Functional Response of Aquatic Macroinvertebrate Communities to Temporality in Tropical Temporary Ponds
by
, ,
Aliano J. Tette-Pomárico
1,*,
Cesar E. Tamaris-Turizo
1,
Ángela J. Motta Diaz
2 and
Pedro Eslava-Eljaiek
1 1
Grupo de Investigación en Biodiversidad y Ecología Aplicada, Universidad del Magdalena, Santa Marta 470003, Colombia
2
Unidad de Ecología en Sistemas Acuáticos, University Pedagógica y Tecnológica de Colombia, Tunja 150009, Colombia
*
Author to whom correspondence should be addressed.
Water 2023, 15(15), 2753; https://doi.org/10.3390/w15152753
Submission received: 31 May 2023
/
Revised: 22 June 2023
/
Accepted: 26 June 2023
/
Published: 29 July 2023
(This article belongs to the Special Issue Freshwater Biodiversity: Conservation and Management)
Abstract
:Temporary or stationary wetlands (ponds) are bodies of shallow water that experience periodic droughts and an irregular flood cycle throughout the year. Although these wetlands are widely distributed in the Colombian territory, there have been few studies on their ecology. The aim of this research is to determine the effects of hydroperiod on the functional diversity of aquatic and semiaquatic macroinvertebrates in five temporary ponds in the department of Magdalena (Colombia). The samplings were performed during the hydroperiods of the filling and drying phases. Samples were collected from all the microhabitats present (sediment, littoral, and limnetic zones). Correlation analyses were performed between the traits and sites in the two hydroperiods, and a multidimensional and comparative analysis of functional diversity was performed, where indices of distance, richness, and functional dispersion were calculated in each hydroperiod. Statistical differences in functional replacement were found for only one of the ponds; however, the other ponds showed a similar trend. These results fit the functional turnover ecological hypothesis in that the response of the aquatic and semiaquatic macroinvertebrate communities was associated with the hydroperiod of the ponds based on the habitat “templet” theory.
1. Introduction
Wetlands are strategic ecosystems that provide ecosystem services such as water regulation, nutrient retention and export, terrestrial biomass decomposition, and biodiversity reservoirs [1,2,3,4]. Among these ecosystems, temporary wetlands, also known as temporary or stationary ponds, are natural water bodies that experience periodic droughts, with an interannual irregular flood cycle that depends on the topography and soil composition [1,5]. The rapid fluctuations in water level and the variable duration of the hydroperiod determines the establishment of a distinct biota. This biota is characterized by its ability to adapt, employ dispersal mechanisms, and exhibit specific life histories that enable survival during drought periods [1,5]. In support of this idea, Southwood [6] proposes the habitat “temple” theory, which suggests that community structure is determined by environmental conditions. For example, monocyclic diaptomids (Copepoda) rapidly develop after the flood phase; brachiopods (anostraceans, notostraceans, and conchostraceans) have diapause eggs that resist drought periods; and coleopterans, dipterans, hemipterans, and odonates have broad dispersal strategies [1,5,7,8].
Among the faunal groups found in temporary ponds, aquatic macroinvertebrates are the most abundant and diverse [1,9]. These communities have been widely studied due to their sensitivity to natural and anthropic environmental changes [10,11]. Many of the studies on aquatic macroinvertebrate communities have evaluated biological diversity from the perspective of community structure (richness and abundance). Recently, studies on these organisms have changed their focus to a functional approach, acknowledging their status as an important component of biodiversity and the variety of ways they interact with resources and their environment [12,13,14,15]. This approach uses the components of functional biodiversity to determine the functioning of an ecosystem [12,16,17]. One form of measurement is through functional traits, which are morphological, physiological, and/or ecological characteristics of organisms that affect their growth, reproduction, and survival [18].
Temporary ponds are highly susceptible to anthropic activities, such as livestock rearing, agriculture, transportation, and construction. These actions alter pond geomorphology, thereby affecting physicochemical and biological conditions [19]. Moreover, these ecosystems are regarded as climate change indicators due to their sensitivity to changes in hydroperiods [20]. In Colombia, it has been estimated that temporary wetlands cover more than 17 million hectares, but the scarcity of scientific studies on these ecosystems poses a challenge to formulating policies and management strategies [4].
The present study aims to comprehend the effects of temporality on the functional diversity of aquatic macroinvertebrates in the temporary ponds. Our hypothesis is that the biological composition of aquatic macroinvertebrates undergoes changes in both abundance and diversity as the water level fluctuates in these ponds. Consequently, we expect shifts in biological traits, such as a transition from a high abundance of organisms with gills during the filling phase of the pond to a high abundance of organisms with skin adaptation during the drought period.
2. Materials and Methods
Study area: Samples were collected from five temporary ponds in the department of Magdalena: three were in the central zone (P1, P2, and P3) of the department, and two were in the southern zone (P4 and P5) (Figure 1; Table A3). The soil around the ponds is used for grazing cattle, except in P4, where the soil is used for farming. The climate regime in the central zone is bimodal, with two dry periods (a strong drought between December and March and a slight drought between June and July) and two rainy seasons (one mild, between April and May, and a strong one between August and November). However, in the southern zone of Magdalena, the climatic regime is monomodal, with a well-marked dry season between December and March and continuous rains between April and November [21].
Sampling: Sampling was carried out during the period when the pond water level increased—filling phase (November 2020), and sampling also occurred during the period when the water level decreased—drying phase (February 2021). At each visit, three replicates of sediment from the center of the water body and three replicates from the limnetic and littoral zones were obtained. The sediment was collected approximately in the limnetic zone with an Ekman dredge (866 cm3). In the littoral and limnetic zones, a 2 m transect parallel to the line shore was established, where the macroinvertebrates were collected using a type D manual net (with a net opening of 250 µm). Subsequently, a linear sweep was performed in the littoral zone, while a zigzag sweep was conducted in the limnetic zone within a 2 m2 area [22]. The samples were deposited in high-density plastic bags previously labelled and preserved in 96% ethanol. In the laboratory, all samples were separated manually. The sediment samples were passed through a 300 µm sieve. The macroinvertebrates were preserved in 70% ethanol and identified in a Carl Seizz Stemi 508 stereoscope based on taxonomic keys and reference documents [9,23,24,25].
