https://orcid.org/0000-0002-9071-2962
Figures
Abstract
The temporal variability of fish habitat utilization is poorly understood in tropical deltaic systems due to high water turbidity, which limits visual censuses, and to the lack of long-term data incorporating climate variability events. We aimed to assess the influence of body size and El Niño Southern Oscillation (ENSO) variability on the cross-habitat utilization rate of 14 fish species of commercial relevance in the Ciénaga Grande de Santa Marta (CGSM). We estimated the utilization of mangroves and coastal lagoons based on relative catch frequencies from encircling gillnets used within a long-term catch monitoring program, and then tested for significant changes in each species’ habitat utilization as a function of body size and climate variability. Six species showed a high dependence on mangroves and four on coastal lagoons for most body size classes (including juveniles) and ENSO conditions. One species (Elops smithi) showed a high utilization of mangroves in some ENSO phases and body size classes, while three species showed a high utilization of both mangroves and coastal lagoons. Mangrove utilization by six species (Megalops atlanticus, E. smithi, Centropomus undecimalis, Mugil incilis, Mugil liza, and Ariopsis canteri) increased in larger body sizes at low depths, which usually occurs under dry ENSO conditions, when predatory risk is higher in coastal lagoons. Another species (Caquetaia kraussi) increased its mangrove utilization from the body size at which its feeding habits change. Mangroves and coastal lagoons are important nurseries and habitats for adults of the main commercial fish species in the CGSM. Seascape habitats and fringe/riverine mangroves must be conserved in tropical deltas to promote not only nurseries but also fish lifecycles.
Citation: Sánchez-Núñez DA, Viloria Maestre E, Rueda M (2024) Cross-habitat utilization of fish in a tropical deltaic system as a function of climate variability and body size: Are mangroves fish nurseries in a tropical delta? PLoS ONE 19(8): e0308313. https://doi.org/10.1371/journal.pone.0308313
Editor: Tzen-Yuh Chiang, National Cheng Kung University, TAIWAN
Received: January 10, 2024; Accepted: July 21, 2024; Published: August 16, 2024
Copyright: © 2024 Sánchez-Núñez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: A repository for the figures' data from the article has been created: The database where the data was extracted is of public access: http://sipein.invemar.org.co/informes/tallas/externos/ ONI database is also of public access https://origin.cpc.ncep.noaa.gov/products/analysis_monitoring/ensostuff/ONI_v5.php The data of the paper figures are available at: Sanchez-Núñez, David Alejandro; Viloria Maestre, Efrain; Rueda, Mario (2024), “Data from Cross-Habitat Utilization of Fish in a Tropical Deltaic System as a Function of Climate Variability and Body Size: Are Mangroves Fish Nurseries in a Tropical Delta?”, Mendeley Data, V1, https://data.mendeley.com/datasets/xkj793sdmz/1.
Funding: Universidad Nacional de Colombia (Hermes code 57242) and INVEMAR awarded to DASN. The funders had no role in study design, and analysis, decision to publish, or preparation of the manuscript. INVEMAR, the Marine and Coastal Research Institution of Colombia, provided data on fishery monitoring and physicochemical variables in the Pajarales Complex of the Cienaga Grande de Santa Marta. We used such data in our study. This is the contribution #1380 of INVEMAR.
Competing interests: The authors have declared that no competing interests exist.
Introduction
The presence of mangroves is often linked to higher fish densities in different geographical locations and environmental settings [1–4]. Although the nursery function has been predominantly highlighted in most mangrove fish and fishery studies, the high utilization of sub-adults and adults has also been described in several fish species and mangrove settings [5, 6]. The nursery function of mangroves has been associated with the supply of shelter from predators, greater food availability, and the favorable microclimatic and hydrodynamic conditions for juveniles within mangrove roots [7, 8]. On the other hand, the increased utilization of mangroves and macrophyte vegetation by some species of larger fish has been linked to ontogenetic dietary shifts, higher mobility, and the supply of adequate shelter during daytime [6, 9–11].
Mangrove-fish relationships have been broadly studied in oligotrophic clear waters (i.e., Caribbean karstic areas), while fewer studies have been carried out in deltaic systems, which are usually subject to high nutrient loads and turbidity levels, and where seagrasses and coral reefs are limited or absent [3, 11–14]. The underrepresentation of deltaic mangrove settings in the literature linking mangroves and fishery is probably due to low visibility in these turbid waters, which hinder visual censuses, a cost-efficient method broadly used to analyze the habitat dependency and shifts of fish in mangrove environments with clearer waters [2, 15]. Since 40% of the world’s mangroves are deltaic [16], there is a clear knowledge gap in understanding mangrove-fishery relations and the flexibility of habitat utilization by fish in this dominant mangrove type, such as cross-habitat movements and utilization over entire lifecycles [5, 9, 17].
