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Article

Predation Risk, Foraging and Reproduction of an Insectivore Fish Species Associated with Two Estuarine Habitats

by
Éden Hávila Lima Guedes
,
Juan Alves Pereira
,
Gitá Juan Soterorudá Brito
,
Alexandre da Gama Fernandes Vieira Júnior
and
André Luiz Machado Pessanha
*
Programa de Pós-Graduação em Ecologia e Conservação, Universidade Estadual da Paraíba, Laboratório de Ecologia de Peixes, Avenida das Baraúnas, 351, Bairro Universitário, Campina Grande 58429-500, PB, Brazil
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(11), 707; https://doi.org/10.3390/d16110707
Submission received: 16 October 2024 / Revised: 7 November 2024 / Accepted: 8 November 2024 / Published: 20 November 2024
(This article belongs to the Section Marine Diversity)
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Abstract

:
Pneumatophore fringes and mudflats are extremely valuable habitats and provide structures on which many fish species benefit in terms of food and reduced predation risk. We analyzed the spatiotemporal patterns in feeding habits, reproductive aspects and effects of predatory fish presence to assess the ecological drivers of the common halfbeak, Hyporhamphus unifasciatus, in a Brazilian estuary. Sampling was conducted during the rainy and dry periods. In summary, the results demonstrated that the number of predatory fishes was a strong predictor of population abundance and biomass, followed by pneumatophore complexity. The abundance and biomass values tended to increase with increasing habitat structural complexity towards the upper estuary. There was evidence that fish exhibited movement during the rainy season related to spawning events and subsequent juvenile recruitment in this area. Hymnoptera was the item most frequently ingested and made the greatest contributions to the volume of diet in habitat types throughout the year. There was an increase in the condition factor in the rainy season, which was associated with energy reserves, reproduction and growth (fitness). We concluded that predation is an important ecological process that operates at local spatial scales and that, together with the density of pneumatophores, it could affect the abundance of common halfbeak populations associated with estuarine habitats.

1. Introduction

Estuarine fishes are closely associated with multiple habitat types in tropical estuaries, comprising vegetated (e.g., mangrove, seagrass meadows and saltmarsh) and unvegetated habitats (e.g., mudflat and sandflat) [1,2]. This habitat heterogeneity exerts a major influence on the species in estuarine regions, increasing diversity and species [3]. Habitat features, including substratum composition, water conditions [4] and presence and type of vegetation [5], influence the distribution and abundance of fish species. Each habitat feature influences the way in which fish exploit resources for food, and for spawning sites and/or refuge [6,7]. Previous studies have also highlighted how heterogeneous environments offer more habitat types and niches, thereby allowing more species to coexist in ecosystems [8,9].
Associations of fishes have been studied extensively in mangrove root systems [10,11] and seagrass meadows [12,13], showing these habitats to contain abundant food resources and to possess characteristics that could reduce the interaction rate between predator and prey [6,14]. Additionally, the foraging efficiency and reproductive success of most fishes change with growth. These differences vary from species to species and, in many cases, are often associated with changes in habitats [15]. In addition, habitat selection for feeding or refuge by fish species has implications for maximizing energy intake and enhancing growth, size distributions and survival rates. Other authors have indicated that the habitat requirements for the estuary-dependent juvenile phase may be quite different when compared to the adult stage of the fish life cycle [1,5].
The pneumatophore fringes of mangroves and mudflats are important habitats that extend into the intertidal and subtidal zones, and are regularly flooded with seawater. In particular, pneumatophores attract juvenile fish due to structural complexity, the lowest predation risk, and high food availability of epiphytic algae and associated invertebrates on their surface area [16,17]. As such, these shallow habitats function as important nursery grounds for fishes in tropical estuaries [15,18]. Habitats may also provide potential refuge from predators for small fishes by reducing prey visibility and limiting the movements of large predators [17,19].
Fishes of the family Hemiramphidae, commonly known as halfbeaks, are epipelagic and inhabit shallow, estuarine and freshwater environments [20]. The common halfbeak Hyporhamphus unifasciatus, one the most abundant fish species [21,22], is a small marine fish (length, TL = 300 mm) [23], characterized by a lower jaw that is much longer than the upper jaw [24]. The species is distributed along the Western Atlantic, from Florida southward through the Caribbean to Uruguay [25]. This species is restricted to coastal habitats such as seagrass beds, tidal creeks and beaches [26], where they feed as generalist to more specialized guilds (e.g., herbivores and insectivores) [11,22]. The common halfbeak is an important resource in many fishing communities due to its abundance and economic value [27,28]. This species is mostly captured in gillnets and beach seines by artisanal fishers, and today is considered overexploited along the Brazilian coastline [29].
To compare how two shallow-water habitat types may affect distribution and abundance for the common halfbeak, changes in diet in juveniles and adults on a temporal scale were first investigated. Next, we tested whether common halfbeaks preferentially inhabit close pneumatophore fringes, such that they are suitable areas for growth because they maximize the condition factor (proxy of energy reserves in the fish body), and that predators would affect abundance. We predicted that density and distribution of fish populations are strongly related to areas with the presence of pneumatophores (used as a proxy for complexity) due to abundant food resources and predation.