Environmental variables: Physical and chemical variables, such as dissolved oxygen concentration (mg/L O2), temperature (°C), acidity (pH), total dissolved solids (mg/L), turbidity (formazin nephelometric units—FNU), and conductivity (µS/cm), were measured in situ using Hanna H19829 multiparameter equipment. In addition, water samples were collected in plastic bottles, which were stored in a plastic refrigerator at 4 °C and transported to the laboratory, where nitrite concentrations (mg/L NO2) were measured using the 1.00609.0001 cuvette test and orthophosphates (mg/L PO4-P) were measured with the Merk test 1.14842.0001, whose readings were performed via the photometric method using the Spectroquant® Move 100.
Data analysis: To characterize the physicochemical variables in the ponds and their relationship with the two phases of the hydroperiod, a principal component analysis (PCA) was performed after transforming the data to log (x) +1. Then, the multicollinearity of the variables was quantified through the variance inflation factor (VIF), taking as a critical value a VIF > 20, which allowed the detection of high multicollinearity in turbidity (VIF = 31.57), conductivity (VIF = 42.44), orthophosphates (VIF = 23.22), and dissolved oxygen (VIF = 23.26); the last two variables were conserved in the analysis given their importance in explaining the biological processes of the ecosystem, and conductivity and turbidity were removed. Additionally, a state of eutrophication was assigned based on the values of PO4-P following the categorization of Moreno-Franco et al. [26].
The functional traits of the organisms were selected based on their possible relationship with the temporality of the ecosystem and environmental variables considering the approaches of Beche et al. [27], Bonada et al. [12], and Motta-Diaz et al. [14]. In total, there were 63 attributes of twelve functional traits, grouped into four categories: three traits related to the life cycle, one reproductive trait, five behavioral and physiological traits, and three morphological traits (Table A1). Each taxon was assigned a score by attribute according to the fuzzy method and by taking into account that some taxa can have more than one attribute; this process consisted of assigning each attribute a value between 0 and 3, where 0: no affinity, the taxon had no affinity with the trait modality; 1: weak affinity, a weak affinity was previously observed or mentioned in the literature, but it was not observed in recent data; 2: moderate affinity, a moderately strong affinity was observed; and 3: strong affinity, a close relationship with the attribute was evidenced [28,29].
The representativeness of the samplings was estimated by the sample coverage (qC) taking into account the abundance and richness data using the iNEXT statistical package [30,31]. Subsequently, the graphic hypothesis proposed by Boersma et al. [32] was evaluated, performing a nonmetric multidimensional scaling analysis (nMDS) using the Gower distance to describe the functional diversity of each community in a “multidimensional functional space” with two axes. Next, as metrics of the communities, the indices for each replicate were estimated: functional distance—FDist [32], functional richness—FRic [33], and functional dispersion—FDis [34]. The FDist involved applying the Markov Chain Monte Carlo (MCMC) algorithm between the functional centroids of each hydroperiods. Next, Welch’s t-test was applied for FRic and FDisp to detect significant differences between the two hydroperiods [35]. Subsequently, to evaluate the association between the different categories of the traits with season and temporality, a fuzzy correspondence analysis (FCA) was performed. Finally, to identify relationships between traits and environmental variables, canonical correspondence analysis (CCA) was performed between functional traits, sampling stations, and physicochemical variables.
All analyses were performed in R Studio 4.1.0. To perform the PCA, the FactoMineR package was used; the functional analyses were developed with FD; the MCMC was executed with MCMCglmm; for the FCA, the ade4 was used; and for the ACC and the NMDS, the VEGAN package was used [36].
3. Results
3.1. Temporal Variation of Environmental Variables
Physicochemical variables did not exhibit any relationship with the distribution and temporarily of the ponds. However, evident temporal changes in the environmental variables were observed when comparing the drying and filling phases in each individual pond (Figure 2). Among the variables, orthophosphates, dissolved oxygen, and temperature showed the strongest correlation with temporal variation in ponds 1, 3, and 5. Ponds 3 and 5 showed the highest values of dissolved oxygen at 2.8 and 1.7 mg/L and the lowest concentrations of orthophosphates (0.1 and 0.13 mg/L, respectively) during the drying phase. In contrast, in pond 1, the maximum values of dissolved oxygen (2.5 mg/L), temperature (°C), and nitrites (4.4 mg/L) were observed during the filling phase (Table 1).
3.2. Effect of Temporality on Functional Diversity of Temporary Ponds
The aquatic macroinvertebrate communities consisted of 55 genera, grouped into 34 families and 12 orders. The sample coverage in each pond was between 0.95 and 0.98, which indicated that the samples were representative at each site and in the two climatic periods (Table 2). Thus, the probability of finding a new individual of a different taxon in any of the ponds was less than 5%.
The composition of aquatic macroinvertebrates exhibited variation during the filling and drying phases. In the filling phase, the proportions of Diptera increased in the stations located further south, while in the drying phase, they showed higher abundance in the stations further north. Additionally, Hemiptera accounted for 18% to 26% of the community during the filling phase, and between 2.3% and 6.9% during the drying phase (Figure A1). These findings suggest a notable fluctuation in the presence and distribution of these taxonomic groups, highlighting their response to the two phases evaluated in temporary ponds.
Broad functional distance in the communities of macroinvertebrates along the ponds indicate a high replacement of taxa, especially in pond 4, due to the absence of zero in the functional centroid in the credible interval in the MCMC (Table 3). However, when considering the comprehensive dataset, which includes information gathered from ponds, the credible interval in the MCMC also excluded zero. Pond 4 presented 13 taxa shared over the two hydroperiods, 10 exclusive taxa in the filling phase (7 Coleoptera, 1 Lepidoptera, 1 Rhynchobdela, and 1 Decapoda), and 11 exclusive taxa in the drying phase (4 Coleoptera, 3 Odonata, 2 Diptera, 1 Basommatophora, and 1 Diplostraca—Cyclestheria sp.).
