Print
Feeding habits of the spotted rose snapper, Lutjanus guttatus, (Actinopterygii, Perciformes, Lutjanidae), in the central Gulf of California, BCS, Mexico
expand article infoFilius L. Valle-Lopez, Xchel G. Moreno-Sánchez, Marina S. Irigoyen-Arredondo, Leonardo A. Abitia-Cárdenas, Emigdio Marín-Enríquez§, Jorge S. Ramírez-Pérez§
‡ Instituto Politécnico Nacional, La Paz, Mexico
§ Universidad Autónoma de Sinaloa, Mazatlán, Mexico
Open Access

Abstract

The spotted rose snapper, Lutjanus guttatus (Steindachner, 1869), is an important resource for the coastal fisheries of the Gulf of California, mainly due to its high commercial value. Despite this, there are no management measures for this species, owing in part to a lack of information on its basic biology and its trophic ecology in the area. In this context, the presently reported study had as objective to describe the feeding habits of L. guttatus through stomach content analyses, as well as to describe possible changes linked to sex, size, and season. Specimens were caught monthly from June 2016 to September 2017 with gillnets in Santa Rosalía, BCS, Mexico. The abundance, weight, and frequency of occurrence of each prey were assessed, and these parameters were integrated into the index of relative importance (%IRI) to determine the importance of each prey item in the L. guttatus diet. The Levin’s index was used to assess the trophic niche width of the species, the feeding strategy was evaluated using Costello’s graphic method and the trophic level was calculated. Finally, to establish whether there were significant differences in the diet by sex, size, or season a PERMANOVA test was used with a 95% confidence level. A total of 202 L. guttatus stomachs were analyzed, 191 of which contained food. A total of 26 prey items were identified. According to the %IRI, the most important prey were the teleost fishes Harengula thrissina (Jordan et Gilbert, 1882) (45.7%) and Sardinops sagax (Jenyns, 1842) (34.8%), the euphausiid Nyctiphanes simplex (13.4%), and the crustacean Penaeus spp. (5.6%). The PERMANOVA analysis resulted in significant differences between the analyzed categories; however, there were no significant differences in the interactions among the categories. According to Levin’s index, L. guttatus had a narrow trophic width, with changes in the main prey consumed by the different categories. According to our results, L. guttatus can be considered a benthopelagic opportunistic carnivorous predator with a narrow trophic niche, presenting mostly quantitative variations in its diet according to sex, size, and season. Its trophic plasticity allows it to take advantage of the most available and abundant food resources.

Keywords

Lutjanidae, diet, sardines, euphausiids, Gulf of California

Introduction

Studies on the food habits of fish are fundamental to understand the structure and functioning of marine ecosystems (Díaz-Ruiz et al. 2004; Freitas et al. 2015), as they allow us to understand ecological aspects of species such as trophic interactions, their role in the food chain, and the energy flow through ecosystems (Brown et al. 2012). They are also extremely important when establishing management plans for species that are exploited due to their economic importance (Rojas-Herrera et al. 2004; Moreno-Sánchez et al. 2016). Within the family Lutjanidae, commonly known as snappers, the genus Lutjanus is the most diverse, as it includes 73 of the 113 species recorded in the family; among these, nine species are distributed in the eastern Pacific (Froese and Pauly 2019).

Snappers are commercially important components of artisanal fisheries worldwide. They are appreciated as a high-quality food resource, they are in high demand by the population, and their commercial value is higher than that of other fish species (Rojas 1997; Rojas-Herrera and Chiappa-Carrara 2002). This is reflected in the global catch numbers; according to the FAO (2020) over the past two decades, an average of 217 000 tons of snapper was caught annually.

Within this family, the spotted rose snapper, Lutjanus guttatus (Steindachner, 1869), is distributed from the Gulf of California, through Mexican Pacific coasts, to Peru. This is a demersal species that inhabits coastal reefs to a maximum depth of 30 m. Sexes are separate and those fish reach the size at first sexual maturity at 30 cm (Sarabia-Méndez et al. 2010).

Lutjanus guttatus is an important resource for fisheries in the coastal area of the Gulf of California, where one of the main economic activities is coastal fishing. Approximately 136 tons are captured annually in the area, representing an economic value of 4 million MXN (~ 207 590 USD) (CONAPESCA 2014).

Various studies have reported on the feeding habits of this species, although the majority of studies have been performed in the southernmost portion of its distribution, corresponding to tropical regions. These studies have reported that L. guttatus is a benthic carnivorous predator that feeds mainly on fish and small crustaceans (Rojas-Herrera and Chiappa-Carrara 2002; Rojas-Herrera et al. 2004; Tripp-Valdez and Arreguín-Sánchez 2009).

Previous studies have also shown latitudinal variations in the feeding habits of L. guttatus. The primary and secondary food items were, respectively, crustaceans and fishes at El Salvador (Rojas-Herrera et al. 2004), whereas they were, respectively, small-sized fish (Engraulidae and Clupeidae) and crustaceans, off the Guerrero coast, Mexico (Rojas-Herrera and Chiappa-Carrara 2002). Moreover, both crustaceans (Xanthidae) and fishes (Engraulidae) were the main prey items in the southern Gulf of California, Mexico (Tripp-Valdez and Arreguín-Sánchez 2009).

These data have led scientists to infer that the composition of the diet in L. guttatus depends mainly on variations in food availability, more than on resource selection by the predator (Rojas-Herrera and Chiappa-Carrara 2002). Moreover, the previously mentioned studies showed that there were changes in the diet of L. guttatus according to intraspecific variations such as size, and that sex and season did not lead to significant differences in diet (Rojas-Herrera and Chiappa-Carrara 2002). It should be noted that L. guttatus plays a role as predator and as prey and that this species is considered important in recirculation and energy transfers from the epifauna and infauna to upper trophic levels (Rojas 2006; Navia et al. 2016).

Despite its economic and ecological importance, there are no studies on the feeding habits of L. guttatus in the subtropical portion of its distribution area. The objective of the presently reported study was to evaluate the trophic spectrum of L. guttatus in the central Gulf of California, analyzing variations in the diet by sex, size, and season, to generate information on its diet in the higher latitudes of its distribution and identify possible variations compared with lower latitudes.

