Trophic niche partitioning among non-native fish species coexisting in a high Andean reservoir

doi:10.21203/rs.3.rs-2444081/v1

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Trophic niche partitioning among non-native fish species coexisting in a high Andean reservoir

https://doi.org/10.21203/rs.3.rs-2444081/v1

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published 01 Feb, 2024

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The arrival of a non-native species to a new environment threatens local biological diversity, causing instability in the functioning of the ecosystem. The adverse ecological effects caused by these species have been scarcely documented for the Magdalena basin. By studying predator-prey interactions, we characterized the trophic niche of three non-native species (Micropterus salmoides, Oncorhynchus mykiss, and Cyprinus carpio) that dominate a high Andean reservoir in the Magdalena basin. To understand whether non-native species are preying on native fish, or if they present specific feeding behaviors that facilitate their establishment in lentic environments, we evaluated the diversity of the prey they consume, their feeding strategy, and possible differences in the feeding scheme. Forty individuals were analyzed, and twenty categories of prey were identified for these species. The consumed prey corresponds to the native biota; however, no native fish were found in the stomach contents evaluated. The diversity of prey consumed is similar amongst species, however, M. salmoides behaves like an important predator, as it consumes a larger amount of prey. We observed that the variation in diet composition amongst the non-native species is different, which favors their coexistence as it reduces the competition amongst them. Analyzing the type of diet of this non-native fish is a useful tool that provides a description of some trophic interactions in this aquatic environment. Our results contribute information on the existing interactions amongst non-native species to the Magdalena basin, which is important for the development of strategies to manage and promote impact mitigation.

habitat fragmentation

species introduction

response to environmental change

species interactions

Magdalena River basin

Species introduction is increasingly recognized as an important contributor to the risk of extinction of local species (Jeschke et al. 2014; Villéger et al. 2015), and the loss of species around the world (Clavero and Garcia Berthou 2005; Vitule et al. 2009). The arrival of non-native species to new environments threatens the native biological diversity (Vitule et al. 2009), and various ecological affectations are associated to the introduction of fish, such as predation, increased competition for resources, hybridization, and disease transmission; this allows for potentially “harmful” interactions with native species and may even affect the functioning of the ecosystem (Gozlan et al. 2010; Cucherousset and Olden 2011). The adverse ecological effects that non-native species cause in the Magdalena River have been scarcely documented (Jiménez-Segura et al. 2016). In this Andean region, introductions are related to anthropic activity and may occur accidentally or intentionally as a result of recreation, aquaculture, sport fishing, biological control, river transposition (Lasso et al. 2020), amongst other activities.

The potential establishment of these species in new locations throughout the basin is closely related to the existing similarity between the environmental conditions of their place of origin and the new environments being colonized (Castellanos-Mejía et al. 2021). In addition, it may be associated with the different perturbation processes (Jiménez-Segura et al. 2016). For example, changes in the connectivity of rivers generated by the construction of dams for hydroelectric power are a key factor contributing to the establishment of these new species in the modified environment (Jiménez Segura et al. 2014); in many cases, non-native species have been reported for this region before the water bodies fragmentation (Rodríguez 1984). Then, the fragmentation of the rivers isolates the bodies of water and generates new environments allowing ecological and behavioral changes in the native species, besides physiological problems, loss of genetic diversity, and habitat deterioration (Arantes et al. 2019; Restrepo-Escobar et al. 2021). The new habitat conditions modify fish distribution (Martínez-Toro et al. 2022; Valencia-Rodríguez et al. 2022; Restrepo-Santamaria et al. 2022b), and increase habitat homogenization, which benefits opportunist invaders (Vitule et al. 2012). Other characteristics that increase a species’ invasion potential are its reproductive strategies, prolonged life expectancy, physiological tolerance, a generalist feeding strategy, and trophic plasticity (Lasso et al. 2020).

A means of characterizing biological invasions is knowing the trophic interactions for the species in its new environment (Cucherousset and Olden 2011). Successful invaders tend to have relatively broad trophic niches or ones that are different from other species in the receptor community (Herbold and Moyle 1986), thus enabling them to use trophic resources unexploited by the other species (Araújo et al. 2011). It has been reported that predation and increased competition for resources caused by invader fish lead to a decrease in native fish diversity in an aquatic environment (Pelicice and Agostinho 2009; Pereira and Vitule 2019). Therefore, identifying the competition and distribution of food resources (i.e., trophic niche) of the species that coexist in a reservoir is a fundamental component to understand the community structure as well as the ecological functions that the organisms can perform in the modified environment (Bezerra et al. 2018; Restrepo-Santamaria et al. 2022a).