Some changes were observed in the functional volume at the following sites: in pond 1, which were explained because Cyclestheria sp. (Diplostraca) and Clamidoteca sp. (Ostracoda) only were found during the filling phase, while Pomacea sp. (Architaenioglossa) and Ora sp. (Coleoptera) were present during the drying phase, generating an increase in functional volume (Figure 3, Table A2). In pond 2, the dipterans Chironomus sp. and Tabanus sp., and the beetle Ora sp., were reported during the drying phase, increasing the functional richness in this period (Figure 3). In addition, a change in abundance of some taxa between the two phases were observed. However, the Welch’s t-test of the indices of FRic and FDisp did not show differences between the hydroperiods (p > 0.05) at any pond (Table 4 and Table 5). This trend was maintained when analyzing the data as a whole, considering the information gathered from ponds.
3.3. Functional Traits and Temporality
The analysis of life cycle traits revealed a consistent temporal pattern among the studied ponds, with no significant changes observed. Ponds 1 and 4 was characterized by the presence of univoltine organisms (c2), indicating a single reproductive cycle within each period (Figure 4). In contrast, ponds 2 and 5 sustained populations of multivoltine organisms in both hydroperiods. Notably, during the filling phase, pond 3 exhibited a distinct pattern with a significant predominance of multivoltine organisms (c3).
Regarding reproductive traits, organisms with endophytic eggs (d8) and isolated cemented eggs (d3) dominated in ponds 1 and 4 during the filling phase. During the drying phase, in pond 1, the organisms with cemented nested eggs (d4) were the most representative, and in pond 6, the organisms with eggs were in free clutches (d5).
The traits associated with behavioral and physiological aspects showed temporal variation in pond 4. During the filling phase, predators (g6) that fed on macroinvertebrates (h7), with cutaneous respiration (e1) and habitat preference of macrophytes, dominated. (i3). During the drying phase, complete swimmers (f3) with gill respiration (e2) were more abundant. Pond 5 presented the highest number of filter feeders (g2) in the filling phase and organisms that breathe through specialized structures such as plastron (e4) in the drying phase. Regarding the morphological traits, it was observed that the organisms without body armor (j3) were mainly associated with pond 4 in the drying phase, and those with cylindrical bodies (l3) dominated in pond 5 in the filling phase.
3.4. Correlation of Environmental Variables and Functional Traits
The morphological and life cycle traits did not show associations with environmental variables measured. However, the attributes of asexual and ovoviviparous reproduction were associated with dissolved oxygen and water temperature. Regarding the behavioral traits and physiological aspects, a dominance of organisms that feed on coarse detritus (h3) with high concentrations of nitrites was observed, while those that feed on sediment particles (h1) were associated with high values of total dissolved solids (Figure 5).
4. Discussion
Our results partially supported our hypothesis. Although most stations did not show significant changes, in the nMDS, there was a tendency to separate the abundance of each hydroperiod in the multidimensional functional space. In fact, pond 4 and the joint analysis of all the data (all) showed evidence of an environmental filter effect on the functional diversity of the macroinvertebrate community. In this way, in pond 4 and y, a greater abundance of predatory organisms and reproduction by endophytic eggs were observed in the filling phase, and these attributes were typical of the most abundant groups in this period, such as coleopterans, odonates and Hemiptera; however, in the drying phase, a greater abundance of organisms without body shielding (Diptera) was observed. These results support a “functional rotation” effect induced by pond hydroperiod, which is common in ecological succession processes [32]. Similarly, these findings are consistent with those of Southwood [6] and the theory of habitat “templet”, in which the habitat acts as a filter that allows the persistence of functional traits that best adjust to the environmental conditions that occur independently of the number of species.
Pond 4 was smaller (0.03 ha) and was completely exposed to solar radiation, so the environmental filter had an early effect on its community [1]. In addition, the climatic effects on the functional diversity of the other ponds were not significant because by being larger, the impact of the climate on the ponds was smaller, and therefore, the filter effect would have been reflected in a period after that evaluated in this study. However, it is necessary to evaluate the relationship of the physical variables associated with the hydroperiod (such as area, depth, and soil type) to verify this trend.
The variables that best explained the differentiation of the ponds with respect to the hydroperiod in the PCA were orthophosphates, whose values at the sites oscillated between the ranges corresponding to mesotrophic and hypertrophic systems [26], except for pond 1, which presented characteristic values of oligotrophic systems. The values of orthophosphates could be an effect of the presence of livestock (ponds 2, 3 and 5) and agriculture in the surrounding area (pond 4), given that these areas contain many products with high concentrations of macronutrients that promote eutrophication and anoxia in temporary ponds [19]. However, the CCA did not show an association of any of the traits used with orthophosphates, which suggests that this variable did not have an effect related to temporality on the functional diversity of the aquatic macroinvertebrates.
The low variability observed in the metrics of functional diversity with respect to the hydrological periods in most of the ponds studied shows that the functional diversity is relatively resistant to the temporality of the bodies of water conferring stability to the ecosystem, as has been verified in temporary lotic systems [12,37]. Culioli et al. [38] noted that when a temporary pond in the region of Corsica (France) reaches a maximum fill level, the structure of the aquatic macroinvertebrate community is stabilized and mainly dominated by predators such as odonates and coleopterans and remains in that state until the drying phase, when most predators begin to leave the pond.
There was no significant correlation found between temporal variability and life cycle traits in most ponds, except for pond 3, where a transition from multivoltine to univoltine attribute was observed between the filling and drying phase. This finding aligns with expectations in tropical ecosystems, where minimal variation in temperature and light conditions leads to continuous periods of growth and reproduction in aquatic macroinvertebrates, resulting in overlapping generations of both univoltine and multivoltine organisms [39]. However, in tropical temporary lotic systems, voltinism is an important functional trait of the variability in the functional diversity of aquatic macroinvertebrates during the different seasons because it is a trait sensitive to niche availability [14,39,40]. Batzer and Wissinger [41] warned that there are aspects of wetland insect ecology that should be reevaluated since much of the information originates from lotic ecosystems. However, Layton and Voshell [42] evaluated the colonization of aquatic macroinvertebrates in experimental temporary wetlands in Virginia (United States) during the four main seasons and considered voltinism an important factor affecting the structure of communities. These wetlands were oligotrophic without fish and low levels of nutrients and organic matter. Therefore, we recommend that the ecological aspects of aquatic and semiaquatic macroinvertebrate communities in temporary wetlands continue to be evaluated in the tropics, where environmental and climatic conditions are different from those in temperate zones.