2. Materials and Methods

2.1. Study Area and Sampling

This study was conducted on the Mamanguape Estuary (6°43′02″ S 35°67′46″ W) situated on the Brazilian northeastern coast. This estuary is fringed by a dense mangrove forest of c. 6000 ha [30]. Prop roots, pneumatophores and mudflats are usually found at the outer edges of a fringe or bordering tidal creeks and channels [27,31]. In this region, Köppen classifies climate as A-type (hot and humid) [32]. Annual rainfall ranges from 1750 to 2000 mm, and the average temperatures hover around 26 °C [33]. The tide occurs in semi-diurnal tidal regimes, with the mean tidal amplitude varying from 0.2 m (low water) to 2.7 m (high water) [31].
Two habitats of the estuary were considered in this study: (1) the intertidal-adjacent Avicennia–Laguncularia pneumatophore fringe that can extend away from the mangrove forest, and (2) the unvegetated mudflat extending 50 m seaward of the pneumatophore fringe. Monthly sampling was conducted in the estuary in 2016: January to July—rainy season and August to December—dry season (except in September due to inclement weather). Fish were collected with three fike nets, set and retrieved approximately 2 to 3 h before and after mean high water, positioned parallel to mangrove fringe so that the opening (and wings) faced landward in each site. Additionally, a beach seine (10 m × 1.5 m; 8 mm mesh size) was hauled parallel to an extension of approximately 30 m and to a maximum depth of 1.5 m, during the low tide. The sampling unit was standardized with three replicates in an effort to capture individuals that use the area. In the laboratory, the fish caught were measured—total size (mm) and weight (g). In order to better characterize the habitat structure of pneumatophores, sampling was performed at different sites along of estuary whenever possible. Three random quadrats of 25 × 25 cm were set on each site along a mangrove forest. In the quadrats we quantified the density of pneumatophores.

2.2. Abundance and Spatial Distribution of Common Halfbeak

Abundance and biomass of common halfbeak were analyzed separately using a univariate statistics (PERMANOVA) (with 9999 permutations) to test for spatial and temporal changes, and applied on two factors: habitat (two fixed levels: pneumatophore fringes and mudflats) and season (two fixed levels: rainy and dry). A resemblance matrix of data was calculated using Euclidean distance. The variables were log-transformed. The log transformation reduced or removed the skewness of original data. Significant factors were further analyzed using a PERMANOVA pair-wise comparison. The analyses were performed using PRIMER v6 + PERMANOVA [34,35].