Assessing habitat utilization changes in estuarine systems as function of climate variability is a research priority for a better understanding of cross-habitat connectivity [5, 18, 19]. Studies relating climate variability and fish populations in tropical deltaic systems have focused less on habitat utilization and more on the effects of fish abundance [20–23]. In deltaic [24] and coastal settings [25, 26], species-specific ontogenetic habitat use patterns have been found within multi-habitat seascapes. Additionally, in non-estuarine mangrove systems, fish species have shown different degrees of habitat use flexibility as a response to spatial, seasonal, and interannual variations [27].
The ecoregion of the Ciénaga Grande de Santa Marta (CGSM) is one of the largest deltaic systems in the Greater Caribbean [28]. The CGSM is highly influenced by climate variability from the El Niño southern oscillation (ENSO), which drives changes in water levels, salinity, mangrove cover, and fish species composition and abundance [29–31]. On the other hand, the CGSM is a relatively well-studied system, where long-term fishery monitoring regarding catch and body size composition is carried out. In the CGSM, the traditional ecological knowledge clearly recognizes the value of mangroves for fisheries [24, 32–34]. Long fisheries datasets offer an opportunity to study the cross-habitat utilization of fish resources in this major deltaic system of the Caribbean.
This study aimed to assess whether the main estuarine and freshwater fish species captured by small-scale fisheries in the CGSM change their relative habitat utilization according to their body size and in response to climate variability. We anticipated finding species-specific habitat preferences for different body sizes, as observed in other seascape environments [24, 26]. Based on the well-known nursery function of mangroves, we hypothesized that individuals in juvenile life stages would dominate fishery catches inside the mangroves, with larger size classes found in coastal lagoons. In addition, we anticipated that habitat utilization would be affected by climate variability, as has been identified in other mangrove settings [27].
Materials and methods
Study area
The CGSM is located between the coordinates 10°40’ and 10°59’N and 74°15’and 74°38’W [35], as shown in Fig 1A. Its climate is tropical semiarid, with an average temperature of 27.5°C and average precipitation and evapotranspiration values of 400 and 1431 mm year-1, respectively [36]. The Fundación, Aracataca, and Sevilla Rivers drain the Sierra Nevada de Santa Marta and are directly connected to the CGSM’s main coastal lagoon, while the Magdalena River is connected to the system through the Clarín, Aguas Negras, and Renegado Channels [28, 37].
(a) Location of fishing grounds and water depth monitoring stations; (b) body size records by fishing ground. Panel (a) was reprinted from INVEMAR under a CC BY license, with permission from original copyright, 2024.
The CGSM has the largest mangrove extension (35,379 ha in 2019) and the largest coastal lagoon in the Colombian Caribbean (44,010 ha in 2018) [38, 39]. Its fishery is one of the most important in Colombia, supporting approximately 4000 fishermen, who catch more than 50 species of fish, crustaceans, and mollusks using several fishing gears and methods. Between 1994 and 2020, the CGSM fisheries monitoring program estimated annual catches of 4178–9269 t and an average fisher monthly income of 821–144 million COP. On the other hand, the climate variability caused by the ENSO has been identified as the main driver of changes in salinity and in the abundance and composition of species targeted for fishing [29].
On an interannual basis, CGSM fishery exhibits a highly variable natural productivity, and, despite its ecological, economic, and social importance, it shows signs of overfishing. Apart from fishermen, the main fish predators in this region are piscivorous birds. This trophic guild is the most predominant, with 23 species and 47% of bird detections, including herons, egrets, pelicans, cormorants, gulls, terns, storks, kingfishers, ducks, and ospreys [40].
The CGSM experienced a strong environmental degradation between 1956 and 1995, losing 56% of its original mangrove coverage (51,150 ha), due to the construction of a road parallel to the coastline, in addition to a road and dikes in the Magdalena River floodplain, which restricted tidal and freshwater connectivity [41]. A rehabilitation project called PROCIENAGA reconnected the CGSM to the Magdalena River delta. This was done by constructing three river diversion channels between 1996 and 1998 in sites that previously connected the river with coastal lagoons during floods [42]. This hydrological rehabilitation project along with continuous channel maintenance, have recovered an area equivalent to 33% of the original mangrove coverage [39]. Mangrove coverage fluctuations have also occurred as a consequence of ENSO climate variability, with dry periods (El Niño phases) driving coverage losses and wet periods (La Niña phases) driving coverage gains [31]. The CGSM’s area of fringe/riverine mangroves, subject to tidal and fluvial inundation, is approximately 941 ha, compared to the 77,461 ha occupied by coastal lagoons [43].