In this study, it was observed that the change in hydroperiod did not have a significant effect on the functional diversity of the macroinvertebrate community. However, a functional turnover was identified during the two hydroperiod evaluated, both in pond 4 and in the overall analysis of all ponds. Also, certain biological traits, such as feeding mode, body armor, reproductive type, and voltinism, were found to be related to the variation in hydroperiod in the studied ponds. These findings highlight the importance of including these traits in future studies addressing the effect of hydroperiod on the biological function of temporary ponds in the Neotropics.
Supplementary Materials
The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/w15152753/s1.
Author Contributions
Conceptualization, and methodology A.J.T.-P. and C.E.T.-T.; software, A.J.T.-P. and Á.J.M.D.; validation, all authors; formal analysis, A.J.T.-P., C.E.T.-T. and Á.J.M.D.; resources, P.E.-E. and C.E.T.-T.; writing—original draft preparation and writing—review and editing, all authors; visualization, A.J.T.-P. and Á.J.M.D.; supervision and project administration, P.E.-E. and C.E.T.-T. All authors have read and agreed to the published version of the manuscript.
Funding
This investigation was financed with funding from Universidad del Magdalena and Patrimonio Autonómo Fondo Nacional De Financiamiento Para La Ciencia, La Tecnología Y La Innovación Francisco José Caldas.
Data Availability Statement
All data is disponible in the appendix and as supplementary data.
Acknowledgments
We thank the owners of the farms Villa Leydi (Municipality of Pivijay), Los Trillizos (Municipality of Pivijay), El Paraíso (Municipality of Pivijay), El miquito (Municipality of Nueva Granada), and La Dicha (Municipality of EL Dificil) for allowing us to carry out this study in the wetlands within their properties. We thank the following researchers for their guidance in determining functional traits in their expert groups: Juan Ignacio Urcola, Matthew Pintar, Marcela González Córdoba, Nicolas Rabet, and Alejandro Oceguera Figueroa. We thank Daniel Serna and Jorge Oliveros for their important work in collecting biological material and identifying taxa.
Conflicts of Interest
The authors have no conflict of interest to declare that are relevant to the content of this article.
Appendix A
Table A1.
Functional traits and attributes of aquatic macroinvertebrates following the proposal by Motta –Díaz et al. [14] and Beche et al., 2006 [27].
| Trait Type | Functional Trait | Attribute | Symbol |
|---|---|---|---|
| Life cycle | Aquatic stage | Egg | a1 |
| Larva and/or pupa | a2 | ||
| Adult | a3 | ||
| Forms of resistance | Statoblast | b1 | |
| Gemmule | b2 | ||
| Cocoon | b3 | ||
| Cells against dehydration | b4 | ||
| Diapause or latency | b5 | ||
| Voltinism | Semivoltine | c1 | |
| Univoltine | c2 | ||
| Multivoltine | c3 | ||
| Reproductive | Reproduction | Ovoviviparous | d1 |
| Free isolated eggs | d2 | ||
| Segmented isolated eggs | d3 | ||
| Segmented nested eggs | d4 | ||
| Free-nested eggs | d5 | ||
| Eggs nested in vegetation | d6 | ||
| Terrestrial nested eggs | d7 | ||
| Endophytic eggs | d8 | ||
| Asexual reproduction | d9 | ||
| Behavioral and Physiological | Breathing | Cutaneous | e1 |
| Gills | e2 | ||
| Plastron | e3 | ||
| Aerial | e4 | ||
| Respiratory pigments | e5 | ||
| Locomotion | Flying | f1 | |
| Surface swimmer | f2 | ||
| Complete swimmer | f3 | ||
| Walker | f4 | ||
| Epibenthic excavator | f5 | ||
| Endobenthic excavator | f6 | ||
| Temporarily fixed to the substrate | f7 | ||
| Feeding mode | Collector | g1 | |
| Filter | g2 | ||
| Shedder | g3 | ||
| Scraper | g4 | ||
| Perforator | g5 | ||
| Predator | g6 | ||
| Food | Sediment particles | h1 | |
| Fine debris | h2 | ||
| Coarse debris | h3 | ||
| Microphytes | h4 | ||
| Macrophytes | h5 | ||
| Microinvertebrates | h6 | ||
| Macroinvertebrates | h7 | ||
| Vertebrates | h8 | ||
| Dead animals | h9 | ||
| Habitat preference | Sediment | i1 | |
| Leaf litter | i2 | ||
| Macrophytes | i3 | ||
| Rocks | i4 | ||
| Branches | i5 | ||
| Water surface | i6 | ||
| Morphological | Body armor | Sclerotized body | j1 |
| Strong case/shell | j2 | ||
| Without adaptation | j3 | ||
| Maximum size | <2.5 mm | k1 | |
| 2.5–5 mm | k2 | ||
| 5–10 mm | k3 | ||
| 11–20 mm | k4 | ||
| 21–40 mm | k5 | ||
| 41–80 mm | k6 | ||
| Body shape | Aerodynamic | l1 | |
| Flattened | l2 | ||
| Cylindrical | l3 | ||
| Spherical | l4 |
Appendix B
Figure A1.
Composition of the orders of aquatic macroinvertebrates in five temporary ponds located in the north of Colombia. It presents data for two distinct phases: the filling phase (A) and the drying phase (R). (A) pond 1; (B) pond 2; (C) pond 3; (D) pond 4; (E) pond 5.
Figure A1.
Composition of the orders of aquatic macroinvertebrates in five temporary ponds located in the north of Colombia. It presents data for two distinct phases: the filling phase (A) and the drying phase (R). (A) pond 1; (B) pond 2; (C) pond 3; (D) pond 4; (E) pond 5.
Table A2.
List of taxa found in the ponds during the two phases of the hydroperiod. A: Filling phase; R: drying phase.
Table A2.
