Effect of intraspecific and interspecific competition on the facultative and obligatory shredders forage activity in subtropical system

doi:10.21203/rs.3.rs-3957013/v1

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Effect of intraspecific and interspecific competition on the facultative and obligatory shredders forage activity in subtropical system

https://doi.org/10.21203/rs.3.rs-3957013/v1

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While the significance of competition for resources in shaping the structure of aquatic ecosystems is well recognized, its specific effects on the dynamics of allochthonous matter in streams have received limited attention and remain poorly understood, mainly between interspecific and intraspecific competition. In this study, we investigated the effects of interspecific and intraspecific competition on the shredder organisms Phylloicus and Aegla in leaf litter banks. The impact of competition was assessed through experimental treatments: i - Phylloicus competition-free; ii - Aeglacompetition-free; iii - intraspecific competition within Aegla; iv - intraspecific competition within Phylloicus; v - interspecific competition. In the competition-free treatment, a single organism was placed in a 2-L microcosm, whereas in the competitive pressure treatments, two organisms were placed in a 4-L microcosm, with a 0.05-mm mesh separating them. Our results revealed that interspecific competition had a greater impact on Phylloicus, while intraspecific competition exerted a stronger influence on Aegla. Phylloicusexhibited higher efficiency as a shredder compared to Aegla, which can be attributed to its broader feeding range and unique strategies in leaf litter utilization. The presence of potential competitors led to a reduction in consumption rates in Phylloicus, indicating its sensitivity to competition. Moreover, Aegla's predatory behavior and cannibalism may intensified intraspecific competition within the species. The findings highlight the importance of competition in shaping the feeding activity of shredder organisms in leaf litter banks, which ultimately affects nutrient cycling in aquatic ecosystems.

food activity

leaf litter consumption

predator effect

Neotropical streams

Competition, a fundamental biological interaction, has been shown to have negative effects on organisms (Quiring and McNeil 1984; Cross and Benke 2002), including aquatic insects (Rezende et al. 2015; Cararo et al. 2023b). It can occur within a species (intraspecific) or between different species (interspecific), and the intensity of competition is determined by the competition coefficient of each taxon (Cross and Benke 2002). The outcome of competition can either enhance or diminish the fitness of an organism, depending on its competitive ability (Bird et al. 2019). In aquatic ecosystems, competition often leads to the restriction of space utilization (Baines et al. 2014) and the depletion of available resources (Rezende et al. 2015; Cararo et al. 2023b), resulting in asymmetric effects on reproductive rates within species (intraspecific) (Firmino et al. 2021; Cararo et al. 2023b) or population dynamics between different species (interspecific) (Kohler 1992; Verdú et al. 2009). These competitive interactions play a crucial role in shaping the distribution and abundance of species within aquatic environments (Kohler 1992; Cogo et al. 2014; Durães et al. 2016).

Asymmetric competition in aquatic insects has been associated with a broader dietary range (Englund 1991; Santana-Martínez et al. 2017). Conversely, organisms can gain a competitive edge through specialized strategies in acquiring food resources (Bird et al. 2019). Another crucial aspect is dispersal, as some insects tend to migrate to alleviate competitive pressure (Baines et al. 2014; Durães et al. 2016). This behavior can be attributed to the fact that high competitive pressure can impede population growth (Verdú et al. 2009; Dormann et al. 2018) and, consequently, the ecological processes performed by these organisms (Rezende et al. 2021, 2023). For example, high competitive pressure within specific feeding trophic groups, such as shredders, can lead to reduced leaf litter consumption (Rezende et al. 2015; Cararo et al. 2023b), consequently slowing down nutrient cycling in aquatic environments (Rezende et al. 2021, 2023), mainly in gallery riparian forest (Rezende et al. 2014; Gonçalves et al. 2017). This highlights the importance of comprehending the dynamics of competitive interactions in shaping ecosystem processes and functionality (Rezende et al. 2015; Cararo et al. 2023b).