The Pajarales Complex, a system of coastal lagoons surrounded by mangroves, is located in the northwest of the CGSM ecoregion. Within this complex, there are two small stilt villages of fishermen, with a combined population of 2452 inhabitants [44]. Here, the salinity and dissolved oxygen concentration decline during the La Niña phase, in comparison with neutral ENSO conditions. These parameters increase during El Niño, as ENSO climate variability influences the freshwater flows from the rivers and channel diversions that feed the system [28, 45]. In the northern region of the Pajarales Complex, the average salinity (±SD) values are 8.0±1.2, 19.0±1.1, and 31.2±1.9 g L-1 during La Niña, neutral, and El Niño phases, respectively. Meanwhile, the western part reports 6.2±1.2, 13.3±1.1, and 26.1±1.7 g L-1 for the same phases. The oxygen concentrations reported by northern Pajarales are 7.6±0.2, 8.2±0.2, and 8.2±0.3 mg L-1, and those of the western region are 8.4±0.3, 8.9±0.2, and 9.0±0.3 mg L-1 (S1 Fig). In this region, strong salinity changes favor estuarine species fish during neutral and El Niño phases, as well as freshwater ones under La Niña conditions.
During the wet season, fringe and riverine mangroves, where encircling gillnets are used for fishing, experience daily tidal inundation and high water levels due to increased freshwater delivery from the Aguas Negras Channel into coastal lagoons. Fringe and riverine mangroves and their adjacent coastal lagoon share similar salinity levels. These ecosystems measure around 10 m in width and feature Rhizophora mangle as the dominant species.
Fish species studied
The 14 most abundant commercial species in the CGSM were studied. Of these, eight are estuarine and six are freshwater species. All of them are native, except for the Nile tilapia, which was introduced in Colombia between 1970 and 1975 and invaded the Pajarales Complex in 1995 [23]. It was assumed that this species had already adapted to the complex by 2001 (i.e., the starting year of our dataset), given its high adaptability, reproductive success [46], and the time it had to adapt since its introduction in the Colombian Caribbean. Currently, the Nile tilapia is one of the species with the highest commercial relevance for artisanal fisheries. Between 2001 and 2019, it represented 15% of the catches in the Pajarales Complex. The feeding habits of the studied CGSM species are summarized in Table 1.
Catch data by habitat
The catch data used in this study originate from the fishing monitoring system (SIPEIN) deployed by the Colombian Institute for Marine and Coastal Research (INVEMAR) in the artisanal fisheries of the CGSM and were collected between 1994 and 2020 [57, 58]. The SIPEIN was developed to monitor fishing resources in the CGSM and records daily fishing catches three days a week [59]. In the Pajarales Complex of the CGSM, encircling gillnets with semicircles are independently used for fishing in two habitats: coastal lagoons and mangroves. While using this fishing gear, shallow waters are pounded to promote sediment suspension, thereby asphyxiating the fish [60, 61]. In coastal lagoons, encircling gillnets are deployed beyond 20 m (even hundreds of meters) from the mangrove edges [32]. 5–10 cm mesh is used in both mangroves and coastal lagoons, with mean sizes of 6.6 and 5.1 cm, respectively.
We used SIPEIN data on eight fishing grounds located in the north and the west of the Pajarales Complex from 2001 to 2019. In these areas, the use of encircling gillnets is commonplace (Fig 1B).
Intensity of climate variability
The intensity of the cold and warm episodes of the ENSO was determined using the Oceanic El Niño Index (ONI) [62]. This index is estimated by the NOAA on a monthly basis, and values have ranged from -1.8 to -1.6 during strong La Niña episodes and up to 2.6 during the very strong El Niño of 2015. The fishing records were categorized based on climate variability conditions (El Niño, La Niña, and neutral) and the monthly ONI values [62]. The ENSO affects the regional and local rivers feeding the system in a similar way, with precipitation and water flows increasing during El Niño and decreasing during La Niña [28, 45]. Therefore, it was not necessary to discriminate between local and regional influences with regard to climate variability in the CGSM system.
Water depth
The water depth in the Pajarales Complex during fish catching periods was determined by averaging the depths of four monitoring stations in the area (Fig 1A). On average, INVEMAR monitors each station for eight months per year [63], measuring the water depth in situ from a boat with a Secchi disk.
