Next Article in Journal
Conceptual Models and Calibration Performance—Investigating Catchment Bias
Previous Article in Journal
New Pond—Indicator Bacteria to Complement Routine Monitoring in a Wet/Dry Tropical Wastewater Stabilization System
Previous Article in Special Issue
Short-Term Interactive Effects of Experimental Heat Waves and Turbidity Pulses on the Foraging Success of a Subtropical Invertivorous Fish
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Influence of Eichhornia crassipes (Mart) Solms on a Tropical Microcrustacean Community Based on Taxonomic and Functional Trait Diversity

1
Zoology and Botany Department, Biosciences, Languages, and Exact Sciences Institute (IBILCE), São José do Rio Preto Campus, São Paulo State University Júlio de Mesquita Filho (UNESP), São José do Rio Preto-SP, 15054-000, Brazil
2
Department of Biological Sciences, University of Quebec at Montreal, C.P. 8888 Succ.Centre-Ville, Montreal, QC H3C 3P8, Canada
3
Unesp’s Aquaculture Center (CAUNESP), Jaboticabal Campus, São Paulo State University Júlio de Mesquita Filho (UNESP), Jaboticabal-SP, 14884-900, Brazil
*
Author to whom correspondence should be addressed.
Submission received: 18 May 2019 / Revised: 25 October 2019 / Accepted: 5 November 2019 / Published: 19 November 2019
(This article belongs to the Special Issue Trophic Interactions in Warm Freshwater Ecosystems)

Abstract

:
Macrophytes are important structural attributes of freshwater ponds and wetlands, affecting zooplankton community composition. One of the best-known macrophytes in the world is Eichhornia crassipes, which, due to its high reproductive rate, can quickly occupy large areas of aquatic environments. However, there have been few assessments of the direct effect of this macrophyte, in the absence of predators, for tropical zooplankton communities. The aim of this study was to evaluate the influence of E. crassipes on microcrustacean community structure using species and functional diversity, the latter providing an important tool to evaluate the response to changes in resource availability along an environment gradient. We also evaluated which functional traits were favored when the structural niche offered by submerged parts of the macrophytes was present. We conducted a 30 day mesocosm experiment (117 m3) with and without the presence of floating macrophytes (Eichhornia crassipes) inserted along one edge of the mesocosms. Treatment effects on microcrustacean density and community structure using taxonomic and functional classification approaches were assessed. There was a positive association between macrophyte presence and microcrustacean diversity for both diversity types, showing that the presence of macrophytes enhanced the niche availability for the microcrustacean community, likely through changes to resource diversity through habitat structure provision. In the presence of macrophytes, the abundance of species with the following feeding traits increased: burrowing, benthic habitat preference, and herbivore–detritivore and omnivore–carnivore trophic groups. Results showed that the species capable of using the niche offered by submerged macrophyte structures had benthic traits, enabling their co-existence with species possessing primarily pelagic traits. Using a functional approach, our study demonstrated that Eichhornia crassipes can structure microcrustacean communities and promote diversity, likely via increased habitat diversity, which enables the co-existence of species possessing different adaptations to acquiring resources available in the environment.

1. Introduction

In aquatic ecosystems, the presence of macrophytes has important structuring consequences for microcrustacean communities because their physical characteristics alter habitat structure in ways that can influence resource availability and resource quality [1,2]. It has been reported that for cladocerans, the habitat architecture is an important factor influencing composition [3]. For example, macrophytes increase the availability of attachment surfaces for species that require a substrate for locomotion such as benthic cladocerans, or for species able to use submerged structures to settle and filter water from a stationary position. Macrophytes can increase resources for detritivores because their submerged structures accumulate sediments or detritus [3]. Moreover, macrophytes can also offer a novel prey source for omnivorous or carnivorous microcrustaceans because of increases in associated microorganisms [4]. Macrophytes are reported as essential for increases in diversity of fish fauna because of the greater supply of food resources, but also by offering refuge against predation from larger visual hunting fish [5]. Such changes that indirectly promote resource heterogeneity and higher resource availability may explain greater microcrustacean diversity in littoral zones of aquatic ecosystems, even in the absence of predators, especially where macrophytes are more abundant [6]. Some studies have demonstrated a role for macrophytes as mediators in the interaction between prey and aquatic predators [2,3,4,5,6,7], with zooplankton using plants as a refuge against predation by fish [8,9]. However, zooplankton may also avoid macrophyte areas when fish predation is intense in these areas [7].
One of the most notorious macrophytes in the world is Eichhornia crassipes (Mart) Solms, which, due to its high reproductive rate, can quickly occupy large areas of aquatic environments [10,11]. Because of this, these plants are considered to be pests capable of causing damage to fish production and water quality [11]. Knowing the influences of these plants on all components of aquatic communities is important in understanding how their extreme biomass affects the ecosystems that they invade and inhabit.
A major influence of macrophytes on zooplankton community structure is to promote an increase in microcrustacean taxonomic species richness. However, taxonomic richness may not be sufficient in capturing changes in niche dimensions related to resource availability that lead to compositional shifts, but perhaps not to richness shifts. Furthermore, taxonomic diversity does not consider mechanistically the ways in which species may be adapted to the novel niches offered by Eichhornia in particular, which is a free-floating plant. Functional trait diversity can thus be a more useful tool whereby species identities are replaced by trait combinations that reflect the various means of resource exploitation and, ultimately, the niche space occupied by species in the community [12,13,14]. Evaluating community compositional shifts (relative species abundances) with macrophytes, as well as the traits of the dominant species, allows us to identify the niches introduced by the submerged structures when Eichhornia colonizes.
A community with greater resource use trait diversity could allow more efficient resource exploitation by a community through complementarity [15,16], and could thus augment overall productivity, as has been shown in diatom communities [17]. To evaluate niche complementarity, functional diversity indices are useful tools by which greater values indicate the presence of taxa capable of exploring a greater variety of niche dimensions, indicating a reduction in competition for common resources [15].
In this study, we evaluated how the presence of the free-floating plant Eichhornia crassipes influences the functional structure of microcrustacean communities via changes in resource availability and habitat heterogeneity. We examined species traits related to the use of resource niches provided by macrophytes, and explored with the outcome for functional diversity. The aim of the study was to contribute to understanding the role of macrophytes E. crassipes in structuring microcrustacean communities, which ultimately influence ecosystem functioning through nutrient cycling in aquatic environments [17,18,19].