Materials and methods

Sample collection, processing, and data analysis

Monthly sampling was undertaken from June 2016 to September 2017 in the mining town of Santa Rosalía, Baja California Sur, in the central Gulf of California (Fig. 1). Specimens were obtained from the coastal fishery, which employs 300-m long gillnets with 102 mm mesh size; nets are left approximately 10 h in the water, from sunset to sunrise. Specimens were frozen and transported to the Ecology Laboratory of the Interdisciplinary Centre of Marine Sciences of the National Polytechnic Institute (Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional, CICIMAR-IPN). The total length (Lt, cm) and weight (W, g) of each organism were recorded. Sex was identified through the direct observation of the gonads and confirmed through histological analyses following methods proposed by Arellano-Martínez et al. (2001). Because captured individuals were at or above the size at first maturity (i.e., 30 cm) (Sarabia-Méndez et al. 2010), the specimens were categorized into three groups following Sturges’ rule (Daniel 1997) (group 1 = 28–38 cm, group 2 = 39–48 cm, and group 3 = 49–58 cm).

Figure 1. 

Map of the study area, Santa Rosalía, BCS, central Gulf of California.

To identify the seasonal variation in sea surface temperature, the monthly and annual mean values of sea surface temperature were calculated based on MODIS-AQUA satellite images with 1.1 km resolution. Temperature data were obtained from the ERDDAP portal of the National Oceanic and Atmospheric Administration (NOAA). The general mean value of the time series was calculated and was used to define the seasons: cold-season months were below the surface temperature mean value (November–May) and warm-season months were above the surface temperature mean value (June–October) (Fig. 2).

Figure 2. 

Monthly surface sea temperature (SST) records (black line) in the central Gulf of California during the sampling period. The dotted line indicates the general mean value of the time series. The gray bars indicate the warm months (months with SST above the mean value) and the black bars indicate the cold months (months with SST below the mean value). The primary y axis shows surface sea temperature values in degrees Celsius and the secondary y axis shows anomalies with respect to the general mean value of the time series during the sampled period.

Prey items were identified to the lowest possible taxonomic level using specialized identification keys. For fish, the keys by Whitehead (1985), Fischer et al. (1995), and Lowry (2011) were used. For crustaceans, the key by Morris et al. (1980) was used, and for other invertebrates, the keys by Iverson and Pinkas (1971), Brusca (1980), and Keen (2012) were used. For the trophic analysis of L. guttatus, specimens were categorized according to sex (male or female), size (group 1 = 28–38 cm, group 2 = 39–48 cm, and group 3 = 49–58 cm), and season (cold or warm).

Feeding habits

A species accumulation curve was graphed to assess whether the number of stomachs containing food was adequate to represent the diet of L. guttatus. The curve was created using the program EstimateS Swins820 (Colwell 2009), using the numerical abundance of each prey item and Shannon–Wiener’s diversity index (H′) for each stomach. The coefficient of variation (CV) was calculated to assess the number of stomachs necessary to adequately represent the diet in general and by category (sex, size, and season). If the CV took on values equal to or below 5% (0.05), the number of stomachs was deemed sufficient to adequately represent the diet (Jiménez-Valverde and Hortal 2003; Moreno-Sánchez et al. 2019).

The quantitative importance of each prey item in the L. guttatus diet was described using the numerical (%N), gravimetric (%W), and frequency of occurrence (%FO) indices (Hyslop 1980). These indices were then integrated into the index of relative importance (IRI) proposed by Pinkas et al. (1971):

IRI = (%N + %W) ∙ %FO

To contrast the results of the presently reported study with those found in previous studies, results are presented as a percentage (Cortés 1997):

% IRI i=100IRIii-1nIRII

Levin’s standardized index (Bi) was used (Krebs 1989) to assess the trophic width of L. guttatus. Values close to zero indicate that the species present a specialist feeding strategy, whereas values close to one indicate that the species has a generalist strategy (Labropoulou and Eleftheriou 1997):

Bi=1n-11jPij2-1

Where Bi is the niche width, ∑j P2ij is the proportion of the jth item in the diet of the ith predator, and n is the total number of prey items.

Data analysis

To interpret the feeding strategy of L. guttatus in the study area, we created a dispersion diagram based on Costello´s graphic method (1990), modified by Amundsen et al. (1996). According to the authors, four strategies can be distinguished: 1) specialized on different trophic resources, (2) more generalist with little individual variation in trophic width, (3) specialist with one prey type, but occasional consumption of other species, and (4) mixed strategy where there are individuals with a specialized diet and other individuals with a more generalist diet. This technique was used complementarily to corroborate the trophic width niche of L. guttatus.

A permutational multivariate analysis of variance (PERMANOVA) with 1000 permutations was undertaken to evaluate possible differences in the L. guttatus diet with respect to sex (male or female), size (group 1 = 28–38 cm, group 2 = 39–48 cm, and group 3 = 49–58 cm), or season (warm or cold), and possible interactions between categories. For this analysis, a numerical matrix was constructed where columns were the prey species and rows were the analyzed stomachs. A Bray–Curtis dissimilarity matrix was used as a similarity measure for the PERMANOVA. This analysis was performed using the Adonis function in the Vegan 2.2-1 library (Oksanen et al. 2015) in the R platform version 3.0.1 (R Core Team 2016), with a 95% confidence interval.

The L. guttatus trophic level was calculated using the formula proposed by Cortés (1999). This equation took into account the type of prey found in stomach contents:

TL=1+j=1nPj·TLj

Where TL = trophic level of L. guttatus, TLj = trophic level of each prey category consumed, Pj = proportion of each prey category in the diet of the predator, and n = number of prey items.

The trophic levels of prey were obtained from FishBase (Froese and Pauly 2019) and the Sea Around Us Project DataBase (Pauly et al. 2020).

Results

A total of 202 L. guttatus specimens were caught, ranging in size from 28 to 55 cm Lt and weighing from 290 to 1675 g. A total of 191 specimens (94.5%) had stomachs containing food and 11 (5.5%) were empty. The prey species accumulation curve reached an asymptote at 109 stomachs, which indicated that the number of analyzed stomachs was sufficient to characterize the diet (CV ≤0.05). The minimum sample size was also achieved for the categories of sex, size, and season (Table 1).

Table 1.

Minimum sample size for Lutjanus guttatus for all samples, by sex, size, and season.