Data analysis
Relative habitat utilization.
The relative habitat utilization of fish species (i) in each of the two Pajarales Complex zones (Z) and each of the two studied habitats (h) was estimated for different body sizes (bs) and ENSO phases (E), by means of the relative catch frequencies (Fr). The catch frequency of a species in a habitat (Frbs,i,h,E,Z), divided by the total catch frequency across both habitats (FrTbs,i,E,Z), indicates the probability of occurrence and, therefore, the relative habitat utilization (Frhbs,i,E,Z) (Eq 1). Frbs,i,h,E,Z is relative to the total number of individuals of all species captured within each habitat, and Frbs,i,E,Z is relative to the total number of individuals of all species captured in the two habitats. Based on the maturity size of each species in the CGSM [59] and the observed changes in catch frequency with body size between habitats, two to four main body size classes were identified for each species. The fishing records from the four fishing grounds in each zone of the Pajarales Complex were pooled together to carry out the aforementioned estimations (Fig 1B).
(1)
In addition to estimating the relative habitat utilization for each ENSO phase, we also calculated this variable for each fish species (i) in the Pajarales Complex, according to the intensity of cold and warm ENSO episodes (EI) (Eq 2).
(2)
Although the fish stocks for each ENSO condition and year were unknown, it was assumed that the relative frequencies resembled the occurrence probabilities, thereby indicating the habitat utilization, given the temporal continuity of SIPEIN monitoring and the large dataset considered (36,817 body size records in the Pajarales Complex). In addition, the fishing power of the encircling gillnets was considered for all the species in the water column, owing to the shallow depth of the studied region (0.2–1.7 m), which allows deploying this fishing gear from the sediment bed of the water column [64].
Differences in habitat utilization.
A Mann-Whitney U test was conducted with the purpose of identifying significant differences in the relative habitat utilization of fish species in mangroves and coastal lagoons, grouping all sizes and ENSO conditions.
Habitat utilization in response to size and climate variability phases.
Two-way Scheirer-Ray-Hare (SRH) tests [65, 66] were employed to assess the influence of size and climate variability (factors) on habitat utilization. This analysis was carried out for each species and habitat. The relative habitat utilization values of each of the two studied Pajarales regions were used as replicates. Three species were analyzed separately: C. kraussi, H. malabaricus, and P. magdalenae. The largest body size class of C. Kraussi was absent in coastal lagoons during all ENSO phases and in all Pajarales zones, hindering the use of two-factor SRH tests with 3*3 factor levels. Instead, we conducted SRH tests with 2*3 factor levels for C. Kraussi. The other two species, H. malabaricus and P. magdalenae, were absent in both habitats during El Niño and La Niña in one of the Pajarales zones and in almost all size classes, also hindering the SRH tests. For these two species, we performed a Kruskal-Wallis test to independently assess the influence of size and climate variability on habitat utilization. The low number of replicates impeded post hoc comparisons of SRH treatments, so we conducted paired Mann-Whitney U test comparisons for each estuarine or freshwater species, in order to identify which habitat had a significantly higher utilization across different ENSO conditions and body size classes.
Habitat utilization in response to the intensity of climate variability and water depth.
First, a Spearman correlation analysis was conducted to assess the relationship between each species’ average catch body size and relative habitat utilization (Frhi,EI) in response to the monthly ONI records [62]. For the species with significant correlations or whose habitat utilization significantly changed with size (see the SRH test described in the previous section), we performed a regression analysis of the water depth vs. the average catch body size per habitat. The water depth data were organized in intervals of 0.03 cm, and the body sizes present in each interval were averaged.
ENSO climate variability generates changes in the CGSM’s water depth [67]. To confirm the existence of a relationship between this variability and the water depth of the Pajarales Complex, we performed simple and multiple regression analyses of water depth as function of the ONI and the intra-annual seasonality, evaluated as the average time of the year in months. The Aguas Negras Channel has a marked intra-annual seasonality: its freshwater flows are 17–32 m3 s-1 between January and April, 39–58 m3 s-1 between May and August, and 50–80 m3 s-1 between September and December [68]. It is important to add that all statistical analyses were carried out using STATISTICA 10.0 and R 4.4.0.
Ethics statement
INVEMAR is the scientific branch of the Colombian Ministry of Environment and Sustainable Development (MinAmbiente) entrusted with research and monitoring in coastal and marine ecosystems. CORPAMAG, the regional environmental authority of the study site, and MinAmbiente designated INVEMAR to monitor fish catches in the CGSM. In this vein, INVEMAR does not require a permit to access or conduct research in the study site. The SIPEIN records fish catches at the harbor to monitor fishing resources. Fish die mainly by asphyxiation due to the use of encircling gillnets. In this study, we were not involved in the sacrifice of fish. Research involving the monitoring of catches by fishermen for subsistence purposes does not require a permit from the research ethics committee of INVEMAR.
