Trophic ecology of the demersal predator Brazilian flathead Percophis brasiliensis (Percophidae) in a coastal upwelling ecosystem, SW Atlantic

Arthur de Barros Bauer¹ and Luciano Gomes Fischer¹

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Abstract​

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Introduction​

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Studies on trophic interactions are important to understand several ecological aspects, such as resource partitioning, ecosystem function, and the transfer of nutrients and energy in the different ecosystem compartments (Paine, 1966; Schoener, 1974; Coll et al., 2009). There are several methods to study different aspects of feeding ecology (Braga et al., 2012; Pethybridge et al., 2018). One of the most traditional and effective methods is the stomach content analysis (SCA). This method allows to identify the prey with high taxonomic precision and quantifies the biomass, number, and frequency of the ingested items (Hyslop, 1980; Cortés, 1997). The approach requires a large number of samples and it provides a snapshot of diet (Baker et al., 2014). More recently, ecologists have used other methods, such as stable isotope analysis (SIA), to overcome some of the SCA limitations (Layman et al., 2012). The stable isotope ratios of nitrogen and carbon in an organism’s tissue reflect the isotopic ratio of the prey and also the environment (Bearhop et al., 2004). Stable isotope values of tissues reflect the diet assimilated over the period that the tissue was synthesized (Bearhop et al., 2002, 2004). For fishes, tissue turnover rates of muscle tissue can range from two to four weeks (Mont’Alverne et al., 2016) to several months (Hussey et al., 2012). Consequently, the use of both SCA and SIA provides a powerful tool to better elucidate diet, feeding behavior, and trophic ecology (Layman, Post, 2008).

In marine environments, variations in feeding habits and, consequently, in the trophic role of fishes are widely observed. Such diet variations are commonly related to ontogenetic development (e.g., Graham et al., 2007; Russo et al., 2007; Andrades et al., 2019), and seasonal fluctuations in prey availability (e.g.,Wellenreuther, Connell, 2002; Beukers-Stewart, Jones, 2004; Mendoza-Carranza, Vieira, 2008). Seasonal changes in the diet of marine species are frequently caused by changes in prey availability, often due to oceanographic processes such as coastal upwellings (Boje, Tomczak, 1978; Giralt et al., 2020).

In coastal ecosystems, upwellings are important oceanographic processes that induce several changes in the marine environment (Margalef, 1978). Upwellings transport nutrients from deep waters to the euphotic layer, leading to an increase in primary productivity and usually increasing the biomass of all trophic levels in a cascade effect (Boje, Tomczak, 1978; Cury et al., 2000; Fernandes et al., 2017). Consequently, it also changes the prey availability and induces seasonal shifts in the predators’ diet (Cury et al., 2000; Miller et al., 2010). Such upwelling events also modify the benthic-pelagic coupling that regulates the nutrient cycling and energy transfer between the benthic and pelagic domains (Navarrete et al., 2005; Dale et al., 2017). Upwellings may change the trophic role of a species, for example, if it shifts its primary diet from benthic to pelagic prey (and vice versa), thereby changing the dynamics and intensity of the benthic-pelagic coupling. Griffiths et al. (2017), in a review on benthic-pelagic coupling, point out that one of the important aspects little understood or quantified is the relative importance of fish predation in the benthic-pelagic coupling dynamics. The benthic-pelagic coupling plays a major role in marine ecosystems but there is little available information about the effects of upwelling-driven shifts on the trophic role of predators (Griffiths et al., 2017).

The coastal region of the SW Atlantic between the Cabo de São Tomé (~22°S) and Cabo Frio (~23°S), Brazil, is particularly known for the periodic coastal upwellings, more frequent (or intense) during the austral summer and winter-spring (Valentin et al., 1987; Campos et al., 2000; Silveira et al., 2000; Acha et al., 2004). These events induce the replacement of the oligotrophic and warm Tropical Water by the nutrient-rich and cold South Atlantic Central Water (SACW) (Valentin et al., 1987; Acha et al., 2004). In this system, changes in the composition and abundance of organisms (e.g.,phytoplankton,zooplankton, andpelagic squids) associated with upwellings were also detected (Costa, Fernandes, 1993; Valentin, Monteiro-Ribas, 1993; Sumida et al., 2005). This region is also considered one of the most productive areas for small and large-scale fisheries on the Brazilian coast (Costa et al., 2017), where the Brazilian flathead Percophis brasiliensis Quoy & Gaimard, 1825 (Percophidae) is one of the most commonly caught as bycatch in bottom trawl fisheries (FIPERJ, 2021).