Category Ns Nsm CV
General 191 109 0.05
Female 125 82 0.05
Male 66 61 0.05
Group 1 94 79 0.05
Group 2 79 54 0.05
Group 3 18 16 0.05
Cold season 141 110 0.05
Warm season 50 43 0.05

General diet

The trophic spectrum of L. guttatus comprised 26 categories of prey items; it included 15 fish species, 11 invertebrate species, and fish remains. A total of 502 prey items were counted; the most abundant were invertebrates (65%, n = 327), mainly the euphausiid Nyctiphanes simplex (43.6%, n = 219) and the shrimp Penaeus spp. (16.9%, n = 85), as well as fish (35%, n = 175), mainly the sardines Sardinops sagax (Jenyns, 1842) (16.3%, n = 82) and Harengula thrissina (Jordan et Gilbert, 1882) (15.1%, n = 76).

The total biomass of stomach contents was 978 g, most of which corresponded to fishes (94.2%, 921.3 g), mainly H. thrissina (49.7%, 486.8 g) and S. sagax (29.8%, 291.5 g), and invertebrates (5.8%, 56.7 g), mainly Penaeus spp. (2.8%, 27.7 g) and N. simplex (1.8%, 18 g).

The most frequent prey items were the fishes S. sagax (38.7%, n = 82) and H. thrissina (36.1%, n = 76), the euphausiid N. simplex (15.1%, n = 219), and the crustacean Penaeus spp. (14.6%, n = 85). According to the %IRI the most important prey species were the fishes H. thrissina (45.7%) and S. sagax (34.8%), the euphausiid N. simplex (13.4%), and the shrimp Penaeus spp. (5.6%) (Table 2, Fig. 3).

Table 2.

General diet of Lutjanus guttatus in the central Gulf of California, Mexico.

Tx Prey N W FO %N %W %FO IRI %IRI TL
Mo Chione spp. 1 0.5 1 0.20 0.05 0.52 0.13 0.003 2.00
Loligo spp. 1 0.5 1 0.20 0.05 0.52 0.13 0.003 3.05
Parvanachis spp. 1 0.5 1 0.20 0.05 0.52 0.13 0.003 2.10
Cr Poecilostomatoida 4 1 2 0.80 0.10 1.05 0.94 0.018 2.00
Penaeus spp. 85 27.7 28 16.93 2.83 14.66 289.74 5.651 2.70
Callinectes spp. 10 2.5 2 1.99 0.26 1.05 2.35 0.046 3.70
Sicyonia disedwardsi 1 0.5 1 0.20 0.05 0.52 0.13 0.003 2.40
Nyctiphanes simplex 219 18 29 43.63 1.84 15.18 690.32 13.464 2.25
Cymothoa exigua 1 0.5 1 0.20 0.05 0.52 0.13 0.003 3.18
Squilla spp. 2 4.5 2 0.40 0.46 1.05 0.90 0.018 2.40
Tu Salpidae 2 0.5 1 0.40 0.05 0.52 0.24 0.005 3.00
Ac Acanthurus spp. 1 0.5 1 0.20 0.05 0.52 0.13 0.003 2.00
Achirus spp. 1 38 1 0.20 3.89 0.52 2.14 0.042 3.00
Ophioblennius steindachneri 1 9 1 0.20 0.92 0.52 0.59 0.011 2.50
Harengula thrissina 76 486.8 69 15.14 49.78 36.13 2345.08 45.737 3.10
Opisthonema libertate 1 19 1 0.20 1.94 0.52 1.12 0.022 2.89
Sardinops sagax 82 291.5 74 16.33 29.81 38.74 1787.64 34.865 2.84
Engraulis mordax 1 12 1 0.20 1.23 0.52 0.75 0.015 2.96
Mugil curema 1 12 1 0.20 1.23 0.52 0.75 0.015 2.01
Benthosema panamense 1 0.5 1 0.20 0.05 0.52 0.13 0.003 3.00
Diaphus spp. 1 3 1 0.20 0.31 0.52 0.26 0.005 3.30
Triphoturus spp. 1 0.5 1 0.20 0.05 0.52 0.13 0.003 3.00
Ophichthus spp. 1 0.5 1 0.20 0.05 0.52 0.13 0.003 3.40
Sebastes spp. 2 0.5 1 0.40 0.05 0.52 0.24 0.005 3.50
Scomber japonicus 1 33 1 0.20 3.37 0.52 1.87 0.036 3.38
Scorpaenodes spp. 1 0.5 1 0.20 0.05 0.52 0.13 0.003 3.87
Fish remains 3 14 1 0.60 1.43 0.52 1.06 0.021
Total 502 978 191 100 100 5127.29 100
Figure 3. 

General trophic spectrum of Lutjanus guttatus in the central Gulf of California, measured with the index of relative importance (%IRI). %W = Prey-specific weight, %N = Prey-specific abundance, %FO = frequency of occurrence, Ss = Sardinops sagax, Ha = Harengula thrissina, Ns = Nyctiphanes simplex, Pe = Penaeus, Opi = Other prey items.

Diet by sex

Of 191 analyzed stomachs containing food, 66 were from males and 125 were from females. There were 10 prey items in male stomachs (5 fishes and 5 invertebrates), and the most important prey according to the %IRI were the fishes S. sagax (64.6%) and H. thrissina (15.4%), and the crustaceans N. simplex (15.2%) and Penaeus spp. (3.7%). There were 19 prey items in female stomachs (12 fishes and 7 invertebrates); the most important prey items were H. thrissina (56.8%), S. sagax (24.7%), N. simplex (11.7%), and Penaeus spp. (6.1%) (Fig. 4). The PERMANOVA showed significant differences in the diet between the two sexes (F = 2.472, P < 0.05) (Table 3).

Figure 4. 

Inter-sexual variation (male or female) in prey items consumed by Lutjanus guttatus in the central Gulf of California, measured with the index of relative importance (%IRI).

Table 3.

Results of the PERMANOVA (Permutational multivariate analysis of variance) analysis of the Lutjanus guttatus diet between sexes (male and female), sizes (G1, G2, and G3), and seasons (warm and cold) in the central Gulf of California, Mexico.