Results
Catch frequencies by habitat
The most frequent species in the mangroves were M. atlanticus, O. niloticus, and E. smithi, while, in the coastal lagoons, M. incilis, M. liza, and C. mapale exhibited high relative catch frequencies (Fig 2). Nine species had a significantly higher preference for mangroves, as well as four for coastal lagoons. One species did not show a significantly higher utilization of any habitat (Table 2).
Water depth as function of climate variability
The intensity of climate variability and the intra-annual seasonality collectively explained the water depth of the Pajarales Complex (r2 = 0.47, p < 0.01 for both independent variables), with climate variability explaining a relatively high degree of the water depth variability (Fig 3). Thus, stronger El Niño episodes and dry seasons generate lower water depths, while wet seasons and stronger La Niña phases entail higher depth values.
SFF: seasonal freshwater flow.
Habitat utilization by estuarine fish species in response to size, climate variability intensity, and water depth
The utilization of M. atlanticus and C. undecimalis in mangroves was significantly higher in comparison with that of coastal lagoons for all body size classes and ENSO conditions (Figs 4 and 5) (Mann-Whitney U, p < 0.05). The habitat utilization of both species significantly changed with size (Table 3).
The standard error in the relative catch frequency between ENSO phases is shown. (a) Estuarine and (b) freshwater fish species.
The standard error in the relative catch frequency between body size classes is shown. (a) Estuarine and (b) freshwater fish species.
For E. smithi, the utilization of mangroves was only significantly greater than that of coastal lagoons in adults and during La Niña phases (Mann-Whitney U, p < 0.05). In M. atlanticus, C. undecimalis, and E. smithi, larger adults were found in mangroves under wetter ENSO conditions and with low water depths usually recorded in drier ENSO phases (Fig 6 and S2 Fig, S1 Table).
For E. plumieri, the utilization of mangroves was higher than that of coastal lagoons across all body sizes and ENSO conditions (Mann–Whitney U, p < 0.05), except for 21–30 cm adults and during El Niño phases. Mangrove utilization decreased by 69% from La Niña to El Niño, but such changes did not significantly affect habitat utilization (Table 3).
The mangrove and coastal lagoon utilization of A. canteri was significantly affected by body size (Table 3), i.e., juveniles and smaller adults preferred coastal lagoons, while larger adults preferred mangroves (Mann-Whitney U, p < 0.05 in all cases). On average, larger fish were present in mangroves with lower water depths, and progressively smaller fish were found in coastal lagoons with drier ENSO conditions (Fig 6 and S2 Fig).
The utilization of coastal lagoons by M. incilis and M. liza was higher than that of mangroves across all body size classes and ENSO conditions (Mann-Whitney U, p < 0.05), except for larger adults and during El Niño in M. incilis, whose utilization of mangroves was influenced by ENSO conditions and their interaction with body size (Table 3, S2 Fig); it grew simultaneously with drier ENSO conditions and larger body sizes, reaching its highest value (61%) for larger adults during El Niño. In M. incilis and M. liza, habitat utilization was significantly affected by size (Table 3), with coastal lagoon utilization declining for larger sizes. In agreement with these results, the relationship between water depth and average body size shows that, on average, larger adults of these species are present in mangroves with lower water depths usually found under drier ENSO conditions.
In C. mapale, the utilization of coastal lagoons was also higher than that of mangroves for all body size classes and ENSO conditions (Mann-Whitney U, p < 0.05), except for juveniles and during neutral phases.
Habitat utilization by freshwater fish species in response to size and climate variability
O. niloticus exhibited a higher utilization of mangroves because it was absent from coastal lagoons in all body sizes and across all ENSO conditions. The habitat utilization of C. kraussi was affected by size (Table 3); juveniles showed a higher utilization of coastal lagoons, while larger adults exhibited a higher utilization of mangroves (Mann-Whitney U, p < 0.05 in all cases).
The habitat utilization of M. muyscorum significantly changed according to ENSO conditions and their interaction with body size: juveniles were only present in coastal lagoons during La Niña, and they were only found in mangroves during neutral and El Niño phases (Fig 4 and S3 Fig). In contrast, larger adults showed a 32% higher use of mangroves during La Niña, compared to a 62% higher use of coastal lagoons during El Niño. Therefore, the average body size increased in mangroves with wetter conditions, and the relative mangrove utilization increased with drier conditions (S1 Table). Considering all size classes, the use of mangroves was only greater than that of coastal lagoons during neutral ENSO phases (Mann-Whitney U, p < 0.05).