Non-native species have been observed in the area of influence of the Riogrande II reservoir, such as black bass Micropterus salmoides (Lacepède 1802), rainbow trout Oncorhynchus mykiss (Walbaum 1792), and the common carp Cyprinus carpio (Linnaeus 1758), which are predominant in lentic environments (i.e., reservoir), whereas in lotic environments (i.e., rivers and tributary streams) the assemblage is principally made up of small native species (Martínez-Toro et al. 2022). The dominance of non-native species and the absence of native species in lentic environments leads us to ask whether non-native species are preying on the native fish or if they present specific feeding behaviors that facilitate their establishment in lentic environments. Based on the trophic differences, they would be expected to occupy the same aquatic environment without apparent competition for food resources. A growing understanding of trophic interactions in non-native species will make it possible to make suggestions that contribute to the management of these species in the aquatic environments of the Colombian Andes (Jiménez-Segura et al. 2016).

2.1. Study Area

Riogrande II reservoir is located in the mountainous region of the basin of the Magdalena and Cauca Rivers at 2,267 m above sea level (masl) (Fig. 1). Temperatures in the region range from 12 to 18 degrees Celsius (°C), with an average annual rainfall of 1,324 mm.; humidity reaches averages near 83% between October and November (Mazo-B. et al. 2015). The reservoir has multiple uses, as it provides drinking water as well as hydropower. It has depths of 35 to 45 m, holds 253 million m³ and floods 1,100 ha; it has an average retention time of 73 days, and its turbid waters have a good chemical quality with total dissolved solids of 18 mg/l (Mazo-B. et al. 2015).

2.2. Sampling Design

Samples were taken in August and October of 2020 at four sites within the reservoir. Fish were captured using three gill nets (each net was 100 m long and 3 m high) at each site; each net had ten mesh sizes (1–10 cm between opposite knots) to increase the probability of capturing various sizes and species. Nets were placed near the shores and, due to safety measures regarding access to the reservoir, they were placed for six hours, from 7:00 to 13:00. The three non-native species captured were M. salmoides, O. mykiss, and C. carpio, which were anesthetized with eugenol (Javahery et al. 2012); they were then sacrificed, and their stomachs were removed for further analysis in the lab. Only stomachs containing food were considered for analysis. Stomach contents were observed using a stereoscope and an inverted microscope; then food was classified into categories, and the lowest possible taxonomic resolution was identified.

2.3. Data Analysis

Percentage of occurrence and volumetric index were estimated for each item found in the sample of the diet of each species (Hyslop 1980). The frequency of occurrence was defined as the number of stomachs containing a prey item, divided by the total number of stomachs of the specific predatory species and expressed as a percentage (%) (Hyslop 1980). Volumetric analysis was estimated directly and indirectly. When estimating directly, the displacement of each type of food or group of food selected from the stomach contents was measured in a graduated cylinder, where the volume of displacement was equal to that of the food (Hyslop 1980). Indirect volumetric analysis was estimated comparing food with blocks of an identified volume in accordance with the shape of the organism to be measured (Hyslop 1980).

The diversity of the prey consumed by the species evaluated was calculated using the effective number of species or Hill numbers (q0, q1, and q2) (Hill 1973), following the method proposed by Jost (2006) and Chao et al. (2014). First-order richness or effective richness is q = 0, which takes into account the amount of prey identified for each species regardless of its frequency of occurrence; the estimator q = 1 which is equal to the exponent of Shannon diversity and is sensitive to the prey with low or medium frequency of occurrence (i.e., common prey), and the diversity order q = 2, which equals the inverse value of the Simpson index and has more sensitivity to prey with greater frequency (i.e., dominant prey) (Jost 2006). To evaluate the representativeness of the diet for each species, rarefaction curves were used based on the number of stomachs analyzed and the interpolation/extrapolation of the Hill numbers, where the confidence interval was constructed using the bootstrap resampling method (Chao et al. 2014), implemented in the iNEXT package (Hsieh et al. 2016). Asymptotic behavior in the extrapolation curve indicates that the diversity of prey observed is representative of the species’ feeding habits, which is supported by the estimation of the sampling coverage, which varies between zero and one, where values near one suggest a good representativeness in the number of stomachs analyzed for the estimation of prey diversity (Hsieh et al. 2016).