List of taxa found in the ponds during the two phases of the hydroperiod. A: Filling phase; R: drying phase.
| Order | Species | P1 | P2 | P3 | P4 | P5 | |||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| A | R | A | R | A | R | A | R | A | R | ||
| Architaenioglossa | Marisa sp. | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| Pomacea sp. | 0 | 5 | 3 | 2 | 0 | 0 | 0 | 0 | 0 | 0 | |
| Basommatophora | Biomphalaria sp. | 0 | 30 | 18 | 136 | 88 | 96 | 19 | 8 | 6 | 128 |
| Physa sp. | 0 | 0 | 13 | 29 | 6 | 12 | 0 | 12 | 2 | 36 | |
| Coleoptera | Anodocheilus sp. | 0 | 0 | 0 | 2 | 0 | 1 | 0 | 0 | 0 | 0 |
| Berosus sp. | 4 | 0 | 1 | 2 | 0 | 0 | 0 | 0 | 0 | 0 | |
| Canthydrus sp. | 0 | 12 | 0 | 2 | 0 | 4 | 0 | 2 | 0 | 0 | |
| Copelatus sp. | 0 | 1 | 0 | 3 | 0 | 3 | 1 | 1 | 0 | 1 | |
| Cybister sp. | 2 | 0 | 0 | 0 | 1 | 0 | 1 | 0 | 1 | 0 | |
| Derallus sp. | 0 | 10 | 0 | 24 | 0 | 5 | 0 | 7 | 0 | 8 | |
| Desmopachria sp1 | 1 | 0 | 0 | 3 | 0 | 0 | 2 | 0 | 0 | 2 | |
| Desmopachria sp2 | 0 | 12 | 0 | 0 | 0 | 2 | 2 | 0 | 0 | 0 | |
| Helochares sp1 | 0 | 2 | 0 | 7 | 0 | 0 | 0 | 0 | 0 | 0 | |
| Helochares sp2 | 0 | 14 | 0 | 18 | 0 | 7 | 0 | 5 | 0 | 10 | |
| Hydrocanthus sp1 | 20 | 19 | 6 | 8 | 27 | 19 | 9 | 2 | 9 | 11 | |
| Hydrocanthus sp2 | 3 | 17 | 0 | 2 | 0 | 2 | 1 | 0 | 1 | 0 | |
| Hydrochus sp | 1 | 0 | 0 | 0 | 0 | 0 | 4 | 0 | 0 | 0 | |
| Hydrovatus sp | 0 | 9 | 0 | 5 | 0 | 0 | 0 | 0 | 0 | 0 | |
| Laccophilus sp1 | 8 | 5 | 0 | 2 | 9 | 1 | 0 | 0 | 1 | 1 | |
| Laccophilus sp2 | 2 | 5 | 0 | 6 | 0 | 3 | 10 | 0 | 2 | 0 | |
| Ora sp. | 0 | 7 | 0 | 10 | 0 | 2 | 0 | 5 | 0 | 0 | |
| Suphis sp. | 0 | 4 | 1 | 4 | 26 | 22 | 2 | 0 | 3 | 12 | |
| Suphisellus sp. | 0 | 3 | 0 | 8 | 0 | 0 | 0 | 0 | 0 | 0 | |
| Tanysphyrus sp. | 0 | 0 | 0 | 5 | 0 | 1 | 9 | 0 | 0 | 0 | |
| Thermonectus sp1 | 8 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 2 | 0 | |
| Thermonectus sp2 | 0 | 0 | 0 | 0 | 0 | 0 | 2 | 0 | 0 | 0 | |
| Tropisternus sp1 | 38 | 8 | 8 | 12 | 21 | 8 | 15 | 8 | 10 | 7 | |
| Tropisternus sp2 | 2 | 0 | 0 | 0 | 0 | 0 | 3 | 0 | 0 | 0 | |
| c.f.tormus sp. | 2 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| Decapoda | Bottiella sp. | 0 | 0 | 0 | 0 | 0 | 0 | 2 | 0 | 0 | 0 |
| Diplostraca | Cyclestheria sp. | 13 | 0 | 29 | 8 | 4 | 5 | 0 | 3 | 0 | 0 |
| Diptera | Ablabesmyia sp. | 11 | 20 | 3 | 34 | 5 | 22 | 17 | 24 | 0 | 14 |
| Chironomus sp. | 2 | 5 | 0 | 13 | 7 | 3 | 3 | 1 | 8 | 0 | |
| Culex sp1 | 4 | 4 | 0 | 8 | 3 | 0 | 0 | 15 | 7 | 0 | |
| Culex sp2 | 15 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 6 | |
| Culicoides sp. | 2 | 17 | 2 | 12 | 0 | 0 | 1 | 0 | 0 | 2 | |
| Mansonia sp. | 0 | 11 | 1 | 17 | 0 | 34 | 2 | 8 | 55 | 54 | |
| Odontomyia sp. | 0 | 0 | 1 | 0 | 0 | 0 | 0 | 8 | 0 | 8 | |
| Simulium sp. | 0 | 0 | 0 | 2 | 0 | 0 | 0 | 0 | 0 | 0 | |
| Tabanus sp. | 4 | 2 | 0 | 4 | 0 | 4 | 1 | 5 | 1 | 9 | |
| Tanytarsus sp. | 3 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| Ephemeroptera | Callibaetis sp. | 2 | 0 | 1 | 0 | 0 | 0 | 1 | 0 | 0 | 0 |
| Hemiptera | Belostoma sp. | 10 | 1 | 10 | 8 | 30 | 5 | 7 | 1 | 4 | 2 |
| Buenoa sp1 | 15 | 0 | 3 | 6 | 25 | 4 | 17 | 0 | 20 | 7 | |
| Buenoa sp2 | 4 | 0 | 0 | 0 | 3 | 0 | 0 | 0 | 0 | 0 | |
| Eurygerris sp. | 0 | 0 | 0 | 0 | 2 | 0 | 0 | 0 | 0 | 0 | |
| Hydrometra sp. | 0 | 0 | 0 | 0 | 2 | 0 | 0 | 0 | 0 | 0 | |
| Mesovelia sp. | 6 | 0 | 0 | 0 | 3 | 0 | 0 | 0 | 0 | 0 | |
| Microvelia sp. | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| Neoplea sp. | 17 | 2 | 2 | 2 | 0 | 0 | 0 | 0 | 1 | 1 | |
| Pelocoris sp. | 1 | 3 | 4 | 15 | 11 | 18 | 11 | 7 | 1 | 3 | |
| Ranatra sp. | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | |
| Lepidoptera | Samea sp. | 0 | 0 | 0 | 0 | 0 | 0 | 2 | 0 | 0 | 0 |
| Odonata | Acanthagrion sp. | 41 | 9 | 0 | 3 | 1 | 2 | 8 | 7 | 7 | 4 |
| Anax sp1 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 2 | 0 | |
| Anax sp2 | 0 | 0 | 0 | 1 | 0 | 2 | 0 | 0 | 0 | 1 | |
| Dythemis sp. | 3 | 7 | 0 | 14 | 0 | 19 | 0 | 8 | 0 | 6 | |
| Neoneura sp. | 16 | 10 | 24 | 35 | 1 | 46 | 16 | 26 | 10 | 7 | |
| Nephepeltia sp. | 1 | 7 | 0 | 11 | 0 | 14 | 0 | 7 | 6 | 13 | |
| Planiplax sp. | 0 | 0 | 2 | 0 | 0 | 10 | 0 | 0 | 0 | 0 | |
| Sympetrum sp. | 0 | 1 | 0 | 8 | 8 | 11 | 5 | 7 | 0 | 2 | |
| Tramea sp. | 3 | 0 | 4 | 18 | 10 | 5 | 0 | 0 | 4 | 0 | |
| Ostracoda | Chlamydoteca sp. | 13 | 0 | 0 | 3 | 0 | 13 | 11 | 19 | 1 | 3 |
| Rhynchobdellida | Helopdella sp. | 0 | 0 | 0 | 0 | 0 | 0 | 3 | 0 | 0 | 0 |
Appendix C
Table A3.