Factor F r P (>F) Significance
Sex 2.472 0.005 0.022 Yes
Size 45.440 0.101 0.002 Yes
Season 5.054 0.011 0.002 Yes
Sex:Size 1.223 0.003 0.248 No
Sex:Season 0.628 0.001 0.767 No
Size:Season 1.585 0.004 0.120 No
Sex:Size:Season 0.605 0.001 0.799 No

Diet by size

A total of 94 stomachs belonging to group 1 (28–38 cm Lt) were analyzed; 14 prey items were found in these stomachs (8 fishes and 6 invertebrates). According to the %IRI, the most important prey in this group were the fishes S. sagax (42.7%) and H. thrissina (29.5%), the euphausiid N. simplex (23.4%), and the shrimp Penaeus spp. (3.9%). A total of 79 stomachs belonging to group 2 (39–48 cm Lt) were analyzed; 15 prey items were found in these stomachs (8 fishes and 7 invertebrates). The most important prey were H. thrissina (65.3%), S. sagax (21.7%), Penaeus spp. (7.9%), and N. simplex (4.2%). A total of 18 stomachs belonging to group 3 (49–58 cm Lt) were analyzed; 7 prey items were found in these stomachs (5 fishes and 2 invertebrates). The most important prey items were the fishes S. sagax (46.8%) and H. thrissina (44.4%), and the shrimp Penaeus spp. (3.2%) (Fig. 5). The PERMANOVA test showed significant differences in the diet between the three size groups (F = 45.4, P < 0.05) (Table 3).

Figure 5. 

Size variation (G1, G2, or G3) in prey items consumed by Lutjanus guttatus in the central Gulf of California, measured with the index of relative importance (%IRI).

Diet by season

A total of 141 stomachs from the cold season and 50 stomachs from the warm season were analyzed. During the cold season, the diet included 16 prey items (7 fishes and 9 invertebrates). According to the %IRI, the most important prey were H. thrissina (46.4%), S. sagax (29.4%), N. simplex (21.1%), and Penaeus spp. (2.6%). During the warm season, the diet included 14 prey items (11 fishes and 3 invertebrates). According to the %IRI, the most important prey were S. sagax (43.1%), H. thrissina (34.1%), and Penaeus spp. (21.3%) (Fig. 6). The PERMANOVA test showed that there were significant differences in the diet between the two seasons (F = 5, P < 0.05) (Table 3).

Figure 6. 

Seasonal variation (cold or warm) in prey items of Lutjanus guttatus in the central Gulf of California measured with the index of relative importance (%IRI).

According to the PERMANOVA test, there were no significant differences in the interaction between sex and size (F = 1.2, P = 0.24), between sex and season (F = 0.62, P = 0.76), between size and season (F = 1.5, P = 0.12), or between sex, size and season (F = 0.6, P = 0.79) (Table 3).

Trophic niche width and feeding strategy

According to Levin’s standardized index (Bi), L. guttatus can be considered a specialist predator (Bi = 0.13). Bi values were consistent across the studied categories: by sex (males: Bi = 0.12; females: Bi = 0.12), size (G1: Bi = 0.12; G2: Bi = 0.13; G3: Bi = 0.11), and season (cold: Bi = 0.11; warm: Bi = 0.15). The feeding strategy confirmed that L. guttatus is a benthopelagic predator with a narrow trophic niche; it feeds on a reduced number of prey items that are abundant and frequent (S. sagax, H. thrissina, and Penaeus spp.). However, according to Costello’s graph, the dominance of the main prey varies according to sex, size, and season (Fig. 7).

Figure 7. 

Costello graph. Prey-specific abundance (%N) vs. frequency of occurrence (%FO) in the general diet of Lutjanus guttatus in the central Gulf of California. (A) General, (B) female, (C) male, (D) size group 1, (E) size group 2, (F) size group 3, (G) cold season, (H) warm season. Ss = Sardinops sagax, Ha = Harengula thrissina, Ns = Nyctiphanes simplex, Pe = Penaeus spp., Sj = Scomber japonicus.

Trophic level

The trophic level calculated for L. guttatus was 3.9. The trophic levels for males and females were 3.8 and 3.9, respectively; for size group 1, 2, and 3 trophic levels were 3.8, 4.0, and 4.0, respectively; for cold and warm seasons trophic levels were 3.8 and 3.9, respectively.

Discussion

Several studies have reported on the feeding habits of lutjanid species at various locations. For example, studies on Lutjanus analis (Cuvier, 1828) (see Duarte and García 1999), Lutjanus argentiventris (Peters, 1869) (see Vázquez et al. 2008), Lutjanus campechanus (Poey, 1860) (see Wells et al. 2008), Lutjanus decussatus (Cuvier, 1828), Lutjanus fulviflamma (Forsskål, 1775), Lutjanus fulvus (Forster, 1801), Lutjanus gibbus (Forsskål, 1775) (see Kamukuru and Mgaya 2004; Nanami and Shimose 2013), Lutjanus griseus (Linnaeus, 1758) (see Guevara et al. 2007), Lutjanus malabaricus (Bloch et Schneider, 1801) (see Takahashi et al. 2020), Lutjanus peru (Nichols et Murphy, 1922) (see Moreno-Sánchez et al. 2016), Lutjanus sanguineus (Cuvier, 1828), and Lutjanus sebae (Cuvier, 1816) (see Senta and Peng 1977) have found that snappers are active, mainly carnivorous predators that feed on a wide variety of pelagic and benthic prey, mainly fishes and crustaceans, as well as on bivalves, gastropods, cephalopods, and planktonic organisms such as urochordates. Several authors have also reported that the species within the genus feed on different prey according to the study area, and they have therefore been considered opportunistic predators, which could reflect the high trophic plasticity that allows them to take advantage of the most abundant resources.

In the presently reported study, the trophic spectrum of L. guttatus included 26 categories of prey items. The most important prey items in the diet were fish from the family Clupeidae and crustaceans of the families Euphausiidae and Penaeidae. This is similar to what was reported by Rojas (1997) for this species off the Costa Rica coast, where it fed on 22 categories of prey items, mainly crustaceans from the family Penaeidae. Rojas et al. (2004) reported that off the coast of El Salvador the L. guttatus trophic spectrum comprised 15 categories of prey items, mainly crustaceans of the families Squillidae, Portunidae, and Penaeus. Tripp-Valdez and Arreguín-Sánchez (2009) reported that off Nayarit, Mexico, L. guttatus fed on 26 categories of prey items, the most important of which were crustaceans of the family Xanthidae and fish of the family Engraulidae. However, what was found in the presently reported study differs from what was found by Rojas-Herrera and Chiappa-Carrara (2002) off Guerrero, Mexico, mainly regarding the number of prey item categories; these authors found that at that location the trophic spectrum of the species comprised 88 prey item categories, mainly fish of the families Engraulidae, Clupeidae, and Bregmacerotidae.