Aquatic shredder insects are essential for nutrient cycling in freshwater ecosystems (Navarro et al. 2013; Sena et al. 2020; Sena 2021), due to their foraging activities (Biasi et al. 2019), and/or shelter/case construction ability (Rezende et al. 2021; Cararo et al. 2023a). These feeding activities are crucial for the breakdown of organic matter and the release of nutrients into the ecosystem (Graça et al. 2015; Sena et al. 2020). In tropical and subtropical streams, such as those found in the Neotropics (Rezende et al. 2014, 2023; Gonçalves et al. 2017), two prominent shredder species are Phylloicus Müller 1880 (Trichopera, Calamoceratidae) (Holzenthal and Calor 2017; Sena 2021) and Aegla Dana 1852 (Decapoda, Aeglidae) (Santos et al. 2008; Bond-Buckup et al. 2012). These species, characterized by their significant biomass (Parra et al. 2011; Rezende et al. 2015), contribute to the fast decomposition of organic matter and nutrient recycling in these stream ecosystems (Cogo et al. 2014; Biasi et al. 2019; Cararo et al. 2023a).

Phylloicus insects are known as detritivores that primarily feed on plant leaf litter (Navarro et al. 2013; Sena 2021), with their larval stage specializing in shredding and constructing their homes using leaf discs (Holzenthal and Calor 2017). On the other hand, Aegla crustaceans are opportunistic omnivores (Parra et al. 2011; Bond-Buckup et al. 2012), that consume leaf litter, macrophytes, and prey depending on availability (Santos et al. 2008; de Almeida et al. 2021). Despite their different feeding strategies, both species are potential competitors, as they occupy the same trophic group and share the same aquatic environment (Dormann et al. 2018). However, competition for plant detritus may be more asymmetrical for Phylloicus, as it relies on plant leaf litter as its main food source (Rezende et al. 2021), while Aegla has the flexibility to consume other food sources as well (Parra et al. 2011; de Almeida et al. 2021). This potential competition between Phylloicus and Aegla may have implications for ecosystem functioning and dynamics (Parra et al. 2011; de Almeida et al. 2021; Cararo et al. 2023a). However, only the interaction through predation was tested (Cerezer et al. 2016), and no previous studies have been found that specifically investigate the competition between Phylloicus and Aegla.

Based on the understanding that Phylloicus and Aegla can potentially compete with each other for feeding resource (Bond-Buckup et al. 2012; Holzenthal and Calor 2017), and considering that competition can influence foraging behavior (Parra et al. 2011; Cararo et al. 2023b), particularly in the case of Phylloicus as an obligatory detritivore shredder (Holzenthal and Calor 2017) compared to Aegla as a facultative detritivore shredder (Bond-Buckup et al. 2012), our hypothesis is that competitive pressure will negatively affect the foraging behavior of these organisms, with a greater impact on Phylloicus as the obligatory detritivore shredder. Therefore, our objective was to examine the foraging activities of Phylloicus larvae and Aegla adults in the presence and absence of both intra- and interspecific competitors.

Field procedures

Aegla spp. (Aeglidae, Decapoda) and Phylloicus spp. (Calamoceratidae, Trichoptera) specimens were collected from a first-order stream (27°00’32.8” S 52°40’55.1” W) within the Chapecó River drainage basin in Santa Catarina State, Brazil. The stream channel had a length of approximately 1 meter, with a depth of 0.1 meters. Measurements of stream channel length (± 1 meter), depth (± 0.1 meters), water temperature (18.8 ± 0.78°C), pH (5 ± 0.04), and turbidity (21.05 ± 19.02 NTU) were taken using a multianalyzer (model 85, YSI Incorporated). The sampling site was located within an Atlantic Rain Forest remnant, characterized by an average annual temperature of 19.4°C, and an altitude ranging between 670 and 700 meters above sea level.

Sampling of Phylloicus spp. and Aegla spp. was conducted using an aquatic kick net, and the organisms were collected through active search methods. Phylloicus spp. were standardized based on leaf case size (1.5 cm), while Aegla spp. were standardized by dorsal length, which serves as an indication of the same species and larval stage.

Laboratory procedures

The invertebrates were carefully transported to the Laboratory of Ecological Entomology in cool boxes and subsequently transferred to microcosms for the experiment. The microcosms used for the competition treatments measured 10 cm x 15 cm x 30 cm, while those for the competition-free treatments had dimensions of 10 cm x 14 cm x 15 cm. To create a suitable environment, all microcosms were filled with sterilized gravel at the bottom and filled with filtered water. The volume of water added was 4 L for the competition treatments and 2 L for the competition-free treatments, ensuring a density of 1 individual per 2 L of water.

