Corresponding author: Xchel G. Moreno-Sánchez ( xchel.moreno@gmail.com ) Academic editor: Ken Longenecker
© 2021 Filius L. Valle-Lopez, Xchel G. Moreno-Sánchez, Marina S. Irigoyen-Arredondo, Leonardo A. Abitia-Cárdenas, Emigdio Marín-Enríquez, Jorge S. Ramírez-Pérez.
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Citation:
Valle-Lopez FL, Moreno-Sánchez XG, Irigoyen-Arredondo MS, Abitia-Cárdenas LA, Marín-Enríquez E, Ramírez-Pérez JS (2021) Feeding habits of the spotted rose snapper, Lutjanus guttatus, (Actinopterygii, Perciformes, Lutjanidae), in the central Gulf of California, BCS, Mexico. Acta Ichthyologica et Piscatoria 51(1): 95-105. https://doi.org/10.3897/aiep.51.63227
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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.
Lutjanidae, diet, sardines, euphausiids, Gulf of California
Studies on the food habits of fish are fundamental to understand the structure and functioning of marine ecosystems (
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 (
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 (
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) (
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 (
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 (
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 (
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.
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.
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.
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
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 (
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 (
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 (
Levin’s standardized index (Bi) was used (
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.
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
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 (
The L. guttatus trophic level was calculated using the formula proposed by
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 (
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
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 |
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
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 |
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.
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.
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 |
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.
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.
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
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.
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.
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.
Several studies have reported on the feeding habits of lutjanid species at various locations. For example, studies on Lutjanus analis (Cuvier, 1828) (see
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
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 (
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
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 (
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 (
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
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
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 (
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 (
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 (
This behavior has been observed in other species of the genus Lutjanus such as L. argentiventris (see
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) (
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.
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).