Differences among trophic spectra at different locations could be associated with the characteristics of each habitat. At locations where the number of prey items consumed by the species was lower, the ecosystems presented more homogeneous conditions; for example, L. guttatus individuals in Costa Rica are surrounded by mangroves, whereas in Nayarit, Mexico, the area has sandy bottoms and rocky substrates (Tripp-Valdez and Arreguín-Sánchez 2009). However, off Guerrero, Mexico (Rojas-Herrera and Chiappa-Carrara 2002) where the number of prey items consumed by the species was greatest, the species richness could be due to the heterogeneity of the ecosystem, which includes rocky substrates, reef patches, soft bottoms, and a wide continental platform with variable oceanography dynamics (Palacios-Salgado et al. 2014), which allows the species to feed on a greater number of prey items. The study area in the presently reported investigation (Santa Rosalía, BCS) was characterized by sandy and rocky bottoms, where oceanographic processes such as the dominance of regional winds that favor upwelling led to large numbers of prey species such as S. sagax, with approximate abundances of 488 640 t (Martínez-Zavala et al. 2010), Harengula thrissina, with approximate abundances of 150.3 ind. 10 m–2 (Franco-Gordo et al. 2008), and N. simplex, with approximate abundances of 889 ind. 1000 m–3 (Gómez-Gutiérrez et al. 2010).

Significant inter-sexual differences in the proportion of prey items were found; the main prey consumed by the two sexes were the same, but there were differences in the proportions of each prey type consumed. Females consumed a greater proportion of Sardinops sagax, whereas males ate a greater proportion of Harengula thrissina. This same behavior has been reported for other species in the study area (e.g., Mycteroperca rosacea; see Moreno-Sánchez et al. 2019), and could be the result of an ecological strategy by the species to optimize prey consumption and reduce or avoid intraspecific competition (Werner 1979).

Moreover, the difference in diet between the sexes could reflect the energy needs of males and females. For other species in the genus, such as L. campechanus, it was reported that females presented greater energy reserves in muscle as well as liver compared with males; these energy reserves were later used for the formation and maturation of gonads (Schwartzkopf and Cowan 2016). In the case of prey species consumed by L. guttatus, sardines are known for their high energy value, as was reported by Abitia-Cárdenas et al. (1997) and Navarro-García (unpublished1) for the striped marlin, Kajikia audax (Philippi, 1887), and the leopard grouper Mycteroperca rosacea, with values oscillating around 3.19–4.97 kcal· g–1 dry weight.

This suggests that the diet differences observed are not due to the energetic demands of females and their different metabolic requirements, but to both sexes having a marked preference for seasonally abundant prey, providing thus an excellent example of the optimal foraging theory. Individuals are selecting prey based on the prey’s vulnerability to capture and time spent to find and handle prey, maximizing thus their energy gains to maximize meeting their requirements (Gerking 1994).

Regarding the difference in the number of prey item categories between sexes, we found a greater number of prey categories (n = 19) in females than in males (n = 10). This type of result has been reported by Doncel and Paramo (2010) for the species Lutjanus synagris (Linnaeus, 1758) in the Colombian Caribbean, where females fed on a greater number of prey categories (n = 23) than males (n = 16). These authors attributed this result to differences in size between the sexes; females were smaller and consumed more crustaceans and mollusks compared with males, which were larger and consumed large amounts of crustaceans and fish. In the presently reported study, the two sexes were of similar size (females = 38.4 ± 5 cm Lt; males = 38.1 ± 4.9 cm Lt), so differences in the diet could be due to other factors. Differences could be due to variations in the distribution and habitat of the two sexes. Santamaría-Miranda et al. (2003) reported that off Guerrero, Mexico, L. peru females were more abundant in areas close to the coast compared with males. This would agree with what was found in the presently reported study because the proportion of males to females was 1:1.9 (M:F), resulting from their capture relatively close to the coast. It has been observed that H. thrissina forms large schools near the coast (Hobson 1968). In this study it was found that L. guttatus females fed on large amounts of H. thrissina compared with males, which could reflect differences in distribution between the two sexes.

There were changes in diet according to size with differences in the proportions of prey consumed, as well as in the variety of prey present in stomach contents. There was an increase in the proportion of fish in the diet compared with invertebrates with increasing L. guttatus size. This change in diet with predator ontogeny has been observed in other species of the genus such as L. analis (see Duarte and García 1999), L. campechanus (see Wells et al. 2008), and L. peru (see Moreno-Sánchez et al. 2016), and has also been observed in other locations where this species has been studied (e.g., Rojas-Herrera and Chiappa-Carrara 2002; Rojas-Herrera et al. 2004; Tripp-Valdez and Arreguín-Sánchez 2009). This has been attributed to morphological differences among the size groups. According to Allen (1985), prey selection in snappers is linked to mouth diameter, with smaller individuals having a smaller mouth aperture, which leads them to consume small-sized prey (e.g., crustaceans), compared with larger individuals with larger mouth apertures that can consume larger prey such as fish. Moreover, the ability to move, hunt, and capture prey could increase with increasing spotted rose snapper size (Rojas 1997; Moreno-Sanchez et. al. 2019).

Seasonal variations in prey items were also detected. For example, there was a notable increase in the consumption of the euphausiid N. simplex during the cold season. It has been reported that euphausiids N. simplex carry out daily vertical migrations in the water column; they are found at greater depths during the day and move to the surface at night. It has also been reported that they undertake their migrations closer to the surface in the cold season when the water column homogenizes, reaching temperatures ≤17°C, whereas in the warm season euphausiids migrate upwards to waters over 50 m deep, avoiding warm surface waters (Gómez-Gutiérrez et al. 2010).

This could explain the increase in the importance of N. simplex in the diet of L. guttatus in the cold season and its lower importance in the diet in the warm season. According to this and the optimal foraging theory, L. guttatus individuals could obtain greater energy benefits by feeding on prey items that are abundant in winter, as they do not spend energy searching for less abundant organisms that are harder to catch (Gerking 1994). This could also be due to the reproductive season of the spotted rose snapper; there are two reproductive periods, one from March to April, which coincides with euphausiid consumption, and a longer period from August to November when L. guttatus consumed mainly sardines. These changes in the consumption of prey species could be due to the reproductive season having a high energetic cost for individuals (Arellano-Martínez et al. 2001).