To maintain optimal conditions, the microcosms were equipped with continuous aeration and placed in an experimental room with a controlled temperature of 18 ºC, matching the air temperature in the room. Throughout the experiment, a light/dark cycle of 12 hours light and 12 hours dark was maintained. The pH of the water in the microcosms was carefully monitored and remained within a circumneutral range, with an average value of 6.32 (ranging from 6.05 to 7.16). Temperature was carefully controlled and kept constant at 18 ºC during the entire duration of the experiment.

As for the organic matter used in the microcosm experiments, it consisted of leaf litter discs with a diameter of 1.2 mm obtained from Inga uruguensis Hook. & Arn., a native and abundant plant species found in riparian vegetation. The leaf litter discs were collected using nets suspended 1.5 meters above the ground. Prior to distribution among the treatments, the discs underwent oven-drying at 60°C for 48 hours and were then weighed on a precision balance (Shimadzu, AUW220D model) to determine their initial dry mass.

Experimental design

Leaf consumption was evaluated in a 15-day experiment, consisting of three treatments and two control groups (Fig. 1). There were 3 replicates for intraspecific competition within Aegla spp., 3 replicates for intraspecific competition within Phylloicus spp., and 9 replicates for interspecific competition. Additionally, there were 9 control replicates for Aegla spp. (competition-free) and 9 control replicates for Phylloicus spp. (competition-free), resulting in a total of 33 microcosms and 48 organisms (Table SM 1).

In the competition and control treatments, the microcosms were carefully arranged. Each 4 L microcosm housed two organisms and 10 leaf discs (5 leaf discs per organism) to simulate leaf consumption. To avoid direct interaction between the organisms, a net was used to divide the microcosms in half, with each half accommodating one organism and five leaf discs. In the competition-free control, a single organism and 5 leaf discs were placed in each 2 L microcosm.

At the end of the experiment, the remaining leaf material was collected from the microcosms and subjected to further drying and weighing to determine the final dry mass. Additionally, a separate experiment (n = 16) was conducted to assess leaf detritus decomposition by microbial activity under the same experimental design, but in the absence of invertebrates. The results revealed an average leaf litter consumption of 7.82% (± 0.18 standard error – SE) due to microbial activity.

Leaf litter quality

The concentrations of nitrogen and phosphorus in Inga uruguensis leaf litter were determined by cutting the conditioned leaves into 1.98-cm-diameter discs, which were then freeze-dried. Sets of five discs were weighed using a balance with a precision of 0.01 mg. Nitrogen content was analyzed using a CHN basic analyzer (Carlo Erba 1500 for WI; Thermo Electron Corp. Milan, Italy), while phosphorus content was determined using the ascorbic acid method after acid digestion. The chemical analysis revealed nitrogen content of 1.04 mg.g^− 1 (± 0.04) and phosphorus content of 12.84 mg.g^− 1 (± 3.32) in the I. uruguensis leaves.

After drying and weighing the leaves, they were pulverized for the analysis of resistance to rupture, which measures the hardness of intact leaves (expressed as kPa^− 1), following the method described by Baerlocher et al. (2020). The average hardness of the initial leaves was found to be 0.36 kPa^− 1 (± 0.09). Furthermore, the caloric values (expressed as kcal.g^− 1) of the initial leaf litter were determined in triplicate using an oxygen bomb calorimeter with an automatic temperature control system. The mean caloric value of the initial leaves was calculated to be 5.61 kcal.g^− 1 (± 0.52).

Statistical analysis

We determined the invertebrate leaf consumption by calculating the percentage of leaf litter mass loss (LML) in each microcosm. This was done by subtracting the final dry mass (DM_FINAL) from the initial dry mass (DM_INITIAL) of the leaf litter and dividing it by the initial dry mass: LML = [(DM_INITIAL - DM_FINAL) / DM_INITIAL]. To account for microbial decomposition, we corrected the values by subtracting the mean LML observed in microcosms without larvae. The leaf litter mass loss (LML) in treatments with competitive pressure was divided by the number of organisms evaluated to calculate the per capita leaf litter consumption for each treatment. This approach enabled us to compare and analyze the consumption rates on an individual basis, providing valuable insights into the impact of competition on leaf litter consumption.