In P. magdalenae and H. malabaricus, the higher habitat utilization of mangroves was not affected by body size or ENSO phases (Kruskal Wallis test, p > 0.05 in all cases). Mangroves did not exhibit a higher utilization during El Niño and La Niña, or by juveniles of both species (Mann-Whitney U, p > 0.05) due to low replicates. i.e., the absence of fish in one Pajarales zone.
In T. magdalenae, the utilization of coastal lagoons was higher than that of mangroves across all size classes and ENSO conditions (Mann-Whitney U, p < 0.05). However, mangrove utilization was significantly influenced by ENSO conditions and their interaction with body size, and it only occurred under neutral conditions, increasing from 3% in juveniles to 9% in adults.
Discussion
Habitat utilization by estuarine fish species in response to body size, climate variability, and water depth
The high dependence of the tarpon (M. atlanticus) and the snook (C. undecimalis) on mangroves agrees with several literature records. In a worldwide review, C. undecimalis was considered a highly mangrove-affiliated species, while sites with a high degree of mangrove edge accounted for a large number of M. atlanticus occurrences [69, 70]. Mangroves are recognized as nurseries for these species, corroborating our findings with regard to M. atlanticus and C. undecimalis juveniles’ greater preference for mangroves.
The preference of the ladyfish (E. smithi) for mangroves is consistent with a study showing the absence of E. saurus in disturbed mangroves when compared to pre-disturbed and restored sites (prior to 2010, E. smithi was usually identified as E. saurus in the Western Atlantic) [48, 71]. In the CGSM, E. smithi individuals caught during the day exhibited a relatively low or partial digested stomach contents, suggesting a nocturnal predatory behavior [48]. The encircling gillnets used in this study to estimate habitat utilization were set up during the day. Thus, the high mangrove utilization of E. smithi adults may indicate the use of this habitat as daytime resting and refuge sites.
In M. atlanticus, C. undecimalis, and E. smithi, the increasing utilization of larger body sizes in mangroves with drier ENSO conditions or lower water depths could indicate a predator avoidance strategy. Wading birds, which are common fish predators in mangrove environments, have high foraging success in shallow waters, as well as a greater preference for sites with sparse or intermediate vegetation density [72, 73]. Likewise, it has been found that some fish species avoid shallow waters far from cover or increase their use of cover at lower water depths [74, 75]. Consistently, predatory risk would increase for M. atlanticus, C. undecimalis, and E. smithi, which have relatively large bodies, in coastal lagoons at low inundation levels, as happens during El Niño. In such conditions, they would be easily located by predators. Increased mangrove utilization with larger body sizes and drier conditions has also been found in southwestern Florida for Lutjanus griseus and Haemulon Sciurus, which was attributed an expansion of habitat breadth with ontogeny and to a strategy to avoid predation [6].
The high mangrove utilization values found for E. plumieri agree with its plasticity regarding diet and habitat utilization. During El Niño, in several localities of the CGSM, this species exhibits a slightly higher utilization of mangroves than coastal lagoons [13]. Meanwhile, in the non-estuarine seascapes of Guadeloupe Island, E. plumieri utilizes and feeds in mangroves and seagrasses [26]. Although our records show E. plumieri’s greater preference for mangroves in comparison with coastal lagoons in the Pajarales Complex, this species ranked first and second in density and biomass in the main CGSM lagoon before 1998 [76, 77]. The collapse of oyster banks between 1996 and 2000, leading to that of the bivalve Mytillopsis sallei, the main food source of E. plumieri in coastal lagoons, drove a decline of this species in the system [76]. Currently, E. plumieri ranks fifth and twelfth, respectively, regarding encircling gillnet catch frequency in the main lagoon of CGSM and in the coastal lagoons of the Pajarales Complex. However, despite the decline in dominance, the generalized diet of this species [26, 49] may have favored the utilization of mangroves and its persistence in CGSM.