Percophis brasiliensis isa demersal fish endemic to the coastal waters of SW Atlantic, occurring along 5,000 km of coastline, between Rio de Janeiro State, Brazil (22°S) to Santa Cruz Province, Argentina (47°S) (Bernardes et al., 2005; Cousseau, Perrotta, 2013). Percophis brasiliensis is a generalist predator that feeds mainly on Teleostei at the southernmost limit of its distribution (Milessi, Mari, 2012), but information concerning its trophic ecology is still lacking along the Brazilian coast, which covers most of the species distribution. Therefore, in the present study, we investigate possible seasonal and ontogenetic changes in the trophic interaction of P. brasiliensis from the upwelling ecosystem between the Cabo de São Tomé (~22°S) and Cabo Frio (~23°S), Brazil. As previously shown, upwelling ecosystems are highly dynamic, and biological communities are influenced by environmental changes, thus we expect to detect seasonal variations in the P. brasiliensis diet, and for that we use SCA. Also, we expect to find ontogenetic differences in the P. brasiliensis diet since there is evidence of ontogenetic migration where large-sized specimens are found in deeper waters than smaller ones (Barretto, 2007; Rodrigues et al., 2013), for this hypothesis, both SCA and SIA were used.

Material and methods

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Study area and sampling procedure. Percophis brasiliensis specimens were collected monthly between February 2017 and January 2018 from landings of small-scale bottom trawlers. Voucher specimens, as well as tissue samples for molecular studies, were deposited at the fish collection of the Instituto de Biodiversidade e Sustentabilidade – NUPEM, Universidade Federal do Rio de Janeiro (see Catelani et al., 2019), catalog numbers: NPM 2588, NPM 3813, and NPM 5642. The fisheries took place between20 to 50 m depth in the coastal area between 21°50’S to 22°50’S (Fig. 1). The sampled region is characterized by the strong northeast winds, which combined with the coastal morphology, produce strong and seasonal upwelling events, mainly during the summer and spring (Valentin et al., 1987; Campos et al., 2000; Silveira et al., 2000; Acha et al., 2004). To infer coastal upwelling events during the sampling period, the sea surface temperature (SST) was recorded at 2 to 4 h intervals with a data logger (HOBO Tidbit UTBI-001) fixed at 1 m deep in the rocky shores of Praia Grande, Arraial do Cabo, Rio de Janeiro, within the same upwelling ecosystem.

FIGURE 1| Location of the study area (in gray bordered by the dashed line), an upwelling ecosystem, SW Atlantic. The continuous line represents the isobaths of 10, 20, 50, and 100 meters deep.

Stomach content analysis. The 1016 collected specimens were stored in ice and transported to the laboratory immediately after landing and kept frozen until the processing. The total weight (TW, 0.1 g), total length (TL, 1.0 mm), and sex were recorded for each specimen. The stomachs were removed, fixed in buffered formalin solution (10%) for at least 24 h, and preserved in 70% alcohol solution. Prey items were identified to the lowest possible taxonomic level using a stereomicroscope, counted, and weighed (wet weight 0.001 g). Identification guides, taxonomic keys, and original descriptions were used to achieve a precise taxonomic identification (see Figueiredo, Menezes, 1978, 2000; Menezes, Figueiredo, 1980a,b, 1985; Melo, 1996; Costa et al., 2003; Fischer et al., 2011; Rossi-Wongtschowski et al., 2014; Brenha-Nunes et al., 2016; Marceniuk et al., 2016; Conversani et al., 2017; Giaretta et al., 2017; Santificetur et al., 2017). Diet was represented as the percent of the total ingested weight (%W), number (%N), and frequency of occurrence (%F). The stomach fullness index was estimated using the percentage of the stomach content weight in the predator body weight (% BW), by the equation: BW = 100 X SW/(TW-SW), where SW (g) is the stomach content weight and TW (g) the consumer total weight(Hyslop, 1980; Cortés, 1997). To investigate ontogenetic changes, reproduction information was combined with the number of specimens collected with non-empty stomachs. Percophis brasiliensis reach their first sexual maturity (i.e., L50) with 250 mm TL for males and 380 mm TL for females (Militelli, Macchi, 2001). Herein, specimens were classified into three ontogenetic groups: juveniles (200 – 359 mm TL), young adults (360 – 434 mm TL), and adults (435 – 615 mm TL).

Stable isotope analysis. Muscle tissue from P. brasiliensis (n = 41) was collected inside the study area during the austral summer, between December 2017 and January 2018. All samples were freeze-dried, powdered, and weighed (~1 mg) into tin capsules. Stable isotopes of nitrogen and carbon were analyzed using an Elemental Analyzer Continuous Flow Isotope Ratio Mass Spectrometer (Europa Hydra 20/20). Abundances of stable isotopes are expressed in delta (δ) values in parts per thousand (‰), as determined by the equation:

δX = [(R_sample/ R_standard – 1] x 1000

where R_sample and R_standard represent the ¹³C/¹²C and ¹⁵N/¹⁴N ratios in the experimental and control (standards), respectively. The analytical precision of both δ¹⁵N and δ¹³C was < 0.06‰ based on three internal laboratory standards: Amaranth flour with δ¹⁵N and δ¹³C values of 2.55‰ and − 12.98‰; Bovine liver with δ¹⁵N and δ¹³C values of 7.61‰ and − 21.63‰; Keratin with δ¹⁵N and δ¹³C values of 4.74‰ and − 24.38‰. Lipid extractions and mathematical normalization were not performed as any of the C:N ratio values exceeded 3.5 (mean = 3.3) (Post et al., 2007).