In the presently reported study, according to Levin’s standardized index values obtained, L. guttatus could be considered a predator with a narrow trophic width, as it used few trophic resources. Of 26 categories of prey items, only four (i.e., Harengula spp., Sardinops sagax, Nyctiphanes simplex, and Penaeus spp.) were found in great proportions in stomach contents, with high abundance and frequency of occurrence. However, it should be mentioned that according to Costello’s graph, there was a change in the importance of the main prey according to sex, size, and season, which would allow us to classify this species as an opportunist predator that feeds on the most available and abundant prey in a given time and place (Gerking 1994).

This behavior has been observed in other species of the genus Lutjanus such as L. argentiventris (see Vázquez et al. 2008) and L. synagris (see Doncel and Paramo 2010). The strategy of reducing the trophic niche and alternating prey allows an efficient distribution of trophic resources and therefore a reduction in intra- and interspecific competition, as L. guttatus in the Gulf of California shares its habitat with similar predators (e.g., L. peru, L. argentiventris, M. rosacea, among others) (Gerking 1994; Moreno-Sánchez et al. 2016). It has been reported that differences in the diet with other sympatric predators can be a strategy to reduce interspecific competition. This could have an evolutionary component, with the shape of the body and head, the type of dentition, and the mandibular mechanism influencing the type of prey consumed (Rooker 1995; Rojas-Herrera et al. 2004; Nanami and Shimose 2013). Nanami and Shimose (2013) described differences in the type of prey consumed by four sympatric lutjanids based on the body type and dentition. L. decussatus and L. fulviflamma presented a compressed body, long teeth, and a mandibular mechanism that allowed them to open and close the mouth rapidly, and they tended to consume a large number of fish. L. fulvus and L. gibbus had a wider body, short conical teeth, a mandibular mechanism with greater strength in the bite, and consumed a larger number of crustaceans. The species L. peru fed mainly on invertebrates such as the shrimp Penaeus californiensis, the crab Pleuroncodes planipes, and the ostracods Myodocopida gen. spp. in the Gulf of California (Moreno-Sánchez et al. 2016), whereas in the presently reported study L. guttatus fed mainly on fish such as S. sagax and Harengula thrissina, as well as on euphausiids N. simplex and shrimp Penaeus spp. These differences in the type of prey consumed could be due to morphometric differences in the dental and premaxillary bones, as was mentioned by Rojas-Herrera et al. (2004).

The trophic level calculated for L. guttatus was 3.9, which classifies it as a tertiary consumer, coinciding with what has been reported for other species in the genus, such as L. campechanus (TL = 4.2) (Tarnecki and Paterson 2015), Lutjanus purpureus (Poey, 1866) (TL = 3.8), and L. synagris (TL = 3.5) (García and Contreras 2011) and for the same species in Colima, Mexico (TL = 3.7) (Tripp-Valdez and Arreguín-Sánchez 2009). This reflects its feeding habits as a carnivorous predator that feeds mainly on intermediate trophic levels.

According to the results obtained, we conclude that L. guttatus in the central Gulf of California is an opportunistic carnivorous benthopelagic predator, presenting a narrow trophic niche and also displaying changes in feeding strategy according to sex, size, and season, which allows it to minimize intra- and interspecific competition.

Acknowledgments

All authors are grateful to CONACyT, to the Sistema Nacional de Investigadores, the Secretaría de Investigación y Posgrado of the Instituto Politécnico Nacional, and the projects 20196721, 20201105, and 20200266. XGMS and LAAC are thankful for support received through the Comisión de Operación y Fomento de Actividades Académicas and Estímulos al Desempeño de los Investigadores of the IPN. EME is grateful to Mexico’s National Council of Science and Technology (CONACyT) for support through the program “cátedras” (Project No. 2137).

