Regional Variation in the Trophic Ecology of Wahoo (Acanthocybium solandri) in the Western Atlantic Ocean

Abstract

Intrinsic tracers, such as stable isotopes of carbon and nitrogen, are common dietary markers that accumulate in the muscle tissue of consumers and can be used to determine the dietary sources and trophic positions of consumers. The aim of this study was to assess regional variation in the trophic ecology of wahoo (Acanthocybium solandri) using bulk stable isotopes. Muscle biopsies of wahoo were collected from four regions in the western Atlantic Ocean: the eastern Gulf of Mexico, western Gulf of Mexico, Northwest Atlantic Ocean, and Caribbean Sea. Muscle tissue δ¹³C and δ¹⁵N values for wahoo ranged from −15.8‰ to −18.8‰ and from 7.2‰ to 12.8‰, respectively. Wahoo collected in the Caribbean Sea displayed the highest mean δ¹³C value (−16.3‰), and individuals from this region were statistically different from the three other regions sampled. Mean δ¹⁵N values were elevated for wahoo collected in the eastern and western Gulf of Mexico (11.4‰ and 11.1‰, respectively), and the values were over 2‰ higher than samples from the Northwest Atlantic Ocean and Caribbean Sea. Trophic position (TP) was estimated using δ¹⁵N baselines (zooplankton) and δ¹⁵N wahoo values for each region, and mean TP was 0.4 to 0.9 higher in the Caribbean Sea relative to the three other regions, suggesting that wahoo in this region feed on higher-trophic-level prey. The results indicate that δ¹⁵N baselines and the trophic positions of wahoo each vary as a function of their geographic location, which supports the hypothesis that this species feeds opportunistically throughout its range.

1. Introduction

Top predators play an important role in the overall health and sustainability of marine ecosystems. Many higher-order predators (e.g., billfishes, swordfish, tunas, wahoo) are capable of regulating populations of lower-level consumers through top-down control [1]. As a result, shifts in their foraging may initiate trophic cascades that affect multiple trophic levels of the food web [1]. Given the importance of top-down regulation on ecosystem productivity and resiliency, scientists are increasingly interested in determining the trophic relationships of higher-order consumers within their respective food webs, which can provide valuable information on the role of these predators in regulating energy transfer and community structure within marine food webs.

An improved understanding of the source(s) of organic matter (i.e., primary producers) supporting top predators and the trophic structure of marine food webs is crucial for resource managers, as it influences the stability and resiliency of marine ecosystems. To date, trophic information for many predatory marine teleosts is limited, and understanding the role of these apex predators in marine ecosystems throughout their range is vital for proper management of those systems. Intrinsic dietary tracers, such as stable isotopes, are increasingly used in trophic ecology studies of marine fishes [2,3,4,5]. Stable isotope ratios of carbon and nitrogen can elucidate source(s) of organic matter that supports a community and the trophic position of consumers in the food web, respectively. δ¹³C only fractionates 0.5–1.5‰ per trophic level, and this marker is typically used to determine the source(s) of organic matter supporting consumers [5]. In contrast, δ¹⁵N is often used as a proxy for trophic position because this marker fractionates approximately 3‰ over each trophic level [5].

Wahoo (Acanthocybium solandri) are members of the family Scombridae that includes tunas and mackerels. Wahoo are predators found in the epipelagic zone throughout tropical and subtropical waters around the globe [6]. Wahoo are assumed to be opportunistic piscivores with occasional contributions to diet composition from other taxa, including cephalopods and crustaceans [7,8]. The aim of this study was to apply stable isotope analysis (SIA) to evaluate the source(s) of organic matter supporting wahoo and their trophic position across four geographic regions in the western Atlantic Ocean. Two common dietary markers (δ¹³C and δ¹⁵N) were used to elucidate broad feeding inferences of wahoo and assess regional variation in trophic relationships.

2. Materials and Methods

Muscle biopsies of wahoo were collected from four sampling regions in June through October of 2021 (Figure 1): the eastern Gulf of Mexico (n = 11), western Gulf of Mexico (n = 10), Northwest Atlantic Ocean (n = 10), and Caribbean Sea (n = 10). Biopsies were opportunistically collected from individuals caught via recreational and commercial fishing operations once vessels returned to port. All sampled individuals were between 110 cm and 140 cm fork length [9], representing sexually mature adults [10]. Muscle biopsies were collected in the field and stored at −20 °C between collection and processing. Cleaned samples were then lyophilized for 24 h; freezing was completed at −45 °C for 12 h, and drying was completed via vacuum pump at 50 °C for another 12 h. Lyophilized samples were powdered with a mortar and pestle and weighed to 1 mg ± 0.1 mg in 9 × 5 mm tin capsules. Tissue samples were analyzed on an elemental analyzer isotope ratio mass spectrometer (EA-IRMS; Sercon Ltd., Cheshire, UK) at the University of California Davis Stable Isotope Facility. Delta notation (δ) was used to present isotope ratios (¹³C:¹²C or ¹⁵N:¹⁴N) relative to international standards: Vienna PeeDee Belemnite (VPDB) for carbon and air (N₂) for nitrogen. The long-term standard deviations of the isotope ratios at this facility are 0.2‰ for δ¹³C and 0.3‰ for δ¹⁵N. C:N ratios of the analyzed samples were below 3.5, indicating that δ¹³C values were not significantly influenced by lipid content in the muscle and thus did not require lipid extraction [11]. Although smaller sample sizes may affect the power of statistical tests, variation of δ¹³C and δ¹⁵N signatures within regions was lower than among regions and thus the sample size was sufficient to assess regional differences.