Statistical analyses. Factorial PERMANOVA permutation-based multivariate variance analysis was used to investigate the diet changes among ontogenetic groups (three levels: juveniles, young adults, and adults, as a random factor), seasons (four levels: Summer, Autumn, Winter, and Spring, as a fixed factor) and their interaction effects. Then, post-hoc pairwise PERMANOVA tests were used to reveal possible differences among groups. A factorial PERMANOVA was applied to investigate possible diet differences between sex (two levels: female and male, as a fixed factor), ontogenetic groups, and their interactions. Non-metric multidimensional scaling (nMDS) ordination plots were used to illustrate the similarity and potential overlap of the groups (ontogenetic groups and seasons) with the factor (prey items weight). The PERMANOVA and nMDS were based on Bray-Curtis similarity matrices built with the square root of prey masses. The prey mass data was chosen because we believe it better reflects the energy consumed by the predator and also because it has been used in most studies on trophic relationships (Baker et al., 2014). For stomach content analysis (SCA), preys were categorized into six groups based on taxon and habitat use: Pelagic crustaceans, Benthic crustaceans, Demersal fishes, Pelagic fishes, Non-identified fishes, and Demerso-pelagic cephalopods. All PERMANOVA tests were based on 9,999 permutations, and p-values < 0.05 were considered significant. To estimate the niche breadth, the standardized Levins’ index based on prey masses was used (Levins, 1968; Hulbert, 1978). Levins’ index was calculated using the package spaa (Zhang, Ma, 2014). The standardization was carried out based on the formula: B_std=B-1/n-1, where B is the calculated Levins’ index and n is the number of ingested prey items.

To further evaluate possible ontogenetic shifts for P. brasiliensis, linear regression was carried out on δ¹³C and δ¹⁵N values versus TL, then the normality of the residuals was tested. The isotopic niche size and overlap of each ontogenetic group were estimated from δ¹⁵N and δ¹³C values using the standard ellipse area (95%) corrected for small samples (SEAc) using package SIBER (Jackson et al., 2011; Syväranta et al., 2013). The statistical procedures with stomach content and stable isotope data were run in PRIMER v. 7 (Anderson, 2001; Anderson et al., 2008) and R 3.3.2 (R Development Core Team, 2021).

Results​

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Sea surface temperature (SST) data recorded by the data logger confirmed the presence of upwelling events throughout the sampling period (Fig. S1). The events occurred with greater intensity mainly in February, September and October with average temperatures close to 16°C.

Diet description. The non-empty stomachs corresponded to 49% (n = 496) of the total specimens collected and dissected (n = 1016) (Tab. 1). Percophis brasiliensis’ diet was composed of 37 prey taxa, of which 27 were identified at the species level (Tab. 2). Teleostei was the most consumed prey group in %W for all ontogenetic groups, mainly composed of small pelagic fishes (Clupeiformes). The juveniles showed a higher percentage of Teleostei prey, 79.7%W, mainly composed by Engraulidae. For juveniles, crustaceans (mostly shrimps) and Cephalopoda (squids) represented 20.3%W of the prey. The importance of Teleostei is similar between young adults and adults (54.6 and 53.9%W, respectively), with an increase in crustaceans (27.0 and 15.5%W) and cephalopods (17.5 and 29.6%W).

TABLE 1 | The total number of stomachs and the percentage of non-empty stomachs (in parentheses) of each ontogenetic group by season of Brazilian flathead Percophis brasiliensis.

Ontogenetic groups / Seasons	Summer	Autumn	Winter	Spring
Juveniles	86 (38.4)	68 (54.4)	74 (33.8)	56 (51.8)
Young adults	94 (44.7)	113 (49.56)	100 (43.0)	109 (49.5)
Adults	75 (37.3)	105 (53.3)	93 (52.2)	62 (74.2)

TABLE 2 | Diet compositionof ontogenetic groups of Brazilian flathead Percophis brasiliensis. SL = Average standard length (mm), and TW = Average weight of predators (g), %N = Percentage in number, %W = Percentage in weight, %F = Frequency of occurrence. NI = Not identified.