References

  • Abitia-Cárdenas LA, Galván-Magaña F, Rodríguez-Romero J (1997) Food habits and energy values of prey of striped marlin, Tetrapturus audax, off the coast of Mexico. Oceanographic Literature Review 95(2): 360–368.
  • Allen GR (1985) Snappers of the world an annotated and illustrated catalogue of lutjanid species known to date. FAO Fisheries Synopsis 125(6): 1–208.
  • Amundsen PA, Gabler HM, Staldvik FJ (1996) A new approach to graphical analysis of feeding strategy from stomach contents data-modification of the Costello (1990) method. Journal of Fish Biology 48: 607–614. https://doi.org/10.1111/j.1095-8649.1996.tb01455.x
  • Arellano-Martínez M, Rojas-Herrera A, García-Domínguez F, Ceballos-Vázquez BP, Villalejo-Fuerte M (2001) Ciclo reproductivo del pargo lunarejo Lutjanus guttatus (Steindachner, 1986) en las costas de Guerrero, México. Biología Marina y Oceanografía 36(1): 1–8. https://doi.org/10.4067/S0718-19572001000100001
  • Brown SC, Bizzarro JJ, Cailliet GM, Ebert DA (2012) Breaking with tradition: Redefining measures for diet description with a case study of the Aleutian skate Bathyraja aleutica (Gilbert, 1896). Environmental Biology of Fishes 95(1): 3–20. https://doi.org/10.1007/s10641-011-9959-z
  • Brusca RC (1980) Common intertidal in invertebrates of the Gulf of California. 2nd edn. University of Arizona Press, Tucson AZ.
  • Colwell RK (2009) EstimateS: Statistical estimation of species richness and shared species from samples. V. 8.2. [Unknown]: [publisher unknown]. [accessed 2019 Feb 01] http://viceroy.eeb.uconn.edu/estimates
  • Cortés E (1997) A critical review of methods of studying fish feeding based on analysis of stomach contents: Application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 54(3): 726–738. https://doi.org/10.1139/f96-316
  • Daniel WW (1997) Bioestadística. Base para el análisis de las ciencias de la salud. Limusa, México DF.
  • Díaz-Ruiz S, Cano-Quiroga E, Aguirre-León A, Ortega-Bernal R (2004) Diversidad, abundancia y conjuntos ictiofaunísticos del sistema lagunar-estuarino Chantuto-Panzacola, Chiapas, México. Revista de Biología Tropical 52(1): 187–199. https://doi.org/10.15517/rbt.v52i1.14879
  • Doncel O, Paramo J (2010) Food habits of the lane snapper, Lutjanus synagris (Perciformes: Lutjanidae), in the north zone of the Colombian Caribbean. Latin American Journal of Aquatic Research 38(3): 413–426.
  • Duarte LO, Garcia C (1999) Diet of the mutton snapper Lutjanus analis (Cuvier) from the Gulf of Salamanca, Colombia, Caribbean Sea. Bulletin of Marine Science 65: 453–465.
  • FAO (2020) FAOSTAT. Food and Agriculture Organization of the United Nations, Rome.
  • Fischer W, Krupp F, Schneider W, Sommer C, Carpenter KE, Niem VH (1995) Guía FAO para la identificación de peces para los fines de pesca. Pacífico Centro-Oriental. Vol. II and III. Vertebrados. Parts 1–2: 647–1813.
  • Franco-Gordo C, Godínez E, Suárez-Morales E, Freire J (2008) Interannual and seasonal variability of the diversity and structure of ichthyoplankton assemblages in the central Mexican Pacific. Fisheries Oceanography 17(3): 178–190. https://doi.org/10.1111/j.1365-2419.2008.00463.x
  • Freitas MO, Abilhoa V, Giglio VJ, Hostim-Silva M, de Moura RL, Francini-Filho RB, Minte-Vera CV (2015) Diet and reproduction of the goliath grouper, Epinephelus itajara (Actinopterygii: Perciformes: Serranidae), in eastern Brazil. Acta Ichthyologica et Piscatoria 45(1): 1–11. https://doi.org/10.3750/AIP2015.45.1.01
  • Froese R, Pauly D (2019) FishBase: World Wide Web electronic publication. [accessed 2020 December 15] http://www.fishbase.org
  • García CB, Contreras CC (2011) Trophic levels of fish species of commercial importance in the Colombian Caribbean. Revista de Biología Tropical 59(3): 1195–1203. https://doi.org/10.15517/rbt.v0i0.3391
  • Gerking SD (1994) Feeding ecology of fish. Academic Press, San Diego, New York, Boston, London, Sydney, Tokio, Toronto.
  • Gómez-Gutiérrez J, Tremblay N, Martínez-Gómez S, Robinson CJ, Del Ángel-Rodríguez J, Rodríguez-Jaramillo C, Zavala-Hernández C (2010) Biology of the subtropical sac-spawning euphausiid Nyctiphanes simplex in the northwestern seas of Mexico: Vertical and horizontal distribution patterns and seasonal variability of brood size. Deep-sea Research. Part II, Topical Studies in Oceanography 57(7–8): 606–615. https://doi.org/10.1016/j.dsr2.2009.10.010
  • Guevara E, Álvarez H, Mascaró M, Rosas C, Sánchez A (2007) Hábitos alimenticios y ecología trófica del pez Lutjanus griseus (Pisces: Lutjanidae) asociado a la vegetación sumergida en la Laguna de Términos, Campeche, México. Revista de Biología Tropical 55(3–4): 989–1004. https://doi.org/10.15517/rbt.v55i3-4.5972
  • Hobson ES (1968) Predatory behavior of some shore fishes in the Gulf of California. U.S. Bureau of Sport Fisheries and Wildlife Research Report 73: 1–92.
  • Iverson LK, Pinkas L (1971) A pictorial guide to beak of certain eastern Pacific cephalopods. California Department of Fish and Games. Fish Bulletin 152: 83–105.
  • Jiménez-Valverde A, Hortal J (2003) Las curvas de acumulación de especies y la necesidad de evaluar la calidad de los inventarios biológicos. Revista Ibérica de Aracnología 8: 151–161.
  • Kamukuru AT, Mgaya YD (2004) The food and feeding habits of blackspot snapper, Lutjanus fulviflamma (Pisces: Lutjanidae) in shallow waters of Mafia Island, Tanzania. African Journal of Ecology 42(1): 49–58. https://doi.org/10.1111/j.0141-6707.2004.00487.x
  • Keen EM (2012) Adult Euphausiidae of the coastal Northeast Pacific A field guide. SIO 271 Marine Zooplankton profesor Mark Ohman, 45 pp.
  • Krebs CJ (1989) Ecological methodology. Addison Wesley Longman, 620 pp.
  • Labropoulou M, Eleftheriou A (1997) The foraging ecology of two pairs of congeneric demersal fish species: Importance of morphological characteristics in prey selection. Journal of Fish Biology 50(2): 324–340. https://doi.org/10.1111/j.1095-8649.1997.tb01361.x
  • Lowry MS (2011) Photographic catalog of California marine fish otoliths: Prey of California sea lions (Zalophus californianus). NOAA Technical Memorandum NMFS SWFSC, 483 pp.
  • Martínez-Zavala M, Narváez-Martínez MO, Anguiano-Carrazco ML, Santos-Molina JP, Godínez-Cota AR (2010) Captura de peces pelágicos menores en el Golfo de California, temporada 2007–2008. Ciencia Pesquera 18(2): 1–15.