A. Canteri’s high utilization of mangroves and coastal lagoons is consistent with other studies carried out in the CGSM [13]. The shift in preference from coastal lagoons to mangroves found for larger body sizes is likely associated with the aforementioned predator avoidance strategy. Progressively larger fish are being recorded in mangroves at lower water depths, and smaller fish have been observed in coastal lagoons under drier conditions, suggesting that the former are avoiding coastal lagoons when the water depth is low in order to escape predation. The habitat preference changes of larger A. canteri individuals have also been reported in the Gulf of Urabá, another estuarine system in Colombia [78]. In such reports, the utilization of mangroves was higher in small juveniles (6.5–19.2 cm), which feed on the copepods of R. mangle prop roots, and mangrove utilization by larger body sizes decreased in response to diet shifts. These findings appear to contradict our results. However, it should be noted that assessing habitat utilization by A. canteri fish smaller than 15 cm was not possible in our study, and that the study conducted in the Gulf of Urabá did not evaluate habitat utilization as a function of climate variability or water depth. This suggests that A canteri’s habitat selection is highly dynamic and influenced by dietary shifts and predator avoidance behaviors in mangrove estuarine systems.
The high coastal lagoon utilization of M. incilis, M. liza, and C. mapale found in this work agrees with a study carried out in the CGSM, close to the Sevilla River mouth, albeit only for M. incilis [50], as M. liza, and C. mapale showed a higher utilization of the zones adjacent to mangroves. Such differences could be associated with habitat occupation (M. liza) and habitat reproduction requirements (C. mapale). The Lebranche mullet (M. liza) may be partially occupying the niche of the Nile tilapia (O. niloticus), which exhibited a low catch frequency in the zone adjacent to the mangroves of the Sevilla River mouth (5.7%) but usually dominates this transition zone. In fact, seine nets are employed in this ecotone between mangroves and coastal lagoons to capture Nile tilapia, accounting for 55% of its catch frequency. The similar diets of O. niloticus and M. liza (Table 1) suggest the latter’s high utilization of the coastal lagoons in the Pajarales Complex, as the zones adjacent to mangroves are occupied by the former. On the other hand, mangrove creeks are important reproduction sites for Cathorops species [79], whose habits may explain C. mapale’s high utilization of the zones adjacent to the mangroves of the Sevilla River mouth.
The increasing mangrove utilization by M. incilis and M. liza of larger body sizes under drier ENSO conditions, or the presence of larger fish in mangroves at lower water depths, could be related to a predator avoidance strategy, as explained earlier for M. Atlanticus, C. undecimalis, and E. smithi. Likewise, other observations suggest that predator avoidance is a habitat selection mechanism for M. incilis and M. liza. A relatively high utilization of mangroves by these species was observed in several localities of the CGSM during a moderate to strong El Niño episode [13], suggesting a high utilization of mangroves under low inundation conditions. In addition, fishermen describe M. incilis as moving into mangroves during low tides.
The results obtained, showing C. mapale juveniles’ similar utilization of mangrove and coastal lagoons, in addition to the fact that mainly juveniles are found in mangroves during La Niña phases (S2 Fig), are consistent with reports indicating that mangrove creeks are important reproduction sites for Cathorops species during wet periods [79]. On the other hand, the higher utilization of coastal lagoons by C. mapale under dry conditions agrees with previous findings in the CGSM [13].
Fish in mangroves are, on average, 1.5 cm larger than those in coastal lagoons due to the slightly larger gillnet mesh size used in mangrove habitats. This constantly larger mesh size does not affect the results demonstrating an increase in mangrove utilization during El Niño, nor does it impact the increased utilization of larger fish species in shallow water depths for M. atlanticus, E. smithi, C. undecimalis, A. canteri, M. incilis and M. liza
Habitat utilization by freshwater fish species in response to body size and climate variability
The studied freshwater species are commercially relevant in the CGSM, and several of them are also common in other estuarine environments of the Colombian Caribbean [80–82]. However, with the exception of O. niloticus, the ecology of freshwater fish in tropical coastal lagoons has been less studied in comparison with that of estuarine fish [50, 83]. This work is one of the first to address the cross-habitat utilization of freshwater species within a flood plain lagoon.
The unique presence of O. niloticus in mangroves agrees with previous reports for the CGSM, which indicate its very low utilization of coastal lagoons; the Nile tilapia is more frequent in the ecotone between mangroves and coastal lagoons [50]. Similarly, other Oreochromis species exhibit a higher utilization of the ecotone between vegetation and coastal lagoons, as well as of vegetated habitats compared to unvegetated ones [84]. The use of vegetated littoral zones by Oreochomis species has been linked to seeking protection from predators [85, 86].
The increase in mangrove utilization by C. kraussii of larger body sizes may be related to ontogenetic dietary shifts, not to a predator avoidance strategy, since this species does not show a clear relationship between water depth and higher mangrove utilization by larger individuals. On the contrary, this species changes from an omnivorous diet to a fully piscivore one above 19 cm in the Ciénaga Grande de Lorica, Colombia [87]. We also found that, around the same size, its mangrove utilization increases.