Prey Items	Juveniles n = 124, SL = 292, TW = 137			Young adults n = 195, SL = 353, TW = 265			Adults n = 177, SL = 437, TW = 520
	%W	%F	%N	%W	%F	%N	%W	%F	%N
Pelagic prey	42.06	38.71	62.67	54.02	38.95	74.78	63.48	46.33	88.96
Crustaceans	6.85	4.84	44.45	15.64	10.26	69.04	11.67	11.3	84.9
Peisos petrunkevitchi Burkenroad, 1945	6.57	3.23	43.83	15.64	10.26	69.04	10.89	10.17	79.83
Sergestidae NI	0.28	1.61	0.62	0	0	0	0.78	1.13	5.07
Fishes	27.8	25.8	15.13	20.9	18.97	4.16	22.24	18.06	2.28
Anchoa sp.	1.34	1.61	0.62	1.45	2.05	0.26	0.06	0.56	0.05
Anchovia clupeoides (Swainson, 1839)	0	0	0	0.29	0.51	0.07	0	0	0
Carangidae NI	0	0	0	0.65	0.51	0.07	1.1	1.13	0.09
Chirocentrodon bleekerianus (Poey, 1867)	1.71	1.61	0.62	8.54	4.62	0.72	0.58	1.13	0.09
Clupeidae NI	0	0	0	0	0	0	1.39	0.56	0.05
Clupeiformes NI	7.54	4.84	3.09	0.6	0.51	0.07	2.76	2.82	0.23
Engraulidae NI	17.21	17.74	10.8	8.5	9.23	2.64	1.87	6.78	1.23
Engraulis anchoita Hubbs & Marini, 1935	0	0	0	0.59	1.03	0.26	0.11	1.13	0.09
Harengula clupeola (Cuvier, 1829)	0	0	0	0	0	0	5.29	0.56	0.09
Lycengraulis grossidens (Spix & Agassiz, 1829)	0	0	0	0.28	0.51	0.07	0	0	0
Sardinella aurita Valenciennes, 1847	0	0	0	0	0	0	7.5	2.26	0.27
Trachurus lathami Nichols, 1920	0	0	0	0	0	0	1.58	1.13	0.09
Cephalopoda	7.41	7.26	3.09	17.49	11.28	1.58	29.57	20.33	1.78
Doryteuthis pleii (Blainville, 1823)	0.26	1.61	0.93	15.22	4.62	0.66	24.27	14.12	1.14
Doryteuthis sp.	6.85	2.42	0.93	1.33	2.05	0.26	3.94	2.82	0.23
Lolliguncula brevis (Blainville, 1823)	0	0	0	0.39	3.08	0.46	0.1	1.13	0.09
Teuthida NI	0.3	3.23	1.23	0.54	1.54	0.2	1.26	2.26	0.32
Benthic/Demersal prey	16.81	27.45	14.22	31.19	37.97	18.06	24.15	53.59	7.47
Crustaceans	6.07	16.13	7.41	11.36	19.99	9.03	3.82	17.49	4.12
Artemesia longinaris Bate, 1888	0	0	0	0.35	1.54	0.2	0.32	1.69	0.37
Brachyura NI	0	0	0	0.01	0.51	0.07	0	0	0
Dendrobranchiata NI	2.93	10.48	4.94	2.22	5.64	7.18	0.73	4.52	2.78
Farfantepenaeus sp.	0	0	0	1.15	1.03	0.13	1.19	1.13	0.09
Hemisquilla braziliensis (Moreira, 1903)	2.23	1.61	0.62	3.27	5.64	0.72	0.64	3.39	0.32
Hemisquillidae NI	0.55	3.23	1.23	0.4	2.56	0.33	0.37	3.95	0.32
Isopoda NI	0	0	0	0.05	0.51	0.07	0.01	0.56	0.05
Pleoticus muelleri (Bate, 1888)	0	0	0	3.68	2.05	0.26	0.32	1.13	0.09
Portunus spinicarpus (Stimpson, 1871)	0	0	0	0.23	0.51	0.07	0.18	0.56	0.05
Sicyonia sp.	0	0	0	0	0	0	0.06	0.56	0.05
Sicyonia dorsalis Kingsley, 1878	0.36	0.81	0.62	0	0	0	0	0	0
Fishes	10.74	11.32	6.81	19.73	17.47	8.96	20.31	35.54	3.3
Anguilliformes NI	0	0	0	0.86	1.03	0.13	1.02	1.69	0.14
Ctenosciaena gracilicirrhus (Metzelaar, 1919)	0.91	1.61	0.62	1.2	2.05	0.26	1.35	2.26	0.23
Cynoscion guatucupa (Cuvier, 1830)	0.14	0.81	0.31	0	0	0	0.02	0.56	0.05
Cynoscion jamaicensis (Vaillant & Bocourt, 1883)	1.43	0.81	0.31	0.45	1.54	0.2	0.88	1.69	0.18
Cynoscion sp.	2.48	2.42	1.23	0.98	2.05	0.26	0.15	1.13	0.09
Dactylopterus volitans (Linnaeus, 1758)	0	0	0	0	0	0	1.6	1.69	0.18
Dules auriga Cuvier, 1829	1.7	0.81	0.62	5.61	3.08	0.4	2.03	3.39	0.32
Etropus longimanus Norman, 1933	0	0	0	1.57	3.08	0.4	0.8	4.52	0.41
Isopisthus parvipinnis (Cuvier, 1830)	0	0	0	0	0	0	0.21	0.56	0.05
Ophichthus gomesii (Castelnau, 1855)	0	0	0	0.45	0.51	0.07	0	0	0
Paralonchurus brasiliensis (Steindachner, 1875)	0.07	0.81	0.93	0.86	2.05	0.46	1.65	1.69	0.27
Pleuronectiformes NI	0	0	0	0	0	0	0.22	0.56	0.05
Porichthys porosissimus (Cuvier, 1829)	1.1	0.81	0.31	1.76	1.03	5.93	0.98	2.26	0.18
Prionotus punctatus (Bloch, 1793)	0	0	0	0	0	0	0	0.56	0.05
Prionotus sp.	1.13	0.81	0.93	0.49	0.51	0.13	1.01	1.69	0.14
Raneya brasiliensis (Kaup, 1856)	0.09	0.81	0.31	4.86	0.03	0.46	6.33	9.04	0.77
Saurida sp.	0.43	0.81	0.62	0.4	0.51	0.13	0	0	0
Sciaenidae NI	0	0	0	0.24	0	0.13	0.45	0.56	0.05
Stellifer sp.	1.26	0.81	0.62	0	0	0	0	0	0
Symphurus sp.	0	0	0	0	0	0	1.61	1.69	0.14
Gastropoda	0	0	0	0.05	0.51	0.07	0.02	0.56	0.05
Philine sp.	0	0	0	0.05	0.51	0.07	0.02	0.56	0.05
Fishes NI	41.13	49.19	22.84	14.92	40	6.65	12.27	35.59	3.29
Total	325.13 g		n = 323	1112.73 g		n = 1510	2585.24 g		n = 2185