2. Materials and Methods

2.1. Experimental Design

We conducted an experiment using 12 earth pond mesocosms located in the Aquaculture Center, São Paulo State University (UNESP), Brazil (21°15′22′′ S, 48°18′48′′ W) in the autumn of 2011. Mesocosms were 1.50 m deep, 13 m long, and 6 m wide (totaling an area of 78 m2 and a volume of 117 m3) and were thus long enough to allow for zone differentiation between littoral and pelagic areas with macrophyte manipulations. The mesocosms were filled with pond water and had established microcrustacean communities prior to macrophyte addition, with the most abundant taxa being Bosmina longirostris (O. F. Muller, 1785); Diaphanosoma spinulosum Herbst, 1967; Argyrodiaptomus furcatus (Sars, 1901); and Thermocyclops decipiens (Kiefer, 1929). The water was not replenished during the experiment. To observe the influence on microcrustacean community structure, replicated (six times) macrophyte treatments were established, either with or without the presence of Eichhornia crassipes. When present, macrophytes were inserted along one edge of the mesocosm, simulating a small lentic environment with a vegetated littoral zone. The experimental design with treatments and sampling sites in the littoral and pelagic zones are shown in Figure 1.
Eichhornia crassipes were obtained from cultivated macrophyte beds at Universidade Estadual Paulista (UNESP), Jaboticabal campus, where the experiment was performed. Before transplantation, macrophyte roots were washed with water to avoid contamination of mesocosms with organisms from the cultivation area. About 50 individuals of E. crassipes were inserted into each pond of the treatment with macrophytes. Because E. crassipes is a floating species, a 6 m bamboo stake was used to retain the macrophytes 2 m away from the mesocosm edges. Following the introduction of macrophytes on 1 April 2011, the mesocosm communities were left unperturbed for 30 days before microcrustacean samples were collected on 1 May 2011. After 1 month, the macrophytes multiplied and covered an area of 12 m2 in each the macrophyte treatment ponds; their roots grew to a depth of about 40 centimeters below the water surface. The experimental period corresponded to the first month of the dry season (April to September) in this tropical, hot, and rainy region, according to the Köppen–Geiger climate classification [20]. To isolate the effect of macrophytes on zooplankton community structure, predators such as fish were excluded and Chaoborus larvae were not observed.

2.2. Sampling

Samples of water and zooplankton were collected from two locations in each mesocosm: from the pelagic zone in the center and in the littoral zone close to one of the mesocosm edges. In macrophyte-containing mesocosms, littoral samples were taken from the middle of the macrophyte stand. In the control treatment (no macrophytes), the zone close to the margin was sampled as the corresponding zone. In this way, it was possible to standardize the sample method and observe whether the effect on the zooplankton community resulted from the presence of macrophytes and not from the proximity to the pond margin. Samples were collected at noon and at midnight, resulting in four subsamples from each mesocosm—two spatial and two temporal points. This methodology ensured that communities were thoroughly sampled, taking into account potential vertical and horizontal diel migration of the microcrustaceans [21,22,23].
To sample microcrustaceans, 75 L from the water column was pumped from each location and time point using a bilge pump (Jabsco, model 34600-0000, ITT Jabsco, Costa Mesa, CA, USA). Water was filtered through a 45 µm mesh net, and organisms were anesthetized with carbonated water and fixed with 4% buffered formalin. In the laboratory, microcrustacean taxonomic identification was performed using light microscopy and taxonomic keys to identify species [24,25,26] on 2.5 mL subsamples. At least 60 individuals of the most abundant species were counted in each subsample, and the total number of subsamples counted was determined by satisfying the condition that the CV (coefficient of variation) of the densities was less than 0.2 [27]. When there was a low overall density of organisms, the entire sample was counted. Male and female copepods, nauplii, and copepodites were enumerated separately.
At the time of zooplankton sampling, limnological factors were also analyzed to determine whether there were any changes in the physical and chemical characteristics of the mesocosms because of macrophyte inclusion. Using a multiparameter probe (Horiba U-10—Horiba Ltd., Kyoto, Japan) in the littoral and pelagic zones, we measured temperature, dissolved oxygen, pH, and conductivity.

2.3. Functional Traits

Feeding type, average body size, habitat preference, and trophic group are zooplankton traits that can be readily used for functional diversity analyses [28]. All traits were based on literature data.

2.3.1. Feeding Type

This trait captures the manner by which species or groups obtain their food (Table 1). It is the most complex trait and we included some types in our classification. Cladoceran feeding types were classified as follows [29]: Daphnia-type filtration, when filtering occurs in a stationary position with the filtering apparatus on the third and fourth legs; Sida-type, which is similar to Daphnia-type, but the apparatus is located on the first five legs; and Bosmina-type, which is characterized by active horizontal swimming and a less developed filtering apparatus on the thoracic appendages. Copepods can be classified into two types: raptorial for animals that actively capture and kill prey, and stationary suspension for organisms that are more passive and swim less. We also included two other classifications: burrowing type, which digs into the substrate to feed on periphyton or detritus on mud, consisting of most chydorids [30,31,32,33], and attached type, species that attach to substrates such as macrophytes from which they filter water to feed [29].

2.3.2. Body Size

Average body size is a continuous trait (Table 1). However, for the statistical comparison of densities between treatments, microcrustaceans were divided into four size classes: (A) 0.1 to 0.5 mm, (B) 0.6 to 1.0 mm, (C) 1.1 to 1.5 mm, and (D) 1.6 to 2.0 mm. The classes were determined on the basis of maximum sizes of microcrustacean species obtained from the literature.

2.3.3. Habitat Preference

Habitat preference for microcrustaceans consisted of three general categories: benthic, open water (pelagic), and vegetation, for those associated with macrophytes (Table 1). Some species, such as Moina minuta Hansen, 1889, occupy both littoral and open water habitats, and were thus classified as open water-vegetation.

2.3.4. Trophic Group

We applied main categories on the basis of primary prey sources: herbivore, omnivore, carnivore, and detritivore (Table 1). We considered omnivores to be organisms that feed on a variety of materials including plants, animals, algae, and fungi. For species with food preferences that span more than one prey type, combined groups were created: omnivore–carnivore and herbivore–detritivore, as recommended by Barnett et al. [28]. As no exclusively carnivorous species were found, we classified as omnivorous–carnivorous those that, although also feeding on algae, had a diet more similar to that of a predator. To classify an organism as herbivore–detritivore or carnivore–omnivore we used the criteria established by Barnett et al. [28] to differentiate species that were more carnivorous than others.

2.4. Diversity Indices

Diversity indices for the microcrustacean taxonomic data included species richness (S), Shannon–Wiener diversity (H’), and community evenness (J’). These indices were calculated on abundance (#/L) data from the microscope counts. All the taxonomic diversity indices were calculated using the Vegan package in R [33,34] (R Foundation for Statistical Computing, Vienna, Austria).
We used analogous functional diversity indices—functional richness (FRic), functional evenness (Eve), and functional dispersion (FDis). All traits (Table 1) were used to create the species × trait matrix. FRic represents the volume of the functional space occupied by the community and FEve is the regularity of abundance in this volume [12]. FDis represents the mean distance in multidimensional trait space of individual species to the centroid of all species; it can account for relative species abundances by shifting the position of the centroid to that of the more abundant species and then weighting distances of individual species by their relative abundance [6]. All the functional indices were calculated using the FD package in R [34,35], applying distance matrices based on Gower’s index.
Individuals with the same trait were pooled and densities among groups were compared to detect whether the macrophytes influenced the abundance of individuals possessing some specific trait.