To assess the differences in litter consumption among the treatments (i - Phylloicus competition-free; ii - Aegla competition-free; iii - intraspecific competition within Aegla; iv - intraspecific competition within Phylloicus; v - interspecific competition), we conducted a one-way generalized linear mixed-effects analysis using the "glmer" function from the "lme4" package (Crawley 2007). We checked all models for under or overdispersion using the "hnp" package and function. The Gaussian family of error distributions provided the best fit for all models. To account for the specific characteristics of each microcosm and the variation in sample size among treatments, we included the microcosm identity as a random effect in the analysis.

To evaluate the differences among the categorical variables (treatments), we performed orthogonal contrast analysis (Crawley 2007). This analysis involved ordering the treatments in increasing order and testing pairwise comparisons between treatments with the closest values. We applied a stepwise model simplification approach, sequentially adding values with no significant differences and testing them against the next value in the sequence. The “ggstatsplot” function and package were used for data visualization (Patil 2021). All statistical analyses were conducted in R (The R Core Team, version 4.3.0)

The generalized linear mixed-effects model revealed a significant difference among the treatments (GLMM; χ² = 16.74; p = 0.002; Table SM2). Our study demonstrated that Phylloicus in the absence of competition and used as a control group, exhibited the highest per capita leaf litter consumption (26 ± 7.4%; mean ± standard error; Fig. 2) compared to all other treatments. Interestingly, the treatments with competitive pressure, whether from conspecifics (intraspecific; 22 ± 5.9%) or heterospecifics (interspecific; 14 ± 2.7%), showed similar but lower values that in per capita leaf litter consumption of Phylloicus (Fig. 2). Notably, the treatments with only Aegla whether with competitive pressure from conspecifics (4 ± 0.3%) or in the absence of competitive pressure (8 ± 1.3%; control group), displayed the lowest values, and their consumption rates were similar (Fig. 2).

We observed that interspecific competition had a more significant impact on the obligate shredder Phylloicus (Holzenthal and Calor 2017; Cararo et al. 2023a) compared to the facultative shredder Aegla (Cogo et al. 2018; de Almeida et al. 2021). In general, asymmetric competition is the prevailing form of competition (Englund 1991; Dupuch et al. 2014), and there are studies demonstrating its influence on the distribution patterns of shredder organisms (Rezende et al. 2015; Firmino et al. 2022). This observation implies that Phylloicus could have an advantage in leaf banks that have fewer other shredder invertebrates, regardless of whether they are of the same species or different species (Leite et al. 2016; Rezende et al. 2021). High effect of competition could help explain why these organisms are relatively uncommon in certain environments (Boyero et al. 2012; Cararo et al. 2023b). This pattern is somewhat unexpected, as shredder invertebrates typically exhibit aggregated and interspecific distributions (Rezende et al. 2014; Leite et al. 2016). The aggregation pattern may be a response to the trade-off between the effects of competition and predation on foraging activity in the search for food resources (Rezende et al. 2015; Ferreira et al. 2023). Consequently, the organism may reduce its search and feeding efforts to minimize the effects of competition and/or predation (Rezende et al. 2015; Ferreira et al. 2023).

Intraspecific competition exerted a stronger influence on Aegla, likely due to its greater biomass and mobility, which enhance its competitive abilities in resource exploitation (Cogo et al. 2014), compared to Phylloicus. The Aegla genus, known for its predatory behavior and even cannibalism, contributes to the intensification of competitive interactions within the species (de Almeida et al. 2021). Although Aegla has a demonstrated preference for preying on animals, it predominantly relies on plant tissues as a food source in natural environments, reflecting the availability of this resource (Bueno & Bond-Buckup, 2004; Santos et al., 2008). On the other hand, these aggressive behaviors, which may involve the use of weapons, add an additional layer of competition and can have significant impacts on resource exploration in (Palaoro et al. 2020). Consequently, the presence of aeglids in leaf litter banks may result in a reduced breakdown of plant litter and, consequently, slower nutrient cycling (Cerezer et al. 2016), despite their role as important shredders (Biasi et al. 2019).