Trophic position (TP) was calculated using Equation (1), where 3 represents the average enrichment of δ¹⁵N per trophic level [12]. Because baseline δ¹⁵N values of the primary producers varies across sampled regions, adjusted TP (TP_ADJ) estimates were estimated using regional δ¹⁵N values reported for the broader Atlantic Ocean and Gulf of Mexico [13,14]; standard TP (TP_STD) estimates based on a single δ¹⁵N baseline value that does not account for regional variation were also estimated. The isoscapes used provided δ¹⁵N values for zooplankton (δ¹⁵N_ZP), which are indicative of the trophic level above primary producers. Following the average enrichment of δ¹⁵N per trophic level stated above, the δ¹⁵N_producer value was determined by (δ¹⁵N_ZP − 3).

TP_consumer = 1 + (δ¹⁵N_consumer − δ¹⁵N_producer)/3

(1)

Regional variation in δ¹³C and δ¹⁵N values were investigated with a one-way analysis of variance (ANOVA) and Tukey’s honestly significant difference (HSD) test. Quadratic discriminant function analysis was used to determine classification success for each collection region based on δ¹³C and δ¹⁵N values. All statistical analysis was conducted in RStudio (R version 4.2.2).

3. Results

3.1. Regional δ¹³C and δ¹⁵N Values

Muscle tissue δ¹³C and δ¹⁵N values of wahoo varied across the four geographic locations sampled. Specifically, δ¹³C values of wahoo from the Caribbean Sea were significantly different compared to the Northwest Atlantic Ocean and both regions in the Gulf of Mexico (ANOVA, p < 0.01; Figure 2). Wahoo collected from the Caribbean Sea had significantly enriched δ¹³C values (−16.3‰ ± 0.32; mean ± 1 SD), with relatively similar signatures shown in the other three regions: Northwest Atlantic Ocean (−17.2 ± 0.66), eastern Gulf of Mexico (−17.1 ± 0.26), western Gulf of Mexico (−17.0 ± 0.29) (

Table 1. Size (mean FL in cm ±1 SD), baseline zooplankton δ¹⁵N (δ¹⁵N_ZP) values [13,14], standard (STD) trophic position (based on same δ¹⁵N baseline value for all regions), and adjusted (ADJ) range and mean estimates of trophic position (mean ± standard deviation) for wahoo using region-specific δ¹⁵N_ZP values from the four sampling regions. TP_STD based on standard δ¹⁵N_ZP of 6.2 for all four regions, while TP_ADJ range and mean estimates based on region-specific δ¹⁵N_ZP values shown in table.

Region	Size (cm FL)	δ15NZP	TPSTD	TPADJ Range	TPADJ Mean
Gulf of Mexico
East	130.1 ± 8.0	6.2	3.7 ± 0.4	2.9–4.0	3.7 ± 0.4
West	124.4 ± 10.1	6.2	3.6 ± 0.4	2.9–4.2	3.6 ± 0.4
Atlantic Ocean
Caribbean Sea	132.3 ± 6.8	2.0	2.7 ± 0.2	3.7–4.4	4.1 ± 0.2
Northwest Atlantic	123.9 ± 5.1	5.5	3.0 ± 0.2	3.0–3.7	3.2 ± 0.2

). Regional variation was also observed for muscle tissue δ¹⁵N values, with samples collected from both regions in the Gulf of Mexico (east = 11.4 ± 1.0, west = 11.1 ± 1.1) displaying significantly higher values relative to samples from the Northwest Atlantic Ocean (9.2 ± 0.59) and Caribbean Sea (8.4 ± 0.53) (ANOVA, p < 0.01; Figure 2); however, no significant differences were detected between the two regions in the Gulf of Mexico or between the two regions in the Atlantic Ocean.

Collection locations in the Gulf of Mexico and Atlantic Ocean were grouped to further evaluate large-scale variation, and δ¹³C and δ¹⁵N signatures from the two larger geographic regions were significantly different (MANOVA, p < 0.01). Quadratic discriminant function analysis (QDFA) parameterized with δ¹³C and δ¹⁵N signatures displayed a relatively high cross-validated classification success (85%) in the two larger regions, indicating that these dietary signatures show promise for retrospectively determining the collection location of wahoo (Gulf of Mexico vs. Atlantic Ocean) for samples of unknown origin.