The trophic strategy was described using the Amundsen graphic method, which is based on a representation of two dimensions – the specific abundance of a prey (Pi), and its frequency of occurrence in the diet of species x (Amundsen 1996). The specific abundance of each prey was expressed as its percentage with respect to the total volume (∑ volume i...n) of the sample and is expressed as follows: Pi= ∑ Si/∑ Sti * 100; where Pi is the specific abundance of prey i. Si is the volume represented by prey i; and Sti is the total volume of the stomach contents (∑ volume i...n) in the sample (Amundsen 1996). The elements on the upper left part of the diagram represent the between-phenotype component (BPC) of the niche amplitude and suggest there is a variation in the use of resources amongst individuals; the elements on the lower right represent the within-phenotype component (WPC), which indicate that most individuals use many types of resources simultaneously. The observations situated on the upper left part of the diagram should be limited to one or a few preys, which reflects a high specialization and reduced niche amplitude (Amundsen 1996).

To evaluate the differences in the feeding scheme of the species in the reservoir, we used non-parametric, multivariate methods. Similarity matrices were generated by using the Jaccard similarity index (presence/absence), which were compiled in a distance matrix of food items (prey) for each species. The differences in diet amongst species were evaluated with a permutational multivariate ANOVA (PERMANOVA), using the adonis function of the vegan package (Oksanen et al. 2022). To evaluate the differences amongst each pair of species we calculated the p-values corrected by Bonferroni with the pairwise.adonis function from the pairwise Adonis package (Martínez Arbizu 2020). The results are shown on a non-metric multidimensional scaling (nMDS) plot to demonstrate the structure of the diet composition of each species, considering a tension of 0.2 as an acceptable goodness adjustment (Clarke et al. 2014). All statistical analyses and graphs were done using R software (R version 1.4.1717; R Development Core Team 2021)

3.1. Diversity of consumed prey

A total of 40 individuals were analyzed corresponding to the three non-native species of fish (Online Resource 1). Twenty categories of food were identified as prey of these species (Online Resource 1). There were no differences in the diversity of prey consumed by these three species. The amount of prey consumed by C. carpio according to the effective number of species indicates that 89.6% of the prey expected to be recorded in their diet were found (13.3 expected prey, standard error, s.e. = 2.1) (Fig. 2). The number of common and dominant prey consumed by this species did not present differences (Fig. 2). M. salmoides was estimated to have a broader diet, and it was found that 56.1% of the items were identified as their prey (21.4 expected prey, s.e. = 10). There were no differences in the number of common or dominant prey consumed (Fig. 2). Oncorhynchus mykiss presented a lower diversity of consumed prey in comparison to other fish species in this reservoir (Fig. 2). It was found that 95.3% of the prey were identified (9.4 expected prey, s.e. = 0.9). There were no differences in the number of common or dominant prey consumed (Fig. 2). The coverage of the analysis of the stomach contents estimated for the three species was over 90%, under a statistical confidence interval of 99% (Online Resource 3). Thus, it can be inferred that the analysis of these species diets is representative (Online Resource 2).

3.2. Feeding strategies

The Amundsen diagram method showed a specialized trophic strategy for C. carpio feeding primarily on animal remains; while insect remains and plant material were secondary elements with a high frequency of occurrence, indicating the tendency to a strong relationship between the WPC and niche amplitude (Fig. 3). M. salmoides fed mainly on aquatic invertebrates, such as the larvae of dipteran, trichopteran, and odonatan insects, but also on other occasional prey with a high BPC at the niche breadth (Fig. 3). On the other hand, the feeding strategy of O. mykiss was dominated by mollusks (Basommatophora) and insect remains (Fig. 3).

3.3. Variation in diet composition amongst species

Diet composition is different amongst the species (Table 1); however, no differences were observed amongst M. salmoides and O. mykiss (Table 1). The results of nMDS revealed the influence of previous interactions in the diet composition of C. carpio, M. salmoides, and O. mykiss (Fig. 4). The value of tension 2D was 0.12, which indicates that the nMDS graphical analysis was significant (Fig. 4).