Intraspecific competition was more intense for Aegla, likely because this organism is a more effective competitor, due to its larger biomass and greater mobility, in resource exploitation (Parra et al. 2011; Marchiori et al. 2014). Furthermore, the behavioral repertoire of Aegla includes predation and even cannibalism (Cerezer et al. 2016; de Almeida et al. 2021), which further intensifies the competitive interactions among individuals. Aegla has been shown to have a clear preference for preying on animals (Cogo et al. 2014, 2018; Cerezer et al. 2016), which may add further predation pressure to this interaction. However, it is worth noting that in their natural environment, aeglids' diet primarily consists of plant tissues due to the high availability of this resource (Santos et al. 2008). Consequently, the presence of aeglids in leaf banks may result in a reduced rate of plant leaf litter shredding (Cerezer et al. 2016), despite their important role as shredders (Biasi et al. 2019).

In this way, our observations reveal that Phylloicus proved to be a more efficient shredder compared to Aegla. This can be attributed to the broader feeding range exhibited by Aegla (Santos et al. 2008), as they are opportunistic omnivores (Cogo et al. 2018). Interestingly, even in the face of stronger interspecific competition, Phylloicus' consumption did not exhibit drastic changes. This pattern can be explained by Phylloicus' limited mobility (Rezende et al. 2014; Leite et al. 2016) and their unique strategy of constructing casings using leaf litter (Sena 2021; Rezende et al. 2021), which helps reduce negative interactions (Rezende et al. 2015; Cararo et al. 2023b), including predation (Ferreira et al. 2023). Moreover, this result may also be influenced by the increased stress and difficulties in active escape experienced by Phylloicus (Rezende et al. 2015; Cararo et al. 2023b). On the other hand, the presence of potential competitors slowed down consumption rates in Phylloicus, as evidenced by the similarities between the intraspecific and interspecific treatments (Rezende et al. 2015; Cararo et al. 2023b), highlighting the organism's sensitivity to these interactions.

Our key findings revealed that shredder organisms were negatively impacted by competitive interactions, leading to changes in their foraging activities, thus supporting our hypothesis. Both Phylloicus and Aegla experienced reduced foraging rates due to competition, but Phylloicus showed greater sensitivity. The results highlight the differential responses of these organisms to interspecific and intraspecific competition. Phylloicus demonstrated higher efficiency as a shredder, attributed to its feeding versatility and adaptive strategies. The limited mobility and casings constructed by Phylloicus may played a crucial role in reducing negative interactions and maintaining its consumption rates. On the other hand, Aegla's competitive advantage stemmed from its larger biomass, highest mobility, and predatory behavior, although its impact on shredding plant tissues may lead to a slower nutrient cycling process. Overall, these findings contribute to our understanding of the ecological dynamics within leaf litter banks in subtropical streams of Neotropics and the important role of competition in structuring shredder communities in freshwater ecosystems.

Funding: Not applicable.

Conflicts of interest/Competing interests: The authors declare no conflicts of interest associated with this manuscript.

Availability of data and material: Data analyzed during this study are included as supplementary files.

Authors' contributions: EC and RR conceived the study, collected ﬁeld data and performed the chemical analyses. RR and CLR managed and analyzed the data. GRD wrote the manuscript with feedback from RR, EC and CALR authors. All authors contributed to the article and approved the submitted version.

Ethics approval: We confirm that this manuscript complies to all Ethical Rules applicable for this journal.

Consent to participate: All authors contributed to the article and approved the submitted version.

Consent for publication: All authors approved this manuscript for publication, if accepted.

Acknowledgments

RSR (projects number 403945/2021-6 and 302044/2022-1) are grateful to National Council for Scientific and Technological Development (CNPq). We thank the support from the Foundation to Support the Research and Innovation of State of Santa Catarina (FAPESC) and the Community University of the Chapecó Region (LabEntEco).

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Effect of intraspecific and interspecific competition on the facultative and obligatory shredders forage activity in subtropical system

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Figures

INTRODUCTION

MATERIALS AND METHODS

Field procedures

Laboratory procedures

Experimental design

Leaf litter quality

Statistical analysis

RESULTS

DISCUSSION

Conclusion

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1