2.3. Reproductive Data and Condition Factor (K)

Gonads were macroscopically examined, and reproductive stage was described [36]. The gonads of each individual were removed, when possible, and weighed (in g). The gonadosomatic index (GSI) is a good indicator of reproductive activity and was calculated for individuals using the formula: GSI = Weight of gonad/Weight of fish × 100 [37]. Common halfbeaks were categorized into size classes: juveniles (<144 mm) and adults (>145 mm) [21].
To assess the variation in condition factor of the common halfbeak from both estuarine habitats, we used a Fulton’s condition factor (K). Individual values of the condition factor were obtained through the formula K = 100 Wt/Lt3 where Wt is total wet weight (mg) and Lt is the total length (mm) [38].
To investigate the distribution of the length frequency, common halfbeak individuals were grouped into 10 mm TL size classes by months, and their recruitment pattern was estimated.

2.4. Gut Content and Diet Analysis

The gut contents of each individual were removed and examined under a stereomicroscope and each dietary item was identified. To analyze the diet, frequency of occurrence (O%) and volumetric (V%) percentages were calculated to characterize the diet [39], and were then used to calculate the Alimentary Index (IAi) [40], presented in percentages. The volume of each item was calculated and analyzed by displacement methods [41]. The method consisted of the estimation of volumetric proportion of each item, and the volume of each item was then calculated based on the total volume of food eaten per consumer. Empty stomachs were excluded from the analysis.
A permutational multivariate analysis of variance (PERMANOVA) (with 9999 permutations) was used to examined variations in volumetric contributions of prey items, and applied to three factors: habitat type (two fixed levels: pneumatophore fringes and mudflats), season (two fixed levels: rainy and dry) and size (two fixed levels: juvenile and adult). A resemblance matrix of data was calculated using Bray–Curtis coefficients. The variables were square-root-transformed. Where a significant difference (p < 0.05) was detected for the factor habitat, post hoc tests were conducted. All analyses were performed using the statistical package PRIMER v6 + PERMANOVA [34,35].

2.5. Predatory Fishes

In order to clarify the abundance of common halfbeak, the predatory fish abundance was estimate in both habitats. Predatory fish species in habitat types were chosen on two criteria: (1) carnivorous with tendency to piscivory, and (2) predator fishes which live in the water column or close to the water surface. The classification of fish species as piscivores was based upon published dietary data from a preliminary study conducted at the estuary [5,11,42]. Fourteen species were recorded: jacks (Carangidae: Caranx latus and C. hippos), snooks (Centropomidae: Centropomus paralellus, C. undecimales, C. ensiferus and C. pectinatus), snappers (Lutjanidae: Lutjanus alexandrei, L. analis, L. apodus and L. jocu), randalls soap (Serranidae: Rypticus randalli), barracuda (Sphyraenidae: Sphyrena barracuda) and needle fishes (Belonidae: Strongylura timucu and S. marina). Additionally, to analyze the influence of predatory fishes on abundance of common halfbeak, abundance of predators was expressed by pooling and combining the number of individuals into family groups in each habitat and season. We also used the t-test to examine the hypothesis of no difference in number of predatory fish species between habitats during in each season.
A multiple regression analysis with number of predatory fishes and habitat structure of pneumatophores as predictors and abundance and biomass of Hyporhamphus unifasciatus as response variables was performed [43]. These data were checked for multicolinearity, normality and homogeneity of variance and were log-transformed, log10(x + 1), to meet the assumptions of multiple regression. We performed hierarchical linear regression analysis: In step 1, the number of predatory fishes as the predictor variable was used because it was assumed to explain a statistically significant amount of variance in fish distribution. In step 2, structure of pneumatophores was added. The analysis were performed using the statistical package SPSS.

3. Results

3.1. Abundance and Spatial Distribution

A total of 534 common halfbeak were caught, totaling 1466.66 g. The pneumatophore fringes showed the highest number of individuals and biomass compared to the mudflat (Figure 1). Seasonally, higher values for the number of individuals and biomass were recorded during the rainy period. Statistically, the spatial effect was, overall, not significant on the number of individuals (pseudo-F2,82 = 0.75; p > 0.001) or biomass (pseudo-F2,82 = 0.04; p > 0.001). Significant differences were found between seasons for both the number of individuals and biomass. However, the interaction effects were not significant between habitat types and seasonal factors (number of individuals: pseudo-F2,82 = 0.20 and biomass: pseudo-F2,82 = 0.26; p > 0.001).
The monthly length–frequency distribution of common halfbeak ranged from 15 to 180 mm TL. Monthly observations showed that the percentages of this species tended to increase during the rainy season (from April to July), with principally large-size individuals observed (Figure 2). The percentages of small-size classes (<100 mm TL) showed the reverse trend, occurring in higher abundance in the dry season (from October to December) (Figure 2).