2.5. Statistical Analyses

2.5.1. Niche Complementarity

SES (standardized effect size) for functional richness was calculated because it excludes the effect of species richness from the analyses, besides being a good test to detect increases in niche complementarity along an ecological gradient [15]. The species density matrix used in this null model analysis consisted of the mean of species densities across the four samples taken from each mesocosm (littoral, pelagic, day, and night) resulting in a matrix with the densities of populations from six mesocosms with macrophytes and six mesocosms without macrophytes. The SES ranking was calculated for each mesocosm following the methodology proposed by Gotelli and Entsminger [36], where the observed values of functional richness was compared with those expected from matrix swap null models, calculated with the independent swap algorithm described in Gotelli and Entsminger [36]. This statistical procedure generated a ranking number whereby the functional richness in each mesocosm was compared with means of random values created for all community combinations.
The SES ranking that resulted for each mesocosm was compared using an independent t-test to assess whether mesocosms with macrophytes had greater functional diversity than that expected by chance (n = 6, degrees of freedom = 5), thereby indicating the presence of functional complementarity. The SES ranking was calculated using the ‘ses.mpd’ and ‘ses.mntd’ functions from the picante package [34] in R statistical software [33].

2.5.2. Potential Drivers of Functional and Species Diversity

Species richness (S), Shannon–Wiener diversity (H’), Simpson’s dominance (D), functional richness (FRic), functional uniformity (FEve), and functional dispersion (FDis) were calculated for each subsample (littoral, pelagic on day and night period). The influence of macrophytes and environmental variables on functional and species diversity was evaluated using generalized additive models (GAM) with integrated smoothness estimation, where all the functional and the species diversity parameters (dependent variables) were modelled with the temperature, concentrations of dissolved oxygen, water conductivity, and pH (independent variables). There were no statistical differences between parameters from both treatments. All models identified the mesocosm (tank) and the littoral and pelagic zones (habitat) with the day (time) included as a random effect. Model selection was using the AIC (Akaike information criterion), adjusted R2, and the significant estimates of the independent variables. All statistical analyses were performed with the package mgcv in R statistical software [33,34,35,36,37,38].

2.5.3. Density Comparison for Species and Functional Groups

To evaluate the responses of individual species or functional groups to macrophytes, subsample densities were pooled according to the statistical analysis performed. Trait densities were log-transformed prior to analyses to reduce heteroscedasticity. For the comparison of species and functional groups densities between treatments, the four subsampled densities from each mesocosm were pooled, resulting in six replicates for each treatment (with and without macrophytes). Comparisons were performed using a two-way ANOVA with treatment and zones as factors. There were no statistical differences between zooplankton densities from day and night samples and thus we pooled the day and night subsamples. It was expected that in the presence of macrophytes, the distribution of species and functional groups would be different between littoral and pelagic zones, whereas these zones would be more similar in mesocosms without macrophytes. The results enabled the identification of macrophyte effects on specific traits. All the statistical analyses were performed using R statistical software [34].

3. Results

Across all samples, a total of two calanoid copepod, two cyclopoid copepod, and eight cladoceran species (from the Sididae, Bosminidae, Moinidae, Daphiniidae, Ilyocryptidae, and Macrothricidae families) were identified (Table 2).

3.1. Community Structure and Environment Variables

There were no significant treatment differences in the mean levels of any environment variables (p > 0.05; Figure S1). Species richness (S) (Figure 2a) and diversity (H’) (Figure 2c) decreased linearly with pH, but were higher in the presence of macrophytes than in the control (Figure 2b,d). Functional richness (FRic) decreased linearly with water conductivity (Figure 2e), whereas functional dispersion (FDis) decreased linearly with water temperature (Figure 2g). Both FRic and FDis were higher in the presence of macrophytes than in the control (Figure 2f,h). Neither functional (FEve) nor taxonomic indicators (J) of evenness were associated with macrophytes, nor with limnological variables.

3.2. Density of Species and Functional Groups

In the presence of macrophytes, significantly greater abundances of species were observed, including those able to attach and burrow to feed, those with benthic habitat preference, and those belonging to herbivore–detritivore, and omnivore–carnivore trophic groups (Figure 3 and Table 3). Reduced densities of species preferring the open water habitat, from the omnivore trophic group and from the largest, class D body size (1.6 to 2.0 mm) were observed in the mesocosms with macrophytes (Table 3).
The distribution of some functional groups between the littoral and pelagic zones of the mesocosms was significantly affected by the presence of macrophytes (Figure 3 and Table 3). The omnivore–carnivore trophic group presented equal abundances in the littoral and pelagic zones with macrophytes (none of this group were present in the control). Class D (1.6 to 2.0 mm) microcrustaceans were more abundant in the pelagic zones of mesocosms without macrophytes. All other groups varied significantly by zone only when macrophytes were present; the omnivore trophic group and open water habitat traits were more abundant in the ponds without macrophytes, whereas the attached, the herbivore-detritivore trophic group, benthic habitat preference, and burrowing feeding were more abundant in littoral zones with macrophytes over the pelagic zones (Figure 3).
The cladocerans Pseudosida bidentata Herrick, 1884; Ilyocryptus spinifer Herrick, 1882; Bosmina longirostris; and Macrothrix paulensis (Sars, 1901), and the copepod Mesocyclops meridianus (Kiefer, 1926) occurred at greater densities in mesocosms with macrophytes (Figure 4 and Table 4). Species with reduced densities in the presence of macrophytes were the cladoceran Ceriodaphnia cornuta Sars, 1886; copepod nauplii; and the copepod Argyrodiaptomus furcatus. With respect to zone differentiation, the cladoceran Ilyocryptus spinifer was more abundant in littoral zones, irrespective of treatment, and Pseudosida bidentata was more abundant in littoral zones of mesocosms with macrophytes (Figure 4 and Table 4).
The SES rankings showed a positive value in the macrophyte treatment (Figure 5), with a significant result (p < 0.05) for the t-test, comparing the macrophyte treatments. A significantly more positive value in the SES ranking indicated a higher functional diversity than expected by chance, implying a higher niche complementarity in mesocosms with macrophytes.