We found significant differences among ontogenetic groups, seasons, and the interaction between these factors (PERMANOVA; p ≤ 0.03) (Tab. 3). Dietary ontogenetic shifts have been detected but these changes vary according to the season. During Autumn and Winter, juveniles differed from young adults and adults (pairwise PERMANOVA; p ≤ 0.02). Only adults showed differences from the other two ontogenetic groups in the Summer (p ≤ 0.04). Juveniles and adults are different during Spring (p = 0.004), but we found no differences between juveniles and young adults, and young adults and adults (p = 0.10 and p = 0.49, respectively). Females (n = 348, 433.1 mm ± 69.2) were larger than males (n = 144, 365.2 mm ± 40.5; PERMANOVA, p = 0.001). However, no differences in diet were observed between males and females (Pseudo-F = 1.36, p = 0.33).

TABLE 3 | PERMANOVA results of the main effects between the factors ontogenetic groups and seasons of Brazilian flathead Percophis brasiliensis, estimated from Bray-Curtis similarity matrix based on %W. Significantly differences (p < 0.05) are presented in bold.

Source	df	MS	Pseudo-F	P(perm)	Perm. (n)
Ontogenetic groups	2	16716	2.832	0.0288	9940
Season	3	19204	3.2602	0.0085	9941
Ontogenetic groups vs. Season	6	5946	1.5593	0.0176	9864
Residual	481	3813.3
Total	492

In juveniles, there was no significant differences in the diet throughout the year (p≥ 0.081), while young adults’ diet differed among all seasons (p< 0.01), except between winter and summer (p= 0.57) when similar %W of demersal fishes and non-identified fish were ingested (Fig. 2). During the autumn, P. brasiliensis fed on the small pelagic shrimp Peisos petrunkevitchi Burkenroad, 1945, while in the spring demersal-pelagic cephalopods were the main prey group. The diet of adults during autumn was significantly different from all other seasons (p< 0.01). Adults and young adults consumed a high proportion (%W) of P. petrunkevitchi during the autumn (Figs. 2–3). Besides, during the autumn, the ingested prey number was four to 29 times higher than in other seasons for juveniles and adults (Tab. S2). Despite the increase in prey number intake mainly between March and April, this pattern is not reflected in the %BW values (Fig. S3). In all other seasons, larger fish have a more diverse diet (Tab. S2).

FIGURE 2| Seasonal variation in dietary composition (%W) for each ontogenetic group of Brazilian flathead Percophis brasiliensis. Seasons: Summer, Sum; Autumn, Aut; Winter, Win; Spring, Spr. Ontogenetic groups: Juvenile, Ju; Young adults, Ya; Adults, Ad.