3.2. Reproductive Data and Condition Factor (K)

In the estuary, two periods of reproductive activity were observed in our study (Figure 3). The first period matched the beginning of the rainy season, but a peak of mature females was registered in July, suggesting that individuals spawn in this season. In the second period, starting in the dry season in approximately October, there were fewer mature females apparent, and the peak of mature females occurred in January (see pneumatophore fringe). The changes in the gonadosomatic index (GSI) of the males showed the same pattern for both habitats, and the values tended to be relatively lower than those of the females (Figure 3).
The condition factor (K) for all fish samples was determined by month and did not reveal similar patterns when compared to habitats), showing the highest values in mudflat (Figure 4). However, there was some indication that the condition factor values for common halfbeak slightly decreased during the dry season in both habitat types.

3.3. Diet

For the diet study, 311 stomachs with prey were analyzed from common halfbeak, of which 41 stomachs were empty (13.2%). In general, common halfbeak fed on prey items that fell onto the water surface (Table 1). In this case, the diet was comprised mainly of insects, which accounted for more than 97% of the overall IAi in juveniles and adults in both habitat types. Although plant material, copepods and other insects were frequently consumed, they were only present in small volumes.
No significant differences in the dietary compositions of common halfbeak were found between habitat types (PERMANOVA: pseudo-F1,245 = 1.87, p > 0.05) and seasons (PERMANOVA: pseudo-F1,245 = 1.13, p > 0.05), which was attributed to the consumption of Hymenoptera throughout the year in the estuary. Significant differences in diet were found among size classes (PERMANOVA: pseudo-F1,245 = 3.13, p < 0.001). The interaction effects were significant between size and seasonal factors (PERMANOVA: pseudo- F1,245 = 3.52; p < 0.001).

3.4. Effect of Presence of Predatory Fish Species

Predatory fishes were present during the whole study period, with jacks and snooks the main species in estuarine habitats, accounting for more than 70% of the species sampled (Figure 5). Jacks and snooks were best represented in terms of abundance in the rainy and dry seasons, respectively. Snappers were abundant (range 7–15%) in mudflats during the dry season and pneumatophore fringes during the rainy season. Randall soap fish, needle fish and barracuda occurred in low numbers in both habitats during the study (Figure 5).
The analysis showed that the abundance of predatory fishes was not significantly different between habitats (t = 9.085; p > 0.01). Unlike spatial abundance, however, there was a significant difference in the abundance of predatory fishes within each habitat during the seasons (lower: t = 12.184; p < 0.01; upper: t = 29.685; p < 0.01).
The hierarchical multiple regression model results showed that the abundance of predatory fishes and habitat types were significant predictors of variations in the abundance and biomass of common halfbeak, as evidenced by the consistent increase in R2 in each step (Table 2). The number of predatory fishes was significantly negatively related to abundance (β = −0.554; p < 0.01) and biomass (β = −0.462; p < 0.01) and explained 30.7% and 21.4% of the variance in the model, respectively. Pneumatophore fringes were significantly related to abundance (β = 0.180; p < 0.01) and biomass (β = 0.223; p < 0.01) and explained 4.7% and 6.1% of the variance in the model, respectively (Table 2).