4. Discussion

The density of individuals with certain functional traits varied between experimental treatments, enabling us to identify which microcrustacean niche dimensions were affected by Eichhornia crassipes macrophytes. This was possible because the traits reflect how niche space is used by species in the community [12]. Thus, increases in density of individuals with the attached feeding type and benthic traits, as we observed for the benthic habitat and herbivore detritivore food preference traits, indicated that macrophytes such as E. crassipes increased resource opportunities for benthic species unable to efficiently exploit pelagic zones. Thus, although their presence may restrict the local niche of pelagic species, E. crassipes are capable of enhancing the niche for other species of microcrustaceans, enabling a greater functional diversity across ponds with both types of zones.
Benthic cladocerans, such as Chydoridae, Macrothricidae, and Ilyocryptidae, are composed of species that have morphological specializations, allowing them to explore the niche offered by submerged structures of macrophytes. Antennae are usually used as an oar to move along a substrate or mud, and the carapaces have morphological adaptations on the ventral margin to permit crawling on surfaces [30]. Most benthic species are able to swim only short distances [30], and the submerged branches and roots of macrophytes as E. crassipes can be used as a substrate for attachment. These submerged structures form a tangled complex of branches of different sizes, shapes, and thicknesses that provide increased availability of microhabitats and niches. For submerged aquatic vegetation (SAV), the increase in zooplankton biomass and functional diversity was also related to the increased availability of habitats and ecological niches provided by submerged macrophyte structures [39]. Increased abundance of organisms in the macrophyte mesocosms with the attached feeding type, benthic habitat preference, as well as the herbivore–detritivore trophic grouping together reflects their feeding strategy consisting of scraping the surfaces of submerged branches of macrophytes for periphyton or accumulated detritus on macrophyte roots [3].
In addition to increasing the foraging area for benthic species, macrophyte-associated microorganisms can also represent novel food resources for predacious microcrustaceans [5], potentially explaining a higher density of omnivore–carnivore trophic group found in the macrophyte treatment. In our study, copepods classified as omnivore–carnivore were represented by the cyclopoid Mesocyclops, a benthic genus, adapted to living among macrophytes, and with a high plasticity for prey preference [40,41]. Even a small increase in food quality via novel micro-organism introductions with macrophyte addition could have enabled the density increase in this trophic group.
Unlike benthic species, filter feeders could not exploit the novel niches offered by macrophytes in littoral zones. Species with the vegetation trait (e.g., of the genera: Simocephalus and Diaphanosoma) possess a feeding apparatus similar to pelagic species, allowing capture of suspended solids in the water column, but with the additional ability to attach to the submerged structures of macrophytes and filter feed from a stationary position [31,32,42]. Such species are often found in the middle of macrophyte stands [28]. In our study, all species categorized as preferring vegetation habitat—Pseudosida bidentate, Simocephalus serrulatus (Koch, 1841), and Macrothrix paulensis—increased in density in E. crassipes stands, indicating the role of these plants in increasing the habitat availability.
Macrophyte forms (floating vs. submerged) may influence resources available for microcrustaceans because the physical assistance offered by each depends on the shape and structure that remains submerged [5], potentially differentially influencing microcrustacean functional groups [39]. The floating form as E. crassipes has submerged roots and stolons, which retain a large amount of detritus that is highly suitable for benthic species use [3], but not for pelagic filter feeders. For pelagic species, submerged macrophytes may offer a better overall habitat, as their growth form allows for some light penetration and phytoplankton growth, also offering greater interstitial space for filtration [7,43] (although this depends on the biomass density of the macrophytes). Thus, the floating macrophytes used in our experiment likely did not adequately increase the foraging area available for microcrustaceans possessing the vegetation habitat trait (primarily filter feeders), explaining the lack of treatment effect.
For the truly pelagic filter feeders with habitat preference for open areas, we detected an avoidance of macrophyte zones, with lower densities of these species and traits in the macrophyte treatment and in their littoral zones. For truly pelagic species, macrophytes may be preferred over open water areas, primarily as a refuge against visual predation from fish in pelagic zones [7], predators that were absent in our study. For pelagic species, the avoidance of macrophyte stands is related to a decrease in phytoplankton production due to light limitation [9,44], thereby diminishing resources for filter feeders such as Ceriodaphnia and calanoid copepods. In addition, the presence of macroinvertebrate predators [45,46] and small fish [47] in macrophyte stands may also cause pelagic species to avoid these sites.
The abundances of the copepod A. furcatus were reduced from positive to almost zero densities with the addition of macrophytes. These taxonomic shifts are associated with the feeding habit of Diaptomidae, a group with a feeding preference for larger phytoplankton and even small planktonic invertebrates, such as rotifers [48]. Macrophytes generally reduce phytoplankton production [38] and change their composition [49], and thus food quality and quantity may have been reduced for such diaptomids, negatively affecting their abundance.
Species and functional diversity indices responded positively to macrophyte presence, although some environmental variables also showed influences. However, irrespective of any environmental effects associated with macrophyte addition, the presence of the macrophyte itself showed a significant beneficial effect on microcrustacean diversity. These findings indicate that resources related to food and habitat structure promoted by macrophytes played an important role in the changes observed in the zooplankton community structure.
With an analysis of community structure, it was possible to evaluate increases in diversity in the macrophyte treatment, as well as to infer that a greater niche space was occupied by the community on the basis of the traits that were most responsive, reflecting an increase in resource and physical heterogeneity offered by macrophyte structures. This conclusion is based on the fact that the responsive traits of microcrustaceans were those related to feeding and specifically to the morphology of appendices used to filter suspended solids, scrape solid surfaces, or actively prey on other organisms [22,29,31,42], as well as functional traits that reflect resource requirements for each species [28].
Species using alternate resource types can be favored by macrophyte presence, as we observed for benthic species, which are normally otherwise unable to inhabit the water column. Thus, an increase in niche complementarity, as observed through augmented functional trait diversity, enabled a more complete resource exploitation by the community. Greater niche complementarity between species and macrophytes was also evidenced by a greater variation in functional group densities between littoral and pelagic zones, observable only in the macrophyte treatment. Furthermore, some functional groups were present in macrophyte-covered littoral zones, indicating a likely increase in resource niche dimensionality and a greater species complementarity.
Functional traits and niche complementarity are significant factors influencing community assembly, and the influence of macrophytes on these will in turn have implications for ecosystem functioning. For plankton communities, functional diversity has been associated with an increase in productivity [17]. The shifts in our microcrustacean communities should have consequences for pond ecosystem functioning because of the important role that these organisms play in linking trophic levels and in recycling nutrients [19,50,51].
The main goal of this study was to verify whether E. crassipes increased the diversity of predator-free microcrustacean communities through increases in habitat heterogeneity and functional complementarity of species. Through the null model comparison, it was possible to confirm that zooplankton functional diversity increased in the presence of the floating macrophyte E. crassipes, promoting changes in the zooplankton community structure. Our observations further indicated a greater niche complementarity in mesocosms with Eichhornia crassipes. This plant is considered to be a pest of aquatic ecosystems in many parts of the world [11] and its increase in abundance can result in a profound change in biodiversity of the aquatic ecosystem. The zooplankton community is considered as a link between producers and consumers in aquatic food chains. Changes in its structure can have a cascading effect throughout the aquatic biota. In addition to the direct effect of macrophytes on zooplankton, demonstrated in this study, several other studies have demonstrated the indirect effects of macrophytes on the interaction between zooplankton and its predators, generating many questions that will certainly be addressed in future studies.