Table 1

Differences in diet composition amongst species
	df	SS	R²	Pseudo-F	P-values
Between species	2	3.449	0.234	6.282	< 0.001
C. carpio vs. M. salmoides	1	2.771	0.234	10.39	< 0.001
C. carpio vs. O. mykiss	1	1..463	0.227	5.588	< 0.001
M. salmoides vs. O. mykiss	1	0.687	0.075	2.351	0.092
Residual	41	11.255	0.55
Total	43	14.705	1.00

PERMANOVA. Abbreviations: df = degrees of freedom; SS = sum of squares. Significant values in bold print.

The non-native species that coexist in the Riogrande II reservoir frequently consume prey, such as the remains of animals and diverse aquatic and terrestrial insects, as well as plant material. This type of consumed prey has been documented in studies on the feeding habits of these non-native species in the neotropics (Di Prinzio et al. 2013; Huser and Bartels 2015; Pereira and Vitule 2019). The diversity of consumed prey is similar amongst species; however, M. salmoides behaves as an important predator as it consumes a greater amount of prey compared to the other species with which it coexists. This species has been documented to be a voracious and opportunistic predator that consumes the native biota where it settles (Pereira and Vitule 2019). Remains of native fish were not found in the stomach contents of the three species evaluated, which agrees with what was observed by Luque and González-Trujillo (2019) for O. mykiss, hence, we ruled out their predation in the reservoir. This suggests that the non-native fish do not distribute throughout the reservoir, and, apparently, lentic and environmental conditions are the factors that determine the assemblage structure (Martínez-Toro et al. 2022), as well as the characteristics associated to their reproduction, morphology, and physiology (Arantes et al. 2019).

In this reservoir, C. carpio seems to have a diet especially constituted by the remains of animals and non-identified organic and inorganic material (i.e., detritus and soil), which suggests that this species feeds in the depths of this aquatic environment. It should be noted that some of the individuals of this population also consume various types of resources simultaneously. It has been reported that, in its native habitat, its diet is largely composed of invertebrates, in addition to presenting benthic habits (Magalhães 1993; Rahman et al. 2010). In environments such as lakes and reservoirs, it has been documented as an opportunistic species that mainly feeds on detritus, plant material, amphipods, and larvae of dipteran insects (Colautti and Freyre 2001; García-Berthou 2001). Thus, the feeding behavior of this species could be related to the availability of resources in the environment where it settles (Rahman et al. 2010).

M. salmoides individuals have an opportunistic strategy in this reservoir. The results suggest there is a variation in the consumption of resources amongst the individuals of the population evaluated. For example, while some individuals fed on juvenile fish of O. mykiss, others fed on various terrestrial and aquatic invertebrates. This behavior was expected, since it is reported as a voracious predator in the environments where it settles and can reduce the diversity of fish species and invertebrates (Jackson 2002; Pereira and Vitule 2019). In its native environment, it is also an important predator that presents ontogenic changes in its diet; adults feed on vertebrates such as fish, amphibians, mammals, and are even cannibalistic, while juveniles feed on terrestrial and aquatic invertebrates (Howick and O’Brien 1983; Hodgson and Hansen 2005; Braun and Walser 2011). The strategy of O. mykiss in the reservoir involves feeding on mollusks and various types of aquatic invertebrates. Similarly, its diet depends on the environment where it settles and differences are according to the availability of resources (Musseau et al. 2018). Prey include aquatic insects found in the drift of the water column, as well as on the surface, and may acquire a substantial proportion of its diet from terrestrial invertebrates that fall from the riverine or lacustrine areas (Segnini and Bastardo 1995; Nakano et al. 1999).

The non-native species present different feeding behaviors in this aquatic environment, which can facilitate coexistence by reducing the potential competition amongst them (Araújo et al. 2011). In the Magdalena basin reservoir environments, fish species that have been reported to settle are those that can consume a wide variety of food resources and opt for differences in feeding behavior to coexist in the same environment (Restrepo-Santamaría et al. 2022a). However, differences in diet are found amongst C. carpio and the other species since M. salmoides acts simultaneously as predator and competitor of O. mykiss. This could be attributed to the fact that the search for similar resources amongst these predators in the same environment could increase the rate of encounter with an opportunist predator, thus, becoming a potential prey (Costantini et al. 2018; Luo et al. 2022). This behavior of M. salmoides could be a response to competition, broadening its diet to reduce any other niche amongst coexisting species (Araújo et al. 2011). It should be noted that, besides the reservoir, O. mykiss is found throughout rivers and streams that are tributaries to this reservoir (Martínez-Toro et al. 2022), where it will probably obtain additional food resources and would not present competition with the native species to settle in these lotic environments (Musseau et al. 2018), however, it has been shown for other high Andean fishes that their diet is mainly composed of mollusks and remains of aquatic invertebrates, both in the juvenile and adult stages (Luque and González-Trujillo 2019).