FIGURE 3| nMDS ordination plot of the Bray-Curtis similarity matrix based on the %W of prey groups of Brazilian flathead Percophis brasiliensis. Juveniles = white, young adults = gray, adults = black. Summer = triangle, Autumn = circle, Winter = square, Spring = inverted triangle. The main prey categories are represented by Spearman’s correlation vectors. The length of each vector provides the strength of the correlation coefficient, where the radius of the circle represents the maximum correlation (=1). Prey categories: PelCru = pelagic crustaceans, BenCru = benthic crustaceans, DemFish = demersal fishes, FisNI = non-identified fishes, and PelSqu = pelagic squids. Dotted lines represent the Bray-Curtis similarity of 68%.

Niche breadth of young adults and adults was smaller during Autumn, probably due to the large ingestion of a single species (Tab. S2). For juveniles, the lowest calculated niche breadth was observed in Spring. In general, the niche breadth slightly decreases with growth, with mean values of standardized Levins’ index = 0.29, 0.27, and 0.26 in juveniles, young adults, and adults, respectively (Tab. S2).

Stable Isotope Analysis. Percophis brasiliensis δ¹³C values ranged between -18.36 and -16.77 ‰, with a mean of -17.58 ± 0.26 ‰, while δ¹⁵N ranged between 11.91 and 14.29 ‰, with a mean of 13.52 ± 0.41 ‰ (Tab. 4). Significant relationships were observed between δ¹³C (r² = 0.092, p = 0.030) and δ¹⁵N (r² = 0.645, p < 0.001) versus total length (Fig. 4).

TABLE 4 | Sample size (n), mean and standard deviation (SD) of the stable isotope values (δ¹⁵N and δ¹³C) of Brazilian flathead Percophis brasiliensis.

Ontogenetic groups	n	δ15N ± SD	δ13C ± SD
Juveniles	13	13.0±0.5	-17.8±0.4
Young adults	11	13.6±0.3	-17.5±0.4
Adults	17	13.9±0.3	-17.4±0.3

FIGURE 4| Relationships between total length (mm TL) versus δ¹⁵N values (‰; above) and total length versus δ¹³C values (‰; below) for Brazilian flathead Percophis brasiliensis. Juveniles (white circles), young adults (gray circles) and adults (black circles).

Based on the measured standard ellipse corrected for small sample size (SEAc), the isotopic niche width decreases with the increase in fish size. Juveniles showed the broader niche (0.37), followed by young adults (0.34) and adults (0.28). The overlap area between juveniles and young adults was 37%, between young adults and adults was 53%, and between juveniles and adults was 28% (Fig. 5).

FIGURE 5| Isotopic niche width and overlap of Brazilian flathead Percophis brasiliensis.ßß

Discussion​

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Coastal upwellings are important oceanographic processes that can induce several changes in trophic interactions in marine ecosystems. The studied area is influenced by coastal upwellings which are more intense in two periods of the year, reportedly summer/autumn and spring (Valentin et al., 1987; Castelao, Barth, 2006). The first coastal upwellings event occurred in late summer to early autumn and the second in late winter to early spring. In the current study, we identified changes in the demersal predator’s diet, the Brazilian flathead P. brasiliensis, during the two recorded upwelling events.

In the summer, P. brasiliensis was more connected to the benthic trophic pathways since half of the diet of young adults and adults were composed of benthic prey (Fig. 2). The benthic pathway depends largely on the sinking of particulate organic matter being ingested by benthic detritivore organisms, which in turn are prey to benthic and demersal fish (secondary consumers), which are then preyed upon by the studied predator (tertiary consumer) (Mann, 1988; Gooday, Turley, 1990). In the late summer (February), intense coastal upwellings occurred. In the following autumn months (March and April), the pelagic shrimp P. petrunkevitchi was the main prey species consumed by both young adults and adults, completely altering the diet and the trophic coupling pathways from benthic to pelagic environment. A study conducted by Simões et al. (2013) in a vicinity area showed that P. petrunkevitchi has a rapid density increase due to the fertilization effects of SACW upwelling. In our study, P. petrunkevitchi was also responsible for a large increase in the ingested prey number found in March and April, probably due to coastal upwellings that occurred in late summer.

The second upwelling event occurred in the late winter to the early spring, probably inducing changes in the predator’s diet. Percophis brasiliensis used mainly the pelagic trophic pathway, preying on small squids and pelagic fish. Pelagic squids represented a large part of the diet (20–45%W) of P. brasiliensis adults throughout the year, young adults (in winter and spring), and juveniles (in summer). The most consumed squid, Doryteuthis plei (Blainville, 1823),inhabits coastal waters and has a short life cycle and very fast growth (five months lifespan, Jackson, Forsythe, 2002). Spawning populations of D. plei were observed during winter, spring, and summer (Rodrigues, Gasalla, 2008), being more abundant during spring-summer in the region (Costa, Fernandes, 1993). During spring–summer, adult D. plei aggregate in shallower waters for spawning, showing increasing feeding activity and taking advantage of the greater prey availability provided by upwellings (Rodrigues, Gasalla, 2008; Gasalla et al., 2010). Seasonal increases in prey availability and consumption provided by intense coastal upwellings, as observed here, may have a positive effect on the physiological condition of fish of different trophic levels (Rosa et al., 2010; Pulgar et al., 2013). These positive effects include improved fitness and reproductive capacity, with direct implications for stock management and conservation (Stevenson, Woods, 2006; Rosa et al., 2010).