  • Moreno-Sánchez XG, Abitia-Cardenas LA, Trujillo-Retana G, Navia AF, Ramírez-Pérez JS, Shirasago-German B (2016) Variation of feeding habits of Lutjanus peru (Actinopterygii: Perciformes: Lutjanidae) caught in two regions of the Gulf of California, Mexico. Acta Ichthyologica et Piscatoria 46(2): 97–108. https://doi.org/10.3750/AIP2016.46.2.05
  • Moreno-Sánchez XG, Perez-Rojo P, Irigoyen-Arredondo MS, Marin-Enríquez E, Abitia-Cárdenas LA, Escobar-Sanchez O (2019) Feeding habits of the leopard grouper, Mycteroperca rosacea (Actinopterygii: Perciformes: Epinephelidae), in the central Gulf of California, BCS, Mexico. Acta Ichthyologica et Piscatoria 49(1): 9–22. https://doi.org/10.3750/AIEP/02321
  • Morris RH, Abbott DP, Haderlie EC (1980) Intertidal Invertebrates of California. Stanford University Press, Stanford (CA), 690 pp.
  • Nanami A, Shimose T (2013) Interspecific differences in prey items in relation to morphological characteristics among four lutjanid species (Lutjanus decussatus, L. fulviflamma, L. fulvus and L. gibbus). Environmental Biology of Fishes 96(5): 591–602. https://doi.org/10.1007/s10641-012-0049-7
  • Navia AF, Cruz-Escalona VH, Giraldo A, Barausse A (2016) The structure of a marine tropical food web, and its implications for ecosystem-based fisheries management. Ecological Modelling 328: 23–33. https://doi.org/10.1016/j.ecolmodel.2016.02.009
  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Warner H (2015) vegan: Community Ecology Package. R Package version 2.2-1. http://CRAN.R-project.org/package=vegan
  • Palacios-Salgado DS, Ramirez A, Rojas-Herrera AA, Granados-Amores J, Melo-García MA (2014) Marine fishes of Acapulco, Mexico (Eastern Pacific Ocean). Marine Biodiversity 44(4): 471–490. https://doi.org/10.1007/s12526-014-0209-4
  • Pauly D, Zeller D, Palomares MLD (2020) Sea Around Us Concepts, Design and Data (seaaroundus.org).
  • Pinkas LS, Oliphant M, Iverson ILK (1971) Food habits of albacore, bluefin tuna, and bonito in California waters. Fish Bulletin 152: 1–105.
  • Rojas JR (1997) Dieta del pargo colorado Lutjanus colorado (Pisces: Lutjanidae) en el Golfo de Nicoya, Costa Rica. Revista de Biología Tropical 45(3): 1173–1183.
  • Rojas JR (2006) Reproducción y alimentación del tiburón enano Mustelus dorsalis (Pisces: Triakidae) en el Golfo de Nicoya, Costa Rica: elementos para un manejo sostenible. Revista de Biología Tropical 54(3): 861–871. https://doi.org/10.15517/rbt.v54i3.13683
  • Rojas M, Maravilla E, Chicas B (2004) Hábitos alimentarios del pargo mancha Lutjanus guttatus (Pisces: Lutjanidae) en Los Cóbanos y Puerto La Libertad, El Salvador. Revista de Biología Tropical 52(1): 163–170. https://doi.org/10.15517/rbt.v52i1.14820
  • Rojas-Herrera AA, Chiappa-Carrara X (2002) Feeding habits of the spotted rose snapper Lutjanus guttatus (Pisces: Lutjanidae) in the coast of Guerrero, Mexico. Ciencias Marinas 28(2): 133–147. https://doi.org/10.7773/cm.v28i2.219
  • Rojas-Herrera AA, Mascaro M, Chiappa-Carrara X (2004) Hábitos alimentarios de los peces Lutjanus peru y Lutjanus guttatus (Pisces: Lutjanidae) en Guerrero, México. Revista de Biología Tropical 52(4): 959–971.
  • Rooker JR (1995) Feeding ecology of the schoolmaster snapper, Lutjanus apodus (Walbaum), from southwestern Puerto Rico. Bulletin of Marine Science 56: 881–894.
  • Santamaria-Miranda A, Elorduy-Garay JF, Villalejo-Fuerte M, Rojas-Herrera AA (2003) Desarrollo gonadal y ciclo reproductivo de Lutjanus peru (Pisces: Lutjanidae) en Guerrero, México. Revista de Biología Tropical 51(2): 489–502.
  • Sarabia-Méndez M, Gallardo-Cabello M, Espino-Barr E, Anislado-Tolentino V (2010) Characteristics of population dynamics of Lutjanus guttatus (Pisces: Lutjanidae) in Bufadero Bay, Michoacan, Mexico. Hidrobiológica 20(2): 147–157.
  • Schwartzkopf BD, Cowan Jr JH (2016) Seasonal and sex differences in energy reserves of red snapper Lutjanus campechanus on natural and artificial reefs in the northwestern Gulf of Mexico. Fisheries Science 83(1): 13–22. https://doi.org/10.1007/s12562-016-1037-1
  • Senta T, Peng C-C (1977) Studies on the feeding habits of red snappers, Lutjanus sanguineus and L. sebae. Proceedings of the Technical Seminar on South China Sea Fisheries Resources, Bangkok, Thailand, 21–25 May 1973. Tokyo, Japan, Japan International Cooperation Agency, 63–66.
  • Takahashi M, DiBattista J, Jarman S, Newman S, Wakefield C, Harvey E, Bunce M (2020) Partitioning of diet between species and life history stages of sympatric and cryptic snappers (Lutjanidae) based on DNA metabarcoding. Scientific Reports 10: e4319. https://doi.org/10.1038/s41598-020-60779-9
  • Tripp-Valdez A, Arreguin-Sanchez F (2009) The use of stable isotopes and stomach contents to identify dietary components of the spotted rose snapper, Lutjanus guttatus (Steindachner, 1869), off the eastern coast of the southern Gulf of California. Journal of Fisheries and Aquatic Science 4: 274–284. https://doi.org/10.3923/jfas.2009.274.284
  • Vázquez RI, Rodríguez-Romero J, Abitia-Cardenas LA, Galván-Magaña F (2008) Food habits of the yellow snapper Lutjanus argentiventris (Peters, 1869) (Percoidei: Lutjanidae) in La Paz Bay, Mexico. Revista de Biología Marina y Oceanografía 43(2): 295–302. https://doi.org/10.4067/S0718-19572008000200008
  • Wells R, Cowan Jr J, Fry B (2008) Feeding ecology of red snapper Lutjanus campechanus in the Northern Gulf of Mexico. Marine Ecology Progress Series 361: 213–225. https://doi.org/10.3354/meps07425
  • Werner EE (1979) Niche partitioning by food size in fish communities. In: Stroud RH, Clepper H (Eds) Predator–Prey Systems in Fisheries Management, Sport Fishing Inst. , Washington DC, 311–322.
  • Whitehead PJP (1985) FAO species catalogue. Vol. 7. Clupeoid fishes of the world. An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, anchovies and wolf-herrings. Part I. Chirocentridae, Clupeidae, and Pristigasteridae. FAO Fisheries Synopsis 125: 1–303.

1Navarro-García RA (2018) Bioenergética de la cabrilla sardinera Mycteroperca rosacea (Streets, 1877) en Santa Rosalía, Baja California Sur, México. Tesis de Licenciatura. Universidad Autónoma de Sinaloa, Facultad de Ciencias del Mar (UAS-FACIMAR), 93 pp.