Coordinates and characteristics of the temporary pods studied.
| Pond | Location | Latitude | Longitude | Depth (m) | Aquatic Macophytes |
|---|---|---|---|---|---|
| P1 | Villa Leidy | 10°30′30.56″ N | 74°29′43.04″ O | <1 | Ludwigia helminthorrhiza and Marsilea vestita. |
| P2 | Los Trillizos | 10°27′52.15″ N | 74°25′52.63″ O | 0.5 | Salvinia rádula and Neptunia oleracea. |
| P3 | El Paraiso | 10°27′10.93″ N | 74°23′33.16″ O | >2 | Salvinia radula, Ludwigia helminthorrhiza and Hymenachne amplexicaulis. |
| P4 | El Miquito | 9°49′3.22″ N | 74°25′52.82″ O | 1 | Salvinia radula and Ludwigia helminthorrhiza. |
| P5 | La Dicha | 9°54′6.36″ N | 74°7′30.90″ O | 1.1 | Pistia stratiotes. |
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Figure 1.
Location of the temporary ponds in the Magdalena department (Colombia).
Figure 2.
Principal component analysis (PCA) of the environmental variables and temporary ponds. TDS: total dissolved solids; PO4-P: orthophosphates; O2: dissolved oxygen; NO2: nitrites. P: pond, A: filling phase; R: drying phase.
Figure 2.
Principal component analysis (PCA) of the environmental variables and temporary ponds. TDS: total dissolved solids; PO4-P: orthophosphates; O2: dissolved oxygen; NO2: nitrites. P: pond, A: filling phase; R: drying phase.
Figure 3.
Non–metric multidimensional scaling (nMDS) of the temporal variation of the functional diversity. Each circle is a taxon and the size is proportional to its abundance. Blue circle: ascent waters. Red circle: relegation waters.
Figure 3.
Non–metric multidimensional scaling (nMDS) of the temporal variation of the functional diversity. Each circle is a taxon and the size is proportional to its abundance. Blue circle: ascent waters. Red circle: relegation waters.
Figure 4.
Fuzzy correspondence analysis (FCA) of the functional traits and temporary ponds. P: pond, A: filling phase; R: drying phase. (A) Lifecycle: (1) aquatic stage: egg (a1), larvae and/or pupa (a2), and adult (a3); (2) resistance forms: statoblast (b1), gemmule (b2), cocoon (b3), cells against dehydration (b4), and diapause or dormancy (b5); (3) voltinism: semivoltine (c1), univoltine (c2), and multivoltine (c3). (B) Reproductive: ovoviviparous (d1), isolated free eggs (d2), isolated eggs, segmented (d3), segmented nested eggs (d4), free-nested eggs (d5), vegetation-nested eggs (d6), terrestrial nested eggs (d7), endophytic eggs (d8), and asexual reproduction (d9). (C). Behavioral and physiological: (1) breathing: cutaneous (e1), gills (e2), plastron (e3), aerial (e4), and respiratory pigments (e5); (2) locomotion: flyer (f1), surface swimmer (f2), all swimmer (f3), walker (f4), epibenthic burrower (f5), endobenthic burrower (f6), and temporarily fixed to the substrate (f7); (3) feeding: collector (g1), filter (g2), shedder (g3), scraper (g4), piercer (g5), and predator (g6); (4) food: sediment particles (h1), fine debris (h2), coarse debris (h3), microphytes (h4), macrophytes (h5), microinvertebrates (h6), macroinvertebrates (h7), vertebrates (h8), and dead animals (h9); (5) habitat preference: sediment (i1), leaf litter (i2), macrophytes (i3), rocks (i4), branches (i5), and water surface (i6). (D) Morphological: (1) body armor: sclerotized body (j1), strong case/shell (j2), and without adaptation (j3); (2) maximum size: <2.5 mm (k1), 2.5–5 mm (k2), 5–10 mm (k3), 11–20 mm (k4), 21–40 mm (k5), and 41–80 mm (k6); (3) body shape: streamlined (l1), flattened (l2), cylindrical (l3), and spherical (l4).
Figure 4.