M. muyscorum and P. magdalenae are migratory fish that spawn in main rivers and use coastal lagoon systems as nurseries during rainy seasons [88]. In addition, it has been suggested that these species use coastal lagoons as shelter and feeding areas, but no specific studies have assessed their cross-habitat utilization [83]. The changing habitat preferences of juveniles and adults of M. muyscorum in response to climate variability suggests that both mangroves and coastal lagoons play a role in the species’ reproduction and adult habitats. On the other hand, H. malabaricus has been widely described as a predator species associated with vegetation [89–91]. Our results, showing these three species’ great preference for mangroves, are consistent with previous studies on H. malabaricus and constitute the first report of M. muyscorum and P. magdalenae’s high utilization of mangrove-associated habitats within tropical coastal lagoon environments.
T. magdalenae is an endemic species of the Magdalena River basin that migrates from high to low watershed areas during dry seasons, presumably to reduce its risk of predation [92]. This species has been scarcely studied, and its preference for coastal lagoons has not been reported elsewhere. T. magdalenae has a predominantly zooplanktivorous diet [56], and its substantial utilization of coastal lagoons suggests that zooplankton is primarily exploited in this habitat. On the other hand, it is not clear why individuals of this species, particularly adults, increase their mangrove utilization only during neutral ENSO phases; more studies are necessary to better understand its cross-habitat utilization.
Future studies
The Nile tilapia (O. niloticus) showed a preference for mangroves across all conditions and development stages, yet it is frequently captured in the CGSM’s transition zone between mangroves and coastal lagoons [50], a habitat not addressed in this work. It is relevant for future studies to assess the differential utilization of ecotones by estuarine and freshwater fish species [5].
The high utilization of a habitat does not necessarily indicate trophic utilization, and the fishing gear used in this work was deployed during daytime. Thus, although this study shows several tendencies in the habitat preferences of estuarine and freshwater species, future studies should focus on mechanisms of mangrove utilization. This includes conducting isotope analyses and assessing habitat utilization during nighttime, in order to better understand the entire scope of cross-habitat utilization by CGSM fish species and the mangrove-fishery linkage.
Conclusions
The high values and increments in mangrove utilization by fish species of the Pajarales Complex in the CGSM are related to different mechanisms, not always to the nursery function. Some species exhibit a high or increasing utilization of mangroves, presumably as consequence of feeding plasticity or dietary shifts. On the other hand, the relatively low inundation usually observed during El Niño events increases the risk of predation and, consequently, the utilization of mangroves by larger fish. Therefore, predator avoidance is a key driver of mangrove utilization and habitat selection in the eutrophic-hypereutrophic turbid waters of the Pajarales Complex.
Water depth in the Pajarales Complex is influenced by climate variability fluctuations, but also by seasonal and daily changes in response to fluvial inputs and tides. All temporal scales of water level fluctuations are expected to generate habitat selection responses by fish in deltaic systems to limit predation.
This study’s findings support recent suggestions regarding the importance of conserving and managing habitat complexity in estuarine environments to sustain fish populations [13, 14]. However, the CGSM’s area of fringe and riverine mangroves, which are subject to tidal or fluvial inundation, is only 1.2% of that occupied by coastal lagoons. Thus, protection–and even the expansion–of these key mangrove types is relevant for the management of CGSM fisheries.
Supporting information
S1 Table. Correlation analysis between the intensity of climate variability (evaluated through the ONI), the average body size, and the relative habitat utilization of fish species.
https://doi.org/10.1371/journal.pone.0308313.s001
(DOCX)
S1 Fig. Average salinity and dissolved oxygen ±SE in the Pajarales Complex zones during the ENSO phases between 2001 and 2019.
https://doi.org/10.1371/journal.pone.0308313.s002
(TIF)
S2 Fig. Violin plots of the body sizes of the main estuarine species caught in different habitats across ENSO phases in the Pajarales Complex of CGSM.
M: mangrove, CL: coastal lagoon.
https://doi.org/10.1371/journal.pone.0308313.s003
(TIF)
S3 Fig. Violin plots of the body sizes of the main freshwater species caught in different habitats across ENSO phases in the Pajarales Complex of the CGSM.
M: mangrove, CL: coastal lagoon.
https://doi.org/10.1371/journal.pone.0308313.s004
(TIF)
Acknowledgments
Special thanks to Domingo Rodríguez Julio, a fisherman who shared some of his knowledge on the habits of fish in deltaic environments.
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