Estadual de Maringá; 1996.
• Zhu Y, Newman SP, Reid WDK, Polunin NVC. Fish stable isotope community structure of a Bahamian coral reef. Mar Biol. 2019; 166(160):1–14. https://doi.org/10.1007/S00227-019-3599-9
  » https://doi.org/10.1007/S00227-019-3599-9

ADDITIONAL NOTES

• HOW TO CITE THIS ARTICLE

  Limeira ÁGC, Frédou T, Soares APC, Lira AS, Le Loc´h F, Viana GFS, Rosa-Filho JS, Munaron JM, Lucena-Frédou F. Trophic ecology and resource partitioning of Haemulidae species along the Northeastern Brazilian continental shelf. Neotrop Ichthyol. 2022; 20(3):e220001. https://doi.org/10.1590/1982-0224-2022-0001

Edited-by

Osmar Luiz

Publication Dates

• Publication in this collection
  14 Oct 2022
• Date of issue
  2022

History

• Received
  06 Jan 2022
• Accepted
  04 Sept 2022