Fuzzy correspondence analysis (FCA) of the functional traits and temporary ponds. P: pond, A: filling phase; R: drying phase. (A) Lifecycle: (1) aquatic stage: egg (a1), larvae and/or pupa (a2), and adult (a3); (2) resistance forms: statoblast (b1), gemmule (b2), cocoon (b3), cells against dehydration (b4), and diapause or dormancy (b5); (3) voltinism: semivoltine (c1), univoltine (c2), and multivoltine (c3). (B) Reproductive: ovoviviparous (d1), isolated free eggs (d2), isolated eggs, segmented (d3), segmented nested eggs (d4), free-nested eggs (d5), vegetation-nested eggs (d6), terrestrial nested eggs (d7), endophytic eggs (d8), and asexual reproduction (d9). (C). Behavioral and physiological: (1) breathing: cutaneous (e1), gills (e2), plastron (e3), aerial (e4), and respiratory pigments (e5); (2) locomotion: flyer (f1), surface swimmer (f2), all swimmer (f3), walker (f4), epibenthic burrower (f5), endobenthic burrower (f6), and temporarily fixed to the substrate (f7); (3) feeding: collector (g1), filter (g2), shedder (g3), scraper (g4), piercer (g5), and predator (g6); (4) food: sediment particles (h1), fine debris (h2), coarse debris (h3), microphytes (h4), macrophytes (h5), microinvertebrates (h6), macroinvertebrates (h7), vertebrates (h8), and dead animals (h9); (5) habitat preference: sediment (i1), leaf litter (i2), macrophytes (i3), rocks (i4), branches (i5), and water surface (i6). (D) Morphological: (1) body armor: sclerotized body (j1), strong case/shell (j2), and without adaptation (j3); (2) maximum size: <2.5 mm (k1), 2.5–5 mm (k2), 5–10 mm (k3), 11–20 mm (k4), 21–40 mm (k5), and 41–80 mm (k6); (3) body shape: streamlined (l1), flattened (l2), cylindrical (l3), and spherical (l4).
Figure 5.
Canonical correspondence analysis (CCA) between functional traits, environmental variables, and temporary ponds. TDS: Total dissolved solids; PO4–P: Orthophosphates; O2: Dissolved oxygen; NO2: Nitrites. P: Pond, A: Filling phase; R: Drying phase. A. Lifecycle: (1) aquatic stage: egg (a1), larvae and/or pupa (a2), and adult (a3); (2) resistance forms: statoblast (b1), gemmule (b2), cocoon (b3), cells against dehydration (b4), and diapause or dormancy (b5); (3) voltinism: semivoltine (c1), univoltine (c2), and multivoltine (c3). B. Reproductive: ovoviviparous (d1), isolated free eggs (d2), isolated eggs, segmented (d3), segmented nested eggs (d4), free-nested eggs (d5), vegetation-nested eggs (d6), terrestrial nested eggs (d7), endophytic eggs (d8), and asexual reproduction (d9). C. Behavioral and physiological: (1) breathing: cutaneous (e1), gills (e2), plastron (e3), aerial (e4), and respiratory pigments (e5); (2) locomotion: flyer (f1), surface swimmer (f2), all swimmer (f3), walker (f4), epibenthic burrower (f5), endobenthic burrower (f6), and temporarily fixed to the substrate (f7); (3) feeding: collector (g1), filter (g2), shedder (g3), scraper (g4), piercer (g5), and predator (g6); (4) food: sediment particles (h1), fine debris (h2), coarse debris (h3), microphytes (h4), macrophytes (h5), microinvertebrates (h6), macroinvertebrates (h7), vertebrates (h8), and dead animals (h9); (5) habitat preference: sediment (i1), leaf litter (i2), macrophytes (i3), rocks (i4), branches (i5), and water surface (i6). D. Morphological: (1) body armor: sclerotized body (j1), strong case/shell (j2), and without adaptation (j3); (2) maximum size: <2.5 mm (k1), 2.5–5 mm (k2), 5–10 mm (k3), 11–20 mm (k4), 21–40 mm (k5), and 41–80 mm (k6); (3) body shape: streamlined (l1), flattened (l2), cylindrical (l3), and spherical (l4).
Figure 5.
Canonical correspondence analysis (CCA) between functional traits, environmental variables, and temporary ponds. TDS: Total dissolved solids; PO4–P: Orthophosphates; O2: Dissolved oxygen; NO2: Nitrites. P: Pond, A: Filling phase; R: Drying phase. A. Lifecycle: (1) aquatic stage: egg (a1), larvae and/or pupa (a2), and adult (a3); (2) resistance forms: statoblast (b1), gemmule (b2), cocoon (b3), cells against dehydration (b4), and diapause or dormancy (b5); (3) voltinism: semivoltine (c1), univoltine (c2), and multivoltine (c3). B. Reproductive: ovoviviparous (d1), isolated free eggs (d2), isolated eggs, segmented (d3), segmented nested eggs (d4), free-nested eggs (d5), vegetation-nested eggs (d6), terrestrial nested eggs (d7), endophytic eggs (d8), and asexual reproduction (d9). C. Behavioral and physiological: (1) breathing: cutaneous (e1), gills (e2), plastron (e3), aerial (e4), and respiratory pigments (e5); (2) locomotion: flyer (f1), surface swimmer (f2), all swimmer (f3), walker (f4), epibenthic burrower (f5), endobenthic burrower (f6), and temporarily fixed to the substrate (f7); (3) feeding: collector (g1), filter (g2), shedder (g3), scraper (g4), piercer (g5), and predator (g6); (4) food: sediment particles (h1), fine debris (h2), coarse debris (h3), microphytes (h4), macrophytes (h5), microinvertebrates (h6), macroinvertebrates (h7), vertebrates (h8), and dead animals (h9); (5) habitat preference: sediment (i1), leaf litter (i2), macrophytes (i3), rocks (i4), branches (i5), and water surface (i6). D. Morphological: (1) body armor: sclerotized body (j1), strong case/shell (j2), and without adaptation (j3); (2) maximum size: <2.5 mm (k1), 2.5–5 mm (k2), 5–10 mm (k3), 11–20 mm (k4), 21–40 mm (k5), and 41–80 mm (k6); (3) body shape: streamlined (l1), flattened (l2), cylindrical (l3), and spherical (l4).
Table 1.
Environmental variables in the temporary ponds. TDS: total dissolved solids; PO4-P: orthophosphates; O2: dissolved oxygen; NO2: nitrites. P: Pond, A: filling phase; R: drying phase. Ol: oligotrophic; Me: mesotrophic; Hi: hypertrophic; Eu: eutrophic.
Table 1.