5. Conclusions

Shallow ecosystems in the tropics are abundant and usually contain extended littoral zones with a high diversity of microcrustaceans. Our study demonstrated that the effect of Eichhornia crassipes on extending the resource base alone was sufficient in altering taxonomic and functional diversity and composition, independent of any supplementary effects that macrophytes may have on predation rates, which could further enhance such shifts. It also contributes to future studies about the trophic interactions mediated by macrophytes, which are still little known in the tropics.

Supplementary Materials

The following are available online at https://0-www-mdpi-com.brum.beds.ac.uk/2073-4441/11/11/2423/s1: Figure S1: Average of limnological variables in mesocosms with and without macrophytes. Table S1: Statistical results of modeling analysis for S (species richness) and the independent variables. Table S2: Statistical results of modeling analysis for H’ (Shannon-Weaver species diversity) and the independent variables. Table S3: Statistical results of modeling analysis for FRic (functional richness) and the independent variables. Table S4: Statistical results of modeling analysis for FEve (functional evenness) and the independent variables. Table S5: Statistical results of modeling analysis for FDis (functional dispersion) and the independent variables.

Author Contributions

Conceptualization, M.S.M.C.-N. and L.R.S.; methodology, M.S.M.C.-N., L.R.S., and S.G.M.O.; formal analysis, L.R.S., B.E.B., and M.S.M.C.-N.; investigation, L.R.S., B.E.B., S.G.M.O., and M.S.M.C.-N.; resources, M.S.M.C.-N. and B.E.B.; data curation, M.S.M.C.-N. and L.R.S.; writing—original draft preparation, L.R.S., B.E.B., S.G.M.O., and M.S.M.C.-N.; writing—review and editing, L.R.S., B.E.B., and M.S.M.C.-N.; supervision, M.S.M.C.-N. and B.E.B.; project administration, M.S.M.C.-N.; funding acquisition, M.S.M.C.-N.

Funding

This research was funded by Research Rectory—São Paulo State University Julio de Mesquita Filho (PROPe-UNESP) and scholarship from São Paulo Research Foundation (FAPESP—2011/15365-9) to S. G. M. Oliveira and from Coordination for the Improvement of Higher Education Personnel (CAPES) to L. R. Stephan.