3.2. Regional TP Estimates

Estimates of standard trophic position (TP_STD) for wahoo were estimated using a standard baseline for all regions. In addition, adjusted TP (TP_ADJ) estimates were derived using δ¹⁵N_ZP values (baseline) for each region from available isoscapes [13,14]. Standard TP estimates of wahoo were between 2.7 and 3.7, with significantly higher values reported for wahoo collected in the Gulf of Mexico (ANOVA, p < 0.001). Adjusted TP estimates of wahoo derived using regional estimates of δ¹⁵N_ZP markedly increased the position of individuals from the Caribbean Sea by nearly two trophic steps (4.1). While this region was characterized by the lowest TP using a single δ¹⁵N baseline value, TP was approximately a half to full trophic step higher when using region-specific baseline values and significantly different from the three other regions (Tukey HSD, p < 0.05). Adjusted TP estimates using region-specific baselines were lowest in the Northwest Atlantic Ocean, and both TP range and means were similar (3.6–3.7) between the two regions in the Gulf of Mexico.

4. Discussion

Regional differences in muscle tissue δ¹³C values of wahoo collected across the four regions were observed, but similarities were also present for individuals collected from different regions within the Gulf of Mexico and within the Atlantic Ocean. Similar δ¹³C values for wahoo in both the eastern and western Gulf of Mexico support the premise that source(s) of organic matter supporting the pelagic food web and associated top predators in this region are similar in ecosystems both east and west of the Mississippi River Delta. Recently reported δ¹³C isoscapes for zooplankton in the outer shelf and slope waters of the northern Gulf of Mexico also reported limited variation in δ¹³C values [15], which is in accord with our findings for wahoo. Outside the Gulf of Mexico, our finding of comparable δ¹³C values for wahoo collected in the Northwest Atlantic Ocean and Caribbean Sea was less expected given the distance between the two regions and different latitudinal biomes of each collection area (tropical versus temperate); however, variation in the δ¹³C values of both phytoplankton and zooplankton in the general areas that wahoo were sampled in the Northwest Atlantic Ocean (Mid-Atlantic Bight) and Caribbean Sea (Lesser Antilles) is generally limited (~1–2‰ range) [16]. This indicates that although these two provinces are separated geographically, primary sources of organic matter and/or δ¹³C values of major autotrophs in both regions may be comparable.

Muscle tissue δ¹⁵N values of wahoo also varied across the four regions, with similarities observed for individuals collected from the two regions in the Gulf of Mexico and from the two regions in the Atlantic Ocean. δ¹⁵N values for wahoo from the Gulf of Mexico were significantly higher than individuals from the Atlantic Ocean and generally comparable to previously reported values for wahoo throughout their range [9,17]. A study conducted in the Galapagos Islands reported mean δ¹⁵N values for wahoo of 15.3‰, nearly 4.0‰ higher than any region assessed in the present study [18]; however, estimating adjusted TP using mean zooplankton δ¹⁵N values from this region of the Pacific Ocean resulted in similar values in our study [19], further confirming the importance of incorporating region-specific baseline δ¹⁵N data for estimating TP. Unique baseline δ¹⁵N values were present across the sampling locations of this study, with significantly lower δ¹⁵N values of zooplankton (δ¹⁵N_ZP) present in the Caribbean Sea [20] compared to the Gulf of Mexico and Northwest Atlantic Ocean. Lower δ¹⁵N_ZP values were shown to be characteristic of oligotrophic waters due to increased nitrogen fixation by diazotrophic cyanobacteria [20,21], whereas waters influenced by anthropogenic nitrogen sources from riverine output such as the Mississippi River delta tend to report higher δ¹⁵N_ZP values [14,22]. Despite significantly higher δ¹⁵N values for wahoo in the Gulf of Mexico, incorporating δ¹⁵N_ZP values into TP estimates accounted for regional variation in δ¹⁵N baselines and elevated the TP of wahoo from the Caribbean Sea. Nevertheless, adjusted TP estimates of wahoo from all four regions were comparable to previously reported values in different parts of their range and also similar to other higher-order marine teleosts in pelagic ecosystems [10,23,24,25], further supporting the premise that wahoo appear to be opportunistic predators that feed at similar trophic levels throughout their range in tropical and subtropical waters.

It is well understood that baseline δ¹³C and δ¹⁵N values and prey fields vary spatially and temporally, and therefore movements or migrations of predators can lead to shifts in prey selection and TP. As a result, a better understanding of the home range and migrations of wahoo may help explain observed regional trends observed in muscle tissue δ¹³C and δ¹⁵N. For example, similarities in muscle tissue δ¹³C and δ¹⁵N values for wahoo in both the eastern and western Gulf of Mexico may be associated with active movements or migrations between the two regions. Conversely, conspicuous differences in δ¹³C and δ¹⁵N values observed for individuals collected from the two larger geographic (Gulf of Mexico vs. Atlantic Ocean) regions may indicate that long-distance movements between these two regions is less likely. Data on the population connectivity of wahoo coupled with higher quality δ¹³C and δ¹⁵N baselines, including other sources of dietary information, are critically needed to elucidate the drivers of region-specific variation and further clarify trophic relationships for this species.