Environmental variables in the temporary ponds. TDS: total dissolved solids; PO4-P: orthophosphates; O2: dissolved oxygen; NO2: nitrites. P: Pond, A: filling phase; R: drying phase. Ol: oligotrophic; Me: mesotrophic; Hi: hypertrophic; Eu: eutrophic.
| Ponds | Period | Trophic 1 | pH | Temperature | O2 | TDS | PO4-P | NO2 |
|---|---|---|---|---|---|---|---|---|
| P1 | A | Ol | 5.81 | 33.60 | 2.50 | 342 | 0 | 4.40 |
| R | Me | 6.03 | 27.72 | 0.50 | 1104 | 0.07 | 3.10 | |
| P2 | A | Me | 6.40 | 30.70 | 0.87 | 43 | 0.03 | 0 |
| R | Me | 6.34 | 29.08 | 1.90 | 72 | 0.03 | 1.60 | |
| P3 | A | Hi | 6.30 | 28.80 | 0.60 | 44 | 0.35 | 0.50 |
| R | Me | 6.93 | 31.76 | 2.80 | 105 | 0.01 | 0.80 | |
| P4 | A | Me | 6.65 | 28.70 | 1.64 | 42 | 0.03 | 0 |
| R | Me | 6.41 | 27.05 | 1.20 | 55 | 0.02 | 1.30 | |
| P5 | A | Eu | 6.61 | 27.12 | 0.72 | 104 | 0.15 | 1.80 |
| R | Eu | 7.15 | 28.36 | 1.76 | 193 | 0.13 | 2.30 |
Note: 1 Categories were assigned based on PO4-P values, following Moreno-Franco et al. [26].
Table 2.
Sample coverage from aquatic macroinvertebrate in the temporary ponds. SC = sample coverage; SC.LCL, SC.UCL = lower and upper confidence limits for the expected sample coverage.
Table 2.
Sample coverage from aquatic macroinvertebrate in the temporary ponds. SC = sample coverage; SC.LCL, SC.UCL = lower and upper confidence limits for the expected sample coverage.
| Ponds | Filling Phase | Drying Phase | ||||
|---|---|---|---|---|---|---|
| SC | SC.LCL | SC.UCL | SC | SC.LCL | SC.UCL | |
| 1 | 0.98 | 0.97 | 0.99 | 0.97 | 0.95 | 0.99 |
| 2 | 0.96 | 0.94 | 0.99 | 0.99 | 0.98 | 0.99 |
| 3 | 0.99 | 0.97 | 0.99 | 0.99 | 0.99 | 1.00 |
| 4 | 0.97 | 0.95 | 0.99 | 0.99 | 0.99 | 1.00 |
| 5 | 0.97 | 0.95 | 0.99 | 0.98 | 0.97 | 0.99 |
Table 3.
Functional distance index (FDist) of temporary ponds.
| Pond | Markov Chain Monte Carlo | ||
|---|---|---|---|
| Mean | Lower Limit | Upper Limit | |
| 1 | −0.017 | −0.050 | 0.012 |
| 2 | −0.018 | −0.042 | 0.005 |
| 3 | −0.015 | −0.043 | 0.019 |
| 4 | −0.023 | −0.036 | −0.004 |
| 5 | −0.057 | −0.103 | 0.003 |
| All | −0.007 | −0.010 | −0.003 |
Table 4.
Functional richness index (FRIc) of temporary ponds. t = T Statistic; df = degrees of freedom.
Table 4.
Functional richness index (FRIc) of temporary ponds. t = T Statistic; df = degrees of freedom.
| Pond | FRic | Welch t-Test | |||
|---|---|---|---|---|---|
| Filling Phase | Drying Phase | t | df | p-Value | |
| 1 | 12.4 | 16.0 | −0.74 | 1.34 | 0.57 |
| 2 | 9.60 | 20.0 | −1.80 | 2.26 | 0.20 |
| 3 | 9.00 | 16.5 | −1.35 | 2.38 | 0.29 |
| 4 | 15.90 | 13.0 | −0.55 | 2.70 | 0.66 |
| 5 | 9.00 | 13.2 | −1.62 | 2.97 | 0.21 |
| All | 0.001 | 0.001 | −1.99 | 23.56 | 0.06 |
Table 5.
Functional dispersion index (FDisp) of temporary ponds. t = T Statistic; df = degrees of freedom.
Table 5.
Functional dispersion index (FDisp) of temporary ponds. t = T Statistic; df = degrees of freedom.
| Pond | FDisp | Welch t-Test | |||
|---|---|---|---|---|---|
| Filling Phase | Drying Phase | t | df | p-Value | |
| 1 | 0.16 | 0.15 | 2.50 | 2.99 | 0.09 |
| 2 | 0.16 | 0.16 | −0.52 | 2.22 | 0.65 |
| 3 | 0.15 | 0.16 | −0.40 | 3.52 | 0.71 |
| 4 | 0.16 | 0.16 | 0.03 | 3.93 | 0.98 |
| 5 | 0.15 | 0.13 | 1.66 | 3.36 | 0.19 |
| All | 0.16 | 0.15 | 1.30 | 23.04 | 0.21 |
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MDPI and ACS Style
Tette-Pomárico, A.J.; Tamaris-Turizo, C.E.; Motta Diaz, Á.J.; Eslava-Eljaiek, P. Functional Response of Aquatic Macroinvertebrate Communities to Temporality in Tropical Temporary Ponds. Water 2023, 15, 2753. https://doi.org/10.3390/w15152753
AMA Style
Tette-Pomárico AJ, Tamaris-Turizo CE, Motta Diaz ÁJ, Eslava-Eljaiek P. Functional Response of Aquatic Macroinvertebrate Communities to Temporality in Tropical Temporary Ponds. Water. 2023; 15(15):2753. https://doi.org/10.3390/w15152753
Chicago/Turabian StyleTette-Pomárico, Aliano J., Cesar E. Tamaris-Turizo, Ángela J. Motta Diaz, and Pedro Eslava-Eljaiek. 2023. "Functional Response of Aquatic Macroinvertebrate Communities to Temporality in Tropical Temporary Ponds" Water 15, no. 15: 2753. https://doi.org/10.3390/w15152753
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