Acknowledgments

The authors thank Research Rectory—São Paulo State University Julio de Mesquita Filho (PROPe-UNESP) and São Paulo Research Foundation (FAPESP—04/04820-3 and 2011/15365-9) for financial support and W. C. Valenti for their support for the experiments. We thank very much N. G. dos Santos and E. F. dos Santos for his help with statistical analysis. We also thank the anonymous reviewers and especially Mariana Meerhoff, the guest editor, for all the criticisms and suggestions that helped to improve the article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Meerhoff, M.; Mazzeo, N.; Moss, B.; Rodríguez-Gallego, L. The structuring role of free-floating versus submerged plants in a subtropical shallow lake. Aquat. Ecol. 2003, 37, 377–391. [Google Scholar] [CrossRef]
  2. Meerhoff, M.; Iglesias, C.; Teixeira De Mello, F.; Clemente, J.M.; Jensen, E.; Lauridsen, T.L.; Jeppesen, E. Effects of habitat complexity on community structure and predator avoidance behavior of littoral zooplankton in temperate versus subtropical shallow lakes. Freshw. Biol. 2007, 52, 1009–1021. [Google Scholar] [CrossRef]
  3. Debastiani-Júnior, J.R.; Elmoor-Loureiro, L.M.A.; Nogueira, M.G. Habitat architecture influencing microcrustaceans composition: A case study on freshwater Cladocera (Crustacea Branchiopoda). Braz. J. Biol. 2016, 76, 93–100. [Google Scholar] [CrossRef]
  4. Thomaz, S.M.; Cunha, E.R. The role of macrophytes in habitat structuring in aquatic ecosystems: Methods of measurement, causes and consequences on animal assemblages’ composition and biodiversity. Acta Limnol. Bras. 2010, 22, 218–236. [Google Scholar] [CrossRef]
  5. Grzybkowska, M.; Dukowska, M.; Leszczynska, J.; Lik, J.; Szczerkowska-Majchrzak, E.; Przybylski, M. The food resources exploitation by small-sized fish in a riverine macrophyte habitat. Ecol. Indic. 2018, 90, 206–214. [Google Scholar] [CrossRef]
  6. Castilho-Noll, M.S.M.; Câmara, C.F.; Chicone, M.F.; Shibata, E.H. Pelagic and littoral cladocerans (Crustacea, Anomopoda and Ctenopoda) from reservoirs of the northwest of São Paulo State, Brazil. Biota Neotropica 2010, 10, 1–10. [Google Scholar] [CrossRef]
  7. Meerhoff, M.; Fosalba, C.; Bruzzone, C.; Mazzeo, N.; Noordoven, W.; Jeppesen, E. An experimental study of habitat choice by Daphnia: Plants signal danger more than refuge in subtropical lakes. Freshw. Biol. 2006, 51, 1320–1330. [Google Scholar] [CrossRef]
  8. Timms, R.M.; Moss, B. Prevention of growth of potentially dense phytoplankton populations by zooplankton grazing, in the presence of zooplanktivorous fish, in a shallow wetland ecosystem. Limnol. Oceanogr. 1984, 29, 472–486. [Google Scholar] [CrossRef]
  9. Burks, R.L.; Lodge, D.M.; Jeppesen, E.; Lauridsen, T.L. Diel horizontal migration of zooplankton: Costs and benefits of inhabiting the littoral. Freshw. Biol. 2002, 47, 343–365. [Google Scholar] [CrossRef]
  10. Patel, S. Threats, management and envisaged utilizations of aquatic weed Eichhornia crassipes: An overview. Rev. Environ. Sci. Biotechnol. 2012, 11, 249–259. [Google Scholar] [CrossRef]
  11. Villamagna, A.M.; Murphy, B.R. Ecological and socio-economic impacts of invasive water hyacinth (Eichhornia crassipes): A review. Frashw. Biol. 2010, 55, 282–298. [Google Scholar] [CrossRef]
  12. Tilman, D.; Knops, J.; Wedin, D.; Reich, P.; Ritchie, M.; Siemann, E. The Influence of Functional Diversity and Composition on Ecosystem Processes. Science 1997, 7277, 1300–1302. [Google Scholar] [CrossRef]
  13. Villéger, S.; Mason, N.W.H.; Mouillot, D. New Multidimensional Functional Diversity Indices for a Multifaceted Framework in Functional Ecology. Ecology 2008, 89, 2290–2301. [Google Scholar] [CrossRef] [PubMed]
  14. Laliberté, E.; Legendre, P. A distance-based framework for measuring functional diversity from multiple traits. Ecology 2010, 91, 299–305. [Google Scholar] [CrossRef]
  15. Manson, N.W.H.; Bello, F.; Mouillot, D.; Pavoine, S.; Dray, S. A guide for using functional diversity indices to reveal changes in assembly processes along ecological gradients. J. Veg. Sci. 2013, 24, 794–806. [Google Scholar] [CrossRef]
  16. Vejrikova, I.; Eloranta, A.P.; Vejrik, L.; Smejkal, M.; Cech, M.; Sajdlová, Z.; Frouzová, J.; Kiljunen, M.; Petarka, J. Macrophytes shape trophic niche variation among generalist fishes. PLoS ONE 2017, 12, e0177114. [Google Scholar] [CrossRef]
  17. Vogt, R.J.; Beisner, B.E.; Prairie, Y.T. Functional diversity is positively associated with biomass for lake diatoms. Freshw. Biol. 2010, 55, 1636–1646. [Google Scholar] [CrossRef]
  18. Ismael, D.; Valenti, W.C.; Matsumura-Tundisi, T.; Rocha, O. Biodiversidade do Estado de São Paulo, Brasil: Síntese do Conhecimento ao Final do Século XX. 4: Invertebrados de Água Doce, 1st ed.; Fapesp São Paulo: São Paulo, Brasil, 1999; p. 176. [Google Scholar]
  19. Rocha, C.M.C.; Lima, D.; Cunha, M.C.C.; Almeida, J.S. Aquatic macrophytes and trophic interactions: A scientometric analyses and research perspectives. Braz. J. Biol. 2019, 79, 617–624. [Google Scholar] [CrossRef]
  20. Alvares, C.A.; Stape, J.L.; Sentelhas, P.C.; de Moraes, G.; Leonardo, J.; Sparovek, G. Köppen’s climate classification map for Brazil. Meteorol. Z. 2013, 22, 711–728. [Google Scholar] [CrossRef]
  21. Lauridsen, T.L.; Pedersen, L.J.; Jeppesen, E.; Sondergaard, M. The importance of macrophyte bed size for cladoceran composition and horizontal migration in a shallow lake. J. Plankton Res. 1996, 18, 2283–2294. [Google Scholar] [CrossRef]
  22. Arcifa, M.S.; Rodrigues, R.A.; Perticarrari, A. Diel vertical migration of cladocerans in a tropical lake. Nauplius 2003, 11, 15–25. [Google Scholar]
  23. Maia-Barbosa, P.M.; Eskinazi-Santana, E.M.; Barbosa, F.A.R. Zooplankton composition and vertical distribution in a tropical lake (Dom Helvécio lake, Southeastern Brasil). Acta Limnol. Bras. 2003, 15, 65–74. [Google Scholar]
  24. Sendacz, S.; Kubo, E. Copepoda (Calanoida e Cyclopoida) de reservatórios do Estado de São Paulo. Bol. Inst. Pesca 1982, 9, 51–89. [Google Scholar]
  25. Reid, J.W. Chave de identificação e lista de referências bibliográficas para as espécies continentais sul-americanas de vida livre da ordem Cyclopoida (Crustacea, Copepoda). Bol. Zool. Univ. São Paulo 1985, 9, 17–143. [Google Scholar]
  26. Elmoor-Loureiro, L.M.A. Manual de Identificação de Cladóceros Límnicos do Brasil, 1st ed.; Editora Universa: São Paulo, Brasil, 1997; p. 155. [Google Scholar]
  27. McCauley, E. The estimation of the abundance and biomass of zooplankton in samples. In A Manual on Methods for the Assessment of Secundary Productivity in FreshWaters, 2nd.; Downing, J.A., Rigler, F.H., Eds.; Blackwell Scientific Publications: Oxford, UK, 1984; Volume 17, pp. 228–265. [Google Scholar]