Despite being a bottom dweller, P. brasiliensis probably performs short vertical migrations in the water column to capture small pelagic fishes (e.g., Anchoa sp. and Chirocentrodon bleekerianus (Poey, 1867)), squids (Doryteuthis sp.), and shrimps (P. petrunkevitchi). Such foraging behavior may contribute to the benthic-pelagic coupling that links the nutrients and energy produced by planktonic organisms (pelagic pathway), and the energy and nutrients derived from benthic production and detrital recycling (benthic pathway) (Marcus, Boera, 1998; Woodland, Secor, 2013; Van Denderen et al., 2018). The pelagic organisms that sink to the bottom due to bycatch must also be considered because there are small to medium-scale fisheries operating in the study area. Understanding the benthic-pelagic coupling processes is important because it affects the benthic/demersal species diversity, productivity, stability (Townsend, Cammen, 1988; Moodley et al., 1998; Gray, 2002) and the marine ecosystem functioning in general (Griffiths et al., 2017). The benthic-pelagic coupling is regulated by different factors such as water column deep, physical mixing, primary production, community composition, and organism life cycles (Marcus, Boera, 1998). Consumers that can use both pelagic and benthic resources, such as P. brasiliensis, have the potential to generate food web stability (Rooney et al., 2006; Van Denderen et al., 2018).

The assessment of the source of organisms’ food has implications for a better understanding of marine food webs. Most of the benthic and/or demersal organisms depend directly or indirectly on the input of organic matter, mainly in the form of debris, which is linked to the productivity of the superficial layers (Mann, 1988; Gooday, Turley, 1990). By feeding directly on pelagic organisms, the population dynamics of these demersal species are linked to the rapid fluctuations in energy pulses provided by oceanographic processes, and to possible changes caused by climatic changes. The sampling period of the current study was characterized by weak La Niña anomalies (NOAA, 2021). El Niño/La Niña-Southern Oscillation anomalies are known to change local climate and precipitation, sea surface temperature, and to intensify or weaken upwellings (Colberg et al., 2004; Middleton et al., 2007; Jacox et al., 2015). Thus, interannual anomalies, as well as global climate changes, have great potential to change the trophic role of species and the dynamics of bento-pelagic coupling.

The stomach content analysis revealed P. brasiliensis as a generalist predator with a broad prey spectrum. With a total of 27 taxa identified at the species level, the species number observed is 56% higher than previously recorded (n = 17) for this species in the Argentine-Uruguayan Coastal Ecosystem (34°S to 41°S; AUCE) based on 657 non-empty stomachs analyzed (Milessi, Mari, 2012). Also, in the AUCE, bony fishes were the most important prey group for P. brasiliensis (%W = 93.1), feeding mainly on the small pelagic fishes Trachurus lathami Nichols, 1920 (%W=58.0) and Engraulis anchoita Hubbs & Marini, 1935 (%W = 24.4%). In the present study, bony fishes were less consumed by P. brasiliensis (%W = 53.9–79.7), depending on the ontogenetic groups.

Ontogenetic diet shifts were detected by both SCA and SIA. A factor that can help to understand such feeding pattern is that juveniles and young adults are commonly found in shallow waters with high temperatures and low salinities, while the larger individuals move to deeper regions in the continental shelf with higher salinity and lower temperatures (Barretto, 2007; Rodrigues et al., 2013). Such changes in habitat use may expose juveniles and adults to different prey availability. Pelagic prey is more important for juveniles, throughout the year they feed mostly on engraulids. Engraulids are often associated with the coastal ecosystem, such as sand beaches, bays, and estuaries (Araújo et al., 2008). Although fish highly contributes to the diet of P. brasiliensis, squids and crustaceans increase their importance from juveniles to adults. The increase of squids (e.g., D. plei) and crustaceans (e.g., P. petrunkevitchi, Artemesia longinaris Bate, 1888, and Pleoticus muelleri (Bate, 1888)) abundances in the studied area are strongly related to the upwellings of cold SACW (Costa, Fernandes, 1993; Simões et al., 2013; Silva et al., 2014; Costa et al., 2017).

As P. brasiliensis grows, there is a significant increase in δ¹⁵N and δ¹³C values, with a decrease in isotopic niche width. The observed variation of δ¹⁵N and δ¹³C values in relation to P. brasiliensis size may be related to the changes in the major components of its diet. Engraulids are small pelagic fishes, that occupy a relatively low trophic position, and feed primarily on zooplankton (Sergipense et al., 1999; Pizarro et al., 2019) that are δ¹⁵N and δ¹³C depleted, 8.4 ± 3.3 and -17.7 ± 0.3 respectively, in the study area (Gatts et al., 2021). This probably explains, at least in part, the lower δ¹⁵N and δ¹³C values observed in juveniles. Larger P. brasiliensis ingested greater amounts of small demersal fish (e.g., Dules auriga Cuvier, 1829) and squid (D. plei) that presented higher δ¹⁵N and δ¹³C values, with δ¹⁵N = 11.7 and δ¹³C = -16.6 and δ¹⁵N = 12.1 and δ¹³C = -16.9, respectively (Gatts et al., 2021). Changes in δ¹⁵N and/or δ¹³C values of demersal predator about size have been reported in the scientific literature, including with Argentine hake Merluccius hubbsi Marini, 1933 and Trichiurus lepturus Linnaeus, 1758 from the continental shelf of southeastern Brazil (Muto, Soares, 2011; Di Beneditto et al., 2013). The SIA data presented in this study are interesting as it corroborates, at least in part, the results of traditional SCA. However, these data must be interpreted with some caution due to limitations related to the number of samples (41 in total) and the sampling period (austral summer). New studies with a greater number of samples for SIA and temporal range could better elucidate the temporal trophic dynamics of the P. brasiliensis under coastal upwellings influence.

Our results showed shifts in the trophic pathways used by the demersal predator, altering the dynamics and the trophic role of the benthic-pelagic coupling. The changes in the P. brasiliensis’ diet are probably influenced by coastal upwelling events in a period characterized by weak La Niña anomalies. This oceanographic process provided fast increases in the availability of pelagic prey, such as small fish, shrimps and squids (Matsuura et al., 1992; Costa, Fernandes, 1993; Gasalla et al., 2010; Simões et al., 2013; Silva et al., 2014; Costa et al., 2017), altering the P. brasiliensis diet and the trophic coupling pathways from benthic to pelagic. By feeding directly on pelagic organisms, the population dynamics of this demersal species is connected with the rapid fluctuations in energy pulses provided by coastal upwellings events. Nonetheless, in this study, specimens were collected over one year, without annual replications. Upwelling ecosystems are strongly influenced by climate change (Bograd et al., 2023) and their temporal effects on the trophic dynamics of P. brasiliensis and other demersal predators are still poorly understood. Long-term studies are needed to better understand natural processes in upwelling ecosystems such as the intensity and frequency of upwelling as well as the biological responses to environmental changes. Furthermore, human interference, such as fishing and climate change, may influence ecological processes in upwelling ecosystems.

Acknowledgments​

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We are grateful to the Laboratório Integrado de Zoologia (LIZ – NUPEM/UFRJ) team for their support on laboratory procedures and analyzes. We also thank Ana Petry, Erica Caramaschi, Tommaso Giarrizzo, and Ryan Andrades for their valuable comments and suggestions, and Carlos Eduardo L. Ferreira and the project Pesquisa Ecológica de Longa Duração da Ressurgência de Cabo Frio for the sea surface temperature data. This work was supported by “Projeto Multipesca”, which is an environmental offset measure established through a Consent Decree/Conduct Adjustment Agreement between PetroRio and the Ministério do Meio Ambiente do Brasil, with the Fundo Brasileiro para a Biodoversidade – FUNBIO as an implementer. ABB received a Ph.D. grant from “Projeto Multipesca”, through the same funding source, and a postdoctoral fellowship (E-26/204.454/2021; E-26/204.455/2021) from FAPERJ.

References​

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Authors

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Arthur de Barros Bauer¹ and Luciano Gomes Fischer¹

^[1]    Instituto de Biodiversidade e Sustentabilidade (NUPEM), Programa de Pós-Graduação em Ciências Ambientais e Conservação, Universidade Federal do Rio de Janeiro, Av. São José do Barreto, 764, São José do Barreto, 27965-045 Macaé, RJ, Brazil. (ABB) arthurbauer.rj@gmail.com (corresponding author), (LGF) luciano.fischer@gmail.com.

Authors’ Contribution

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Arthur de Barros Bauer: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Resources, Visualization, Writing-original draft.

Luciano Gomes Fischer: Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Project administration, Resources, Supervision, Writing-review and editing.

Ethical Statement​

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The collection and transport of specimens were authorized by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio License N° 44025).

Competing Interests

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The author declares no competing interests.

How to cite this article

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Bauer AB, Fischer LG. Trophic ecology of the demersal predator Brazilian flathead Percophis brasiliensis (Percophidae) in a coastal upwelling ecosystem, SW Atlantic. Neotrop Ichthyol. 2024; 22(2):e230115. https://doi.org/10.1590/1982-0224-2023-0115

Copyright​

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This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Distributed under

Creative Commons CC-BY 4.0

© 2024 The Authors.

Diversity and Distributions Published by SBI

Accepted March 22, 2024 by Fernando Gibran

Submitted October 17, 2023

Epub July 8, 2024