4. Discussion

Our results demonstrated that the increased habitat structure, provided by pneumatophore fringes, had the strongest association with habitat selection for common halfbeak. This habitat constitutes important sites for this species to complete its life cycle, as spawning and foraging habitats, because both juvenile and adult life stages are caught in this kind of habitat. Apparently, there is some evidence that fishes move to pneumatophore fringes during the rainy season to spawn and are subsequently recruited in this area. The results also indicated that common halfbeaks altered their habitat use on a seasonal basis during the rainy season. Hyporhamphus unifasciatus showed higher abundance in pneumatophore fringes during this period, which could be a consequence of biotic interactions (predation) and spawning periods. Therefore, the structure of the pneumatophores supported the high biomass of common halfbeak that use these areas for reproduction, growth and development in this tropical estuary. Notably, the differences in the distribution and abundance of common halfbeak were determined by complex responses to habitat characteristics and biotic interactions and offer insights into how habitat use can influence fitness.
In terms of the number of individuals and biomass, the multiple regression model revealed a positive correlation related to pneumatophore presence. In this case, the pneumatophore fringes attracted halfbeak because suspended habitats in the water column increased foraging and shelter opportunities and consequently increased the survival of individuals. In this study, support for the predator refuge hypothesis exists because there are a greater number of refuges for fishes in pneumatophore fringes than in adjacent habitats, such as subtidal deeper areas or non-vegetated mudflats [11]. In fact, these results were consistent with the results of previous studies that highlight that pneumatophore density can affect the abundance of fishes [14,44]. For example, MacKenzie and Cormier [45] reported that the vertical structure and arrangement provided by the height of the pneumatophores that emerge from sediment often produce a dense structure impenetrable by larger organisms. According to Green et al. [44], because the structure is more complex, small fish such as halfbeak might also show higher maneuverability and motility for exploitation of this habitat for feeding during high tides. Some studies have indicated that the arrangement of pneumatophores is also responsible for creating shade for fish species to hide between structures [46,47]. From another perspective, the pneumatophore arrangement supports trapping of sediment and organic matter and directly influences prey availability [48]. Together, these factors are considered important contributors to the increased attraction of fish to mangroves [9].
The populations of common halfbeak found in each estuarine habitat also responded differently to the seasonal conditions in different ways, and these shifts may be in response to predation risk: in pneumatophore fringes, the higher abundance and biomass of predatory fishes were registered during the rainy season, while in mudflats, they were registered during the dry season. The number of predatory fishes was a strong predictor of population abundance and was confirmed by the multiple regression model. From this work, there was a vast difference in abundance of Jack and Snook species among habitat types, and this appeared to indirectly affect abundance of common halfbeak around pneumatophore fringes. Clearly, these temporal pattern differences among habitats reflect natural variability in baseline habitat quality, where the structure of pneumatophores likely provided additional resources that allowed for greater abundance. Rilov et al. [49] suggested that the quality of a habitat was linked to predation risk. These results are consistent with those of MacKenzie and Cormier [45], who describe the same pattern for fish species in reefs and seagrass beds, respectively. This was not surprising at first because species presumably move to sites in response to foraging efficiency and capture rate [13].
In particular, it is also important to recognize here that during the rainy season, when there was an increase in predatory fishes and prey fishes in pneumatophore fringes, the main predators in this area (jacks and snappers) were small in size or juveniles. In many instances, however, the potential predation risk might be affected by the apparent presence of juvenile predatory fishes and thus induce changes in prey behavior leading to adjustments in refuge use and spatial distribution [50]. It is possible that the intensity of predation will be influenced by opportunistic attacks of the interspecific schooling of piscivorous juveniles when fish are concentrated in the pneumatophore fringes. Studies showed that intraspecific schools were an important factor in the aggregation effect in foraging behavior of juvenile predatory fishes [51,52]. Sancho [53] examined another aspect of predation by juveniles. The author found a “midwater” hunting behavior consisting of midwater high-speed attacks on spawning fishes in reefs and, therefore, this may be considered an important behavior in carangid species.
Findings in diet composition in our study showed some differences compared with the results of previous studies. Common halfbeak is commonly regarded as an herbivorous fish, and plant material forms a very significant part of its diet [54,55]. The small amount of animal prey found in gut contents may be partly considered to be incidentally ingested during herbivory, as suggested by Mackenzie and Cormier [45]. The present study, however, found that both juveniles and adults preyed primarily on Hymnoptera, which were widely abundant in fish occupying both habitats. Campos et al. [42] also found that common halfbeak fed mainly on Hymnoptera prey and suggested that this species was characterized as an insectivore in the Mamanguape Estuary. Studies of other Hemiramphidae species also described insects as main food resources, especially for the diet of larger individuals, which tended to be dominated by terrestrial insects [56,57]. Indeed, clearly, common halfbeak utilized allochthonous food items (terrestrial insects), which is very useful information for assessing its potential interactions with local food webs [15].
No clear trend in the quantitative and qualitative dietary constituents could be observed between habitats and seasons. In fact, Hymnoptera species were found in very high abundance in gut contents. Most likely, they constitute a very abundant food resource that may be easily collected provided that fish display adequate behavior to access the item. The prey encounter rate is dependent on the abundance of that prey in the environment [58]. Hymnoptera have been widely documented and are often regarded as the most abundant insect group in mangroves [59,60]. Additionally, these preys also fall from the mangrove forest in the surface layers of the water and are sequentially detected and captured by common halfbeak. The pronounced foraging tactic of common halfbeak to target prey (Hymnoptera) is similar to the registered by Delabiel et al. [59], and is thus presumed to be related to the presence of insects on the seawater surface. This behavior has been registered by other Hemiramphidae across different habitats [57,61], where insects were ingested in proximity to floating objects or sucked from the water surface [56].
The combination of both a lower number of individuals and non-spawning females in the mudflats during the rainy season might suggest that the adults migrate to spawning grounds located in pneumatophore fringes. According to Fowler et al. [62], these spawning-related individuals in the Hyporhamphus genus constitute an important part of the life history of these schooling species. The use of structured habitats, for example, seagrass and mangroves, is closely associated with habitat specifics for spawning, possibly because they represent substrates for egg attachment and increased reproductive success in the case of Hemiramphidae [20]. Large eggs with adhesive filaments are characteristics shared among many of the other members of this family [63,64]. Therefore, fish may utilize habitats such as resting areas to conserve energy before spawning and between spawning events [65]. We suggest that the peak of the spawning period during the rainy season, confirmed by the GSI data of females, is driven by three explanations: seasonal changes in predatory fishes, low turbidity linked to rainfall and the presence of young halfbeak caught in the early dry season (see October for young-of-the-year records). The hypothesized lower predation pressure in pneumatophore fringes during these seasons potentially reduces the risk of large nutritious eggs in the halfbeak [62,64], while the spawning strategy registered during the period of more turbid waters in the Mamanguape Estuary can minimize visual predation on eggs and increase survival. This spawning strategy has also been registered for Hyporhampuhus melanochir and other hemiramphids in Australia [20], and other studies have reported larvae and small juveniles using areas upstream of estuaries related to the lowest salinity in this area [66]. Therefore, spawning during the rainy season maximizes the potential for eggs to be transported because of the high flow of rivers [67]. In the current study, the short spawning period was registered during the dry season, related to higher GSI data in mudflats and recruits that occurred from January to February. Here, water temperature may also have been an important factor in the spawning season because of influences on the metabolic demands of fishes. Water temperature has been identified as a fundamental factor that can influence fish reproduction and growth in tropical estuaries [68,69].
The condition factor (K) showed that the two habitat types were not equally valuable for common halfbeak, especially when comparing their seasonal patterns. Our results demonstrated significant influences of habitat use on the condition factor in the rainy season, and this was important for predicting that energy storage was allocated to growth and survival [70]. Therefore, the condition factor may act to predict the fitness of fishes. Furthermore, pneumatophore fringes provided the best environment because they exhibited favorable conditions for rapidly growing juvenile fish and maximized reproductive fitness. Our results were in accordance with this hypothesis. In this study, the relationship between the condition factor (K) and gonadal development had greater importance in influencing this index. Similar results were reported for Atherinella brasiliensis in this estuary, indicating that habitats that differ in food resources can offer the opportunity to maximize the fitness [71].
In conclusion, this study clearly demonstrates that configuration of habitat is an important determinant of abundance patterns in space and time of common halfbeak populations associated with estuarine areas. The structure of these habitats, represented by pneumatophores, may contribute to these patterns due to the greater habitat complexity providing shelter from predation, increased microhabitat availability and abundant food. This is consistent with the attractiveness hypothesis for fishes in mangrove areas, which suggests that fishes select habitats because of increased food supply, and increased living space or shelter [72]. Several conclusions from this study may prove to be generally applicable in other systems, principally related to predation risk and utilization of food resources in shallow coastal ecosystems. Further investigations based on an ecosystem perspective are needed to understand how the availability of allochthonous food items can supply energy and materials to estuarine food chains and coastal marine ecosystems. The present contribution has brought forward important results for improving the management of suitable estuarine habitats and the maintenance of biodiversity.

Author Contributions

Conceptualization, É.H.L.G. and A.L.M.P.; methodology, É.H.L.G.; formal analysis, A.L.M.P.; investigation, G.J.S.B., É.H.L.G. and A.d.G.F.V.J.; writing—original draft preparation, G.J.S.B., É.H.L.G. and J.A.P.; writing—review and editing, É.H.L.G. and A.L.M.P.; supervision, A.L.M.P. All authors have read and agreed to the published version of the manuscript.

Funding

Financial support was provided by the National Counsel of Technological and Scientific Development (CNPq; Grant# 308340/2018-3). This study was funded by EDITAL N° 18/2020-FAPESQ/CAPES/Termo de outorga n° 047/2021.

Institutional Review Board Statement

This study was conducted under SISBIO Collection of Species Permit number 24557-27/10/2010 issued by ICMBio, Brazilian Environmental Agency, and follows the ethics rules which regulate the scientific use of animals in Brazil (Federal Law 11.794 of 8 October 2008).

Data Availability Statement

All data are included in the article.

Acknowledgments

We thank students of the Laboratory of Fish Ecology (UEPB) for helping in both the laboratory and the field.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Spatial and temporal variation in the number of individuals and biomass of Hyporhamphus unifasciatus caught in mudflat and pneumatophore fringes of the Mamanguape Estuary.
Figure 1. Spatial and temporal variation in the number of individuals and biomass of Hyporhamphus unifasciatus caught in mudflat and pneumatophore fringes of the Mamanguape Estuary.
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Figure 2. Monthly length–frequency distribution of Hyporhampus unifasciatus in the mudflat and the pneumatophore fringes between January and December 2016. n = number of fish.
Figure 2. Monthly length–frequency distribution of Hyporhampus unifasciatus in the mudflat and the pneumatophore fringes between January and December 2016. n = number of fish.
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Figure 3. Monthly values of the gonadosomatic index (mean GSI± standard error) with female and males Hyporhamphus unifasciatus caught in the mudflat and the pneumatophore fringes of the Mamanguape Estuary between January and December 2016.
Figure 3. Monthly values of the gonadosomatic index (mean GSI± standard error) with female and males Hyporhamphus unifasciatus caught in the mudflat and the pneumatophore fringes of the Mamanguape Estuary between January and December 2016.
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Figure 4. Boxplot of monthly values of the condition factors of Hyporhamphus unifasciatus in mudflat (A) and pneumatophore fringes (B) of the Mamanguape Estuary between January and December 2016. Bold lines indicate medians, hinges indicate the 25th and 75th percentiles.
Figure 4. Boxplot of monthly values of the condition factors of Hyporhamphus unifasciatus in mudflat (A) and pneumatophore fringes (B) of the Mamanguape Estuary between January and December 2016. Bold lines indicate medians, hinges indicate the 25th and 75th percentiles.
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Figure 5. Relative abundance and abundance (mean number of individuals ± standard error) of predatory fishes caught in mudflat and pneumatophore fringes of the Mamanguape Estuary between January and December 2016.
Figure 5. Relative abundance and abundance (mean number of individuals ± standard error) of predatory fishes caught in mudflat and pneumatophore fringes of the Mamanguape Estuary between January and December 2016.
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Table 1. Alimentary Index (IAi%) of food items consumed by juvenile and adults of Hyporhamphus unifasciatus among habitats (mudflat and pneumatophore zones) in Mamanguape Estuary (O% = frequency of occurrence, and V% = volume percentage).
Table 1. Alimentary Index (IAi%) of food items consumed by juvenile and adults of Hyporhamphus unifasciatus among habitats (mudflat and pneumatophore zones) in Mamanguape Estuary (O% = frequency of occurrence, and V% = volume percentage).
MudflatPneumatophore Fringes
Juvenile (n = 39)Adult (n = 33)Juvenile (n = 96)Adult (n = 143)
Food ItemsO%V%IAi%O%V%IAi%O%V%IAi%O%V%IAi%
Foraminifera 1.200.020.01
Diatoms 1.200.020.010.833.200.06
Trematoda5.60.20.016.670.120.038.430.220.037.440.300.05
Sipuncula 6.020.370.044.130.220.02
Errantia Polychaeta 1.200.430.017.443.320.55
Sedentary Polychaeta 0.830.290.01
Copepods8.30.40.0516.670.610.429.640.470.086.610.130.02
Gammaridae 1.650.11
Cyprid larvae 1.200.020.010.830.01
Brachyura larvae 6.670.200.061.201.870.040.830.01
Brachyura 3.330.980.14 0.830.10
Tanaidacea 1.200.020.01
Hymenoptera88.970.599.856.6741.8998.0884.3467.1797.7477.6956.1397.33
Coleoptera2.80.30.01 1.200.020.011.650.120.01
Diptera 13.330.160.092.410.950.044.961.010.11
Hemiptera 6.021.340.142.480.160.01
Plant material13.90.50.1020.001.391.1519.285.651.889.928.281.83
Table 2. Results of the hierarchical multiple regression models computed on both number of individuals and biomass the Hyporhamphus unifasciatus of two groups of predictor variables. Significance: ** p value < 0.01.
Table 2. Results of the hierarchical multiple regression models computed on both number of individuals and biomass the Hyporhamphus unifasciatus of two groups of predictor variables. Significance: ** p value < 0.01.
Number of IndividualsBiomass
Predictor VariablesModel 1(β)Model 2(β)Model 1(β)Model 2(β)
Predatory fishes (abundance)−0.554 **−0.526 **−0.462 **−0.423 **
Pneumatophore complexity
Density 0.228 ** 0.287 **
R20.3070.3470.2140.275
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Guedes, É.H.L.; Pereira, J.A.; Brito, G.J.S.; Júnior, A.d.G.F.V.; Pessanha, A.L.M. Predation Risk, Foraging and Reproduction of an Insectivore Fish Species Associated with Two Estuarine Habitats. Diversity 2024, 16, 707. https://doi.org/10.3390/d16110707

AMA Style

Guedes ÉHL, Pereira JA, Brito GJS, Júnior AdGFV, Pessanha ALM. Predation Risk, Foraging and Reproduction of an Insectivore Fish Species Associated with Two Estuarine Habitats. Diversity. 2024; 16(11):707. https://doi.org/10.3390/d16110707

Chicago/Turabian Style

Guedes, Éden Hávila Lima, Juan Alves Pereira, Gitá Juan Soterorudá Brito, Alexandre da Gama Fernandes Vieira Júnior, and André Luiz Machado Pessanha. 2024. "Predation Risk, Foraging and Reproduction of an Insectivore Fish Species Associated with Two Estuarine Habitats" Diversity 16, no. 11: 707. https://doi.org/10.3390/d16110707

APA Style

Guedes, É. H. L., Pereira, J. A., Brito, G. J. S., Júnior, A. d. G. F. V., & Pessanha, A. L. M. (2024). Predation Risk, Foraging and Reproduction of an Insectivore Fish Species Associated with Two Estuarine Habitats. Diversity, 16(11), 707. https://doi.org/10.3390/d16110707

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