  28. Barnett, A.J.; Finlay, K.B.; Beisner, E. Functional diversity of crustacean zooplankton communities: Towards a trait-based classification. Freshw. Biol. 2007, 52, 796–813. [Google Scholar] [CrossRef]
  29. DeMott, W.; Kerfoot, W.C. Competition among cladocerans: Nature of the interaction between Bosmina and Dapnhia. Ecology 1982, 63, 1949–1966. [Google Scholar] [CrossRef]
  30. Fryer, G. Evolution and the Adaptive Radiation in the Chydoridae (Crustacea, Cladocera): A Study in Comparative Functional Morphology and Ecology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1968, 254, 221–382. [Google Scholar] [CrossRef]
  31. Dole-Olivier, M.J.; Galassi, D.M.P.; Marmonier, P.; Creuzé Des ChâTelliers, M. The biology and ecology of lotic microcrustaceans. Freshw. Biol. 2000, 44, 63–91. [Google Scholar] [CrossRef]
  32. Orlova-Bienkowskaja, M.Y. Cladocera: Anomopoda, Daphiniidae: Genus Simocephalus. In Guides To identification of the Microinvertebrates of the Continental Waters of the World; Drumont, H.J.F., Ed.; Backhuys Publishers: Terneuzen, The Netherlands, 2001; pp. 1–127. [Google Scholar]
  33. Oksanen, J.; Blanchet, F.G.; Kindt, R.; Legendre, P.; Minchin, P.R.; O’hara, R.B.; Oksanen, M.J. Vegan: Community Ecology Package. R Package Version 2.0-9. 2013. Available online: https://www.researchgate.net/publication/304765105_vegan_Community_ecology_package_R_package_version_20-9_Computer_program_and_documentation_distributed_by_the_author (accessed on 6 November 2019).
  34. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2014; Available online: http://www.R-project.org/ (accessed on 6 November 2019).
  35. Laliberté, E.; Legendre, P.; Shipley, B.; Laliberté, M.E. Package ‘FD’. Measuring Functional Diversity from Multiple Traits, and Other Tools for Functional Ecology. 2014. Available online: https://mran.microsoft.com/snapshot/2014-11-17/web/packages/FD/FD.pdf (accessed on 6 November 2019).
  36. Gotelli, N.J.; Entsminger, G.L. Swap and fill algorithms in null model analysis: Rethinking the knight’s tour. Oecologia 2001, 129, 281–291. [Google Scholar] [CrossRef]
  37. Kembel, S.W.; Cowan, P.D.; Helmus, M.R.; Cornwell, W.K.; Morlon, H.; Ackerly, D.D.; Blomberg, S.P.; Webb, C.O. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 2010, 26, 1463–1464. [Google Scholar] [CrossRef]
  38. Wood, S.; Wood, M.S. Package ‘mgcv’. R Package Version. 2015, pp. 1–7. Available online: http://cran.uib.no/web/packages/mgcv/mgcv.pdf (accessed on 6 November 2019).
  39. Bolduc, P.; Bertolo, A.; Pinel-Alloul, B. Does submerged aquatic vegetation shape zooplankton community structure and functional diversity? A test with a shallow fluvial lake system. Hydrobiologia 2016, 778, 151–165. [Google Scholar] [CrossRef]
  40. Williamson, C.E. The swimming and feeding behavior of Mesocyclops. Hydrobiologia 1986, 134, 11–19. [Google Scholar] [CrossRef]
  41. Lansac-Thôa, F.V.; Velho, L.F.M.; Higuti, J.; Takahashi, E.M. Cyclopidae (Crustacea, Copepoda) from the upper Paraná river floodplain, Brazil. Braz. J. Biol. 2002, 62, 125–133. [Google Scholar] [CrossRef] [PubMed]
  42. Fryer, G. Functional Morphology and the Adaptive Radiation of the Daphniidae (Branchopoda: Anomopoda). Philos. Trans. R. Soc. Lond. B Biol. Sci. 1991, 331, 1–99. [Google Scholar] [CrossRef]
  43. Iglesias, C.; Goyenola, G.; Mazzeo, N.; Meerhoff, M.; Rodó, E.; Jeppesen, E. Horizontal dynamics of zooplankton in subtropical Lake Blanca (Uruguay) hosting multiple zooplankton predators and aquatic plant refuges. Hydrobiologia 2007, 584, 179–189. [Google Scholar] [CrossRef]
  44. Kuczynska-Kippen, N. The use of bdelloids in reference to rotifer biocoenotic indices as an indicator of the ecological state of small field water bodies: The effect of macrophytes, shading and trophic state of water. Ecol. Indicat. 2018, 89, 576–583. [Google Scholar] [CrossRef]
  45. González-Sagrario, M.L.A.; Balseiro, E.; Ituarte, R.; Spivak, E. Macrophytes as reguge or risky area for zooplankton: A balance set by littoral predacious macroinvertebrates. Freshw. Biol. 2009, 54, 1042–1053. [Google Scholar] [CrossRef]
  46. González-Sagrario, M.L.A.; Balseiro, E. The role of macroinvertebrates and fish in regulating the provision by macrophytes of refugia for zooplankton in a warm temperate shallow lake. Freshw. Biol. 2010, 55, 2153–2166. [Google Scholar] [CrossRef]
  47. Meerhoff, M.; Clemente, J.M.; Mello, F.T.; Iglesias, C.; Pedersen, A.R.; Jeppesen, E. Can warm climate-related structure of littoral predator assemblies weaken the clear water state in shallow lakes? Glob. Chang. Biol. 2007, 13, 1888–1897. [Google Scholar] [CrossRef]
  48. Williamson, C.E.; Reid, J. Copepoda. In Ecology and Classification of North American Freshwater Invertebrates; James, T., Covich, A.P., Eds.; Academic Press: Cambridge, MA, USA, 2001; pp. 915–954. [Google Scholar]
  49. Kraznai, E.; Borics, G.; Várbíro, G.; Abonyi, A.; Padisák, J.; Deák, C.; Tóthmérész, B. Characteristics of pelagic phytoplankton in shallow oxbow. Hydrobiologia 2010, 637, 173–184. [Google Scholar] [CrossRef]
  50. Meschiatti, A.J.; Arcifa, M.S.; Fenerich-Verani, N. Ecology of fish in oxbow lakes of Mogi-Guaçu River. In Estudos Integrados em Ecossistemas: Estação Ecológica de Jataí, 1st ed.; Santos, J.E., Pires, J.S.R., Eds.; Editora Rima: São Carlos, Brasil, 2000; pp. 817–830. [Google Scholar]
  51. Hévert, M.P.; Beisner, B.E.; Maranger, R. Linking zooplankton communities to ecosystem functioning: Toward an effect-trait framework. J. Plankton Res. 2016, 39, 3–12. [Google Scholar] [CrossRef] [Green Version]
Figure 1. Schematic of the experimental design indicating both treatment and zone of sampling in the mesocosms.
Figure 1. Schematic of the experimental design indicating both treatment and zone of sampling in the mesocosms.
Water 11 02423 g001
Figure 2. Relationships between: (a) species richness (S) and pH, adjusted R2 = 0.42; F3,22 = 214.59; (b) species richness (S) by treatment (S = 5.0131 + s(1.4836, Macro) + s(1.0, pH) + ai; ai N(0, 1.372)); (c) Shannon species diversity (H’) and pH, adjusted R2 = 0.3; F3,22 = 106.07; (d) Shannon species diversity (H’) by treatment (H = 0.852 + s(0.308, Macro) + s(1.0, pH) + ai; ai N(0, 0.357)); (e) functional richness (FRic) and conductivity, adjusted R2 = 0.29; F3,22 = 47.1; (f) functional richness (FRic) by treatment (FRic = 0.097 + s(0.0508, Macro) + s(1.0, Conduct.) + ai; ai N(0, 0.0403)); (g) functional dispersion (FDis) and temperature, adjusted R2 = 0.26; F3,22 = 90.81; (h) functional dispersion (FDis) by treatment (FDis = 0.122 + s(0.0519, Macro) + s(1.0, Temp.) + ai; ai N(0, 0.0572)). Obs.: only statistically significant results are shown; other variables presented in the Supplementary Materials (Tables S1–S5).