The reservoirs of the Magdalena basin have been subject to the repopulation of non-native species over the years from time to time as a means of food security for inhabitants living near these environments (Lasso et al. 2020); however, it was unknown that invaders could carry negative effects to an already modified environment (Jiménez-Segura et al. 2016; Valencia-Rodríguez et al. 2022). For example, through its ecological interactions, it has been reported that C. carpio could modify the concentrations of nutrients and turbidity of the water by means of its benthic foraging, as well as decrease the diversity of benthic fauna and macrophytes associated to the environment (Weber and Brown 2009). The introduction of M. salmoides could lead to a decrease in the diversity of non-native fish species and to the local extinction of aquatic biota where it settles (Pereira and Vitule 2019). Changes in the food web are attributed to O. mykiss in addition to altering the structure of the communities (Nakano et al. 1999). In some countries, environmental damage and the management of these species involve extremely high costs (Haubrock et al. 2022), thus, it is important to develop more efficient and proactive management strategies to prevent the introduction of fish and promote the mitigation of its impact. In Colombia, it is fundamental to adopt an approach focused on prevention and management of non-native fish by means of guidelines and agreements obtained through government institutions geared toward environmental protection (e.g., ministry of environment, and regional autonomous corporations).

In conclusion, we present a case study in which the diet analysis amongst non-native fish species in a high Andean reservoir proved useful to provide a description of some trophic interactions in this environment. The invading species that settled there consume a wide variety of prey from the native biota, and present different feeding strategies to capture their prey. M. salmoides stood out for its ferocious behavior, as it not only consumes more prey, but also hunts O. mykiss juveniles – a probable competitor for food. The results of this study should be validated with the implementation of new methodologies, such as the use of stable carbon and nitrogen isotopes, which would provide information on the assimilation of the diet of prey and aid in the determination of niche partitioning or the possible competition for resources, in addition to contributing to understanding the properties and function of the trophic network of the ecosystem (Márquez-Velásquez et al. 2019; Black and Armbruster 2021).

Acknowledgements

The authors would like to thank the members of the Ichthyology Group of the Universidad de Antioquia for their support in the sampling campaign. In addition, we thank Andrés F. Galeano from Empresas Públicas de Medellín for his logistical help in the field. Finally, we thank the editor and anonymous reviewers for their valuable and constructive commentaries.

Author contributions

JDN, DRS, and LJS developed the ideas and designed the methodology; DRS, DVR, and LMMT collected the data; JDN analyzed the samples in the lab; JDN, LMMT, JSO, and DRS analyzed the data; DRS, DVR, and LJS directed manuscript composition; JDN, JSO, and LMMT reviewed and edited the manuscript. All authors contributed to the various drafts of the manuscript and gave their final approval for publication.

Funding

The study was funded through the agreement between the Universidad de Antioquia and Empresas Públicas de Medellín known as “Response of Ichthyofauna to the Development of Colombian Reservoirs -CT-2021-000023-A3”.

Data availability

The data used and derived from this research are available in Supplementary Material Online

Conflict of interest

The authors declare no conflict of interest.

Consent for publication

All authors consented to the publication of the manuscript

Ethics approval

This study was conducted with the recommendations and approval of the Ethics Committee on Animal Testing of the Universidad de Antioquia (CEEA). The protocol was reviewed and approved on November 14, 2017 by CEEA, and the study was approved on December 7, 2017. Specimens were collected under collection permit number 0524 of May 27, 2014.

Consent to participate

All authors consented to participate

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Trophic niche partitioning among non-native fish species coexisting in a high Andean reservoir

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Abstract

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1. Introduction

2. Materials And Methods

2.1. Study Area

2.2. Sampling Design

2.3. Data Analysis

3. Results

3.1. Diversity of consumed prey

3.2. Feeding strategies

3.3. Variation in diet composition amongst species

4. Discussion

Declarations

References

Supplementary Files

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