Figure 2. Relationships between: (a) species richness (S) and pH, adjusted R2 = 0.42; F3,22 = 214.59; (b) species richness (S) by treatment (S = 5.0131 + s(1.4836, Macro) + s(1.0, pH) + ai; ai N(0, 1.372)); (c) Shannon species diversity (H’) and pH, adjusted R2 = 0.3; F3,22 = 106.07; (d) Shannon species diversity (H’) by treatment (H = 0.852 + s(0.308, Macro) + s(1.0, pH) + ai; ai N(0, 0.357)); (e) functional richness (FRic) and conductivity, adjusted R2 = 0.29; F3,22 = 47.1; (f) functional richness (FRic) by treatment (FRic = 0.097 + s(0.0508, Macro) + s(1.0, Conduct.) + ai; ai N(0, 0.0403)); (g) functional dispersion (FDis) and temperature, adjusted R2 = 0.26; F3,22 = 90.81; (h) functional dispersion (FDis) by treatment (FDis = 0.122 + s(0.0519, Macro) + s(1.0, Temp.) + ai; ai N(0, 0.0572)). Obs.: only statistically significant results are shown; other variables presented in the Supplementary Materials (Tables S1–S5).
Water 11 02423 g002
Figure 3. Mean logarithmic densities (± Standard Error (SE)) of functional traits in the littoral and pelagic habitats by macrophyte treatment.
Figure 3. Mean logarithmic densities (± Standard Error (SE)) of functional traits in the littoral and pelagic habitats by macrophyte treatment.
Water 11 02423 g003
Figure 4. Mean logarithmic densities (± SE) by species in the littoral and pelagic habitats by macrophyte treatment.
Figure 4. Mean logarithmic densities (± SE) by species in the littoral and pelagic habitats by macrophyte treatment.
Water 11 02423 g004
Figure 5. Box plots showing the means and standard errors of rankings of standardized effect sizes (SES) for functional diversity comparing the two treatments (p-value < 0.001).
Figure 5. Box plots showing the means and standard errors of rankings of standardized effect sizes (SES) for functional diversity comparing the two treatments (p-value < 0.001).
Water 11 02423 g005
Table 1. Microcrustacean functional traits and their abbreviations.
Table 1. Microcrustacean functional traits and their abbreviations.
Feeding TypesAbbreviations
Daphnia filtrationd.filt
Sida filtrations.filt
Bosmina filtrationb.filt
Raptorialraptorial
Stationary suspensionstat.susp
Burrowingburrow
Attachedattach
Size Class
0.1 to 0.5 mmclass A
0.6 to 1.0 mmclass B
1.1 to 1.5 mmclass C
1.6 to 2.0 mmclass D
Habitat Preference
Benthicbenthic
Open wateropen.water
Vegetationvegetation
Open water vegetationopen.water.vegetation
Trophic Group
Herbivoreherb
Herbivore–detritivoreherb.detr
Omnivoreomnivore
Omnivore–carnivoreomnivore.carnivore
Table 2. List of microcrustacean species found in the experimental mesocosms and their abbreviations.
Table 2. List of microcrustacean species found in the experimental mesocosms and their abbreviations.
CladoceransAbbreviation
Diaphanosoma spinulosum Herbst, 1967disp
Pseudosida bidentata Herrick, 1884psbi
Bosmina longirostris (O. F. Muller, 1785)bolo
Moina minuta Hansen, 1889momi
Ceriodaphnia cornuta Sars, 1886ceco
Simocephalus serrulatus (Koch, 1841)sise
Ilyocryptus spinifer Herrick, 1882ilsp
Macrothrix paulensis (Sars, 1901)mapa
CopepodsAbbreviation
Thermocyclops decipiens female (Kiefer, 1929)thdef
Thermocyclops decipiens malethdem
Mesocyclops meridianus female (Kiefer, 1926)mesmef
Mesocyclops meridianus malemesmem
Argyrodiaptomus furcatus female (Sars, 1901)arfuf
Argyrodiaptomus furcatus malearfum
Notodiaptomus iheringi female (Wrigth, 1935)noihf
Notodiaptomus iheringi malenoihm
Calanoid copepodidcoca
Cyclopoid copepodidcocy
Copepod naupliinaup
Table 3. Two-way ANOVA results comparing log density of each functional group by treatment (with macrophytes and control), by zones (littoral and pelagic), and for the interaction of treatment and zone. Trait abbreviations as in Table 1.
Table 3. Two-way ANOVA results comparing log density of each functional group by treatment (with macrophytes and control), by zones (littoral and pelagic), and for the interaction of treatment and zone. Trait abbreviations as in Table 1.
Functional TraitTreatmentZoneTreatment × Zone
FpdfFpdfFpdf
Feeding Types
attached5.9230.01917.5700.009110.7100.0021
b.filtr12.5260.0011--1--1
burrow12.9720.00114.1110.0491--1
d.filtr--1--1--1
raptorial--1--1--1
s.filtr--1--1--1
stat.susp4.5450.0391--1--1
Habitat Preference
benthic12.9720.00114.1110.0491--1
open.water5.3780.0251--1--1
open.water.vegetation--1--1--1
vegetation4.3050.041--1--1
Trophic Group
herb--1--1--1
herb.detr12.9720.00114.1110.0491--1
omnivore7.1960.0101--1--1
omnivore.carnivore14.243<0.0011--1--1
Size Class
class.A--1--1--1
class.B--1--1--1
class.C--1--1--1
class.D118.521<0.0011--1--1
Table 4. Two-way ANOVA results comparing log species density by treatment (with macrophytes and control), by zone (littoral and pelagic), and for the interaction of treatment and zone. Trait abbreviations as in Table 2.
Table 4. Two-way ANOVA results comparing log species density by treatment (with macrophytes and control), by zone (littoral and pelagic), and for the interaction of treatment and zone. Trait abbreviations as in Table 2.
SpeciesTreatmentZoneTreatment × Zone
FpdfFpdfFpdf
Disp--1--1--1
Bolo12.526<0.0011--1--1
Mapa20.444<0.0011--14.0330.0501
Ilsp8.2560.00617.3450.0091--1
Psbi11.1390.00114.1870.04614.1870.0461
Momi--1--1--1
Sise5.9230.01917.570.008110.710.0021
Ceco9.1240.0041--1--1
Noihm--1--1--1
Noihf--1--1--1
Arfuf118.521<0.0011--1--1
Arfum56.446<0.0011--1--1
Thdef--1--1--1
Naup7.5150.0081--1--1
Cocy1.2230.0081--1--1
Coca--1--1--1

Share and Cite

MDPI and ACS Style

Stephan, L.R.; Beisner, B.E.; Oliveira, S.G.M.; Castilho-Noll, M.S.M. Influence of Eichhornia crassipes (Mart) Solms on a Tropical Microcrustacean Community Based on Taxonomic and Functional Trait Diversity. Water 2019, 11, 2423. https://0-doi-org.brum.beds.ac.uk/10.3390/w11112423

AMA Style

Stephan LR, Beisner BE, Oliveira SGM, Castilho-Noll MSM. Influence of Eichhornia crassipes (Mart) Solms on a Tropical Microcrustacean Community Based on Taxonomic and Functional Trait Diversity. Water. 2019; 11(11):2423. https://0-doi-org.brum.beds.ac.uk/10.3390/w11112423

Chicago/Turabian Style

Stephan, Lígia R., Beatrix E. Beisner, Samuel G. M. Oliveira, and Maria Stela M. Castilho-Noll. 2019. "Influence of Eichhornia crassipes (Mart) Solms on a Tropical Microcrustacean Community Based on Taxonomic and Functional Trait Diversity" Water 11, no. 11: 2423. https://0-doi-org.brum.beds.ac.uk/10.3390/w11112423

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop