Biodiversity Data Journal :
Research Article
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Corresponding author: Leticia Bao (baoleticia@gmail.com)
Academic editor: Ben Price
Received: 13 Nov 2020 | Accepted: 18 Feb 2021 | Published: 04 Mar 2021
© 2021 Leticia Bao, Sebastián Martínez, Mónica Cadenazzi, Mónica Urrutia, Lucía Seijas, Enrique Castiglioni
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Bao L, Martínez S, Cadenazzi M, Urrutia M, Seijas L, Castiglioni E (2021) Aquatic macroinvertebrates in Uruguayan rice agroecosystem. Biodiversity Data Journal 9: e60745. https://doi.org/10.3897/BDJ.9.e60745
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This work is a first approach to the knowledge of insects and other aquatic macroinvertebrates of rice agroecosystems from eastern Uruguay. The composition of the groups collected may represent an approximation to the knowledge of the quality of water sources associated with Uruguayan rice production. Sampling of aquatic macroinvertebrates was carried out during the grain-filling stage in crops without insecticide use, in three localities of Treinta y Tres Department. In each crop, macroinvertebrates were collected with a Surber-type network at the inlet and outlet of water to and from the paddy field and a neighbouring control area. Differences in morphospecies composition were found according to the location and source of water. Insecta was the most represented class in macroinvertebrate samplings (41.5%). Diptera (59.9%), Hemiptera (16.3%) and Ephemeroptera (14.0%) were the most abundant orders within insects. The Richness and Shannon Diversity Indices were higher than those recorded for similar studies in Costa Rica, Italy and Australia.
biodiversity, bio-indicators, water quality
According to the international Ramsar convention, rice fields are considered as artificial wetlands. Around 100 Ramsar sites in the world include rice areas and perform important ecological functions which sustain remarkable biodiversity (
Natural water sources harbour more than 6% of all insect species in the world and a number of those can colonise artificial water ponds formed for rice cultivation or paddy fields (
With the reduction in natural wetlands, the occurrence of rice agroecosystems over wide areas of eastern Uruguay could substitute for different groups of animals for the loss of habitat, particularly for aquatic organisms. Therefore, in this context, rice paddies can be evaluated as habitats that can act as a viable refuge for organisms that inhabit surrounding natural habitats (
The rice crop in Uruguay is produced under irrigation, so the semi-aquatic temporary environment resulting from tilling to pre-harvest could be favourable for insects or other groups that have one or more of their life stages in aquatic environments. Changes in the abundance of aquatic organisms, including insects, have been observed in relation to different rice growth phenological stages (
As different groups have different degrees of water pollution tolerance, the composition of macroinvertebrate communities would change amongst water sources and could generate important information about water quality (
Research related to aquatic macroinvertebrates in Uruguay refers to natural environments (
This work represents the first approach to the study of aquatic organisms in rice crops and for the evaluation of the role of Uruguayan rice agroecosystems in biodiversity conservation of aquatic organisms. The information generated could help to define groups relevant for the ecosystemic services they bring and propose management measures that contribute to their conservation. In addition, group composition in different samples could represent an approximation to water quality knowledge of water sources associated with rice crop production.
Sampling was undertaken in February 2015 in three rice crops from Treinta y Tres Department in north-eastern Uruguay (Fig.
In each crop at each water source (E, O, C), three points were selected and water physicochemical properties were registered: dissolved oxygen (DO), temperature and conductivity (completely randomised design). After this, from each point, macroinvertebrates were collected with a Surber net (30 x 30 cm section) for a 1-minute period. Collected material was placed in vials containing 90% alcohol. Collected individuals were counted and organised by taxa with the aid of taxonomic keys, while insect specimens were sorted to morphospecies, the remaining macroinvertebrates were sorted to family (
Mean values of physicochemical properties for each water source and within each site were calculated and compared by the Tukey Test (p < 0.05). Functional groups and physicochemical properties were analysed by the Mantel Test to study the correlation between water properties and the composition of functional groups (
Using the insect data counting matrix, richness estimators (Chao 1 and Chao 2, Jackknife 1 and Jackknife 2, Bootstrap and ACE) were calculated and a species accumulation curve was performed with EstimateS 9.1.0 software (
A heatmap was constructed with the heatmap function using realtive abundances of each taxonomic group (
Abundance, Richness and Diversity Indices (Simpson, Shannon, Evenness, Margalef, Equitability and Berger-Parker) were calculated for each sample corresponding to each water source and locality (PAST Software,
Water physicochemical properties varied within each site and also between each water source (Table
Physicochemical properties of water at different localities and in different water sources (entrance: E, outlet: O and Control zone: C) in rice agroecosystem in Treinta y Tres, Uruguay.
Locality (site) |
Water source |
Temperature (°C) |
DO (O2 mg/l) |
Conductivity (µS) |
La Charqueada ( |
Entrance |
26.57 ±0.64a |
4.20±0.89abc |
163.67±10.02ab |
Outlet |
26.47±0.64a |
6.27±0.89c |
139.30±10.02a |
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Control |
30.10±0.64b |
6.16±0.89c |
180.50±12.27b |
|
El Tigre ( |
Entrance |
27.53±0.57a |
9.71±0.89b |
89.73±3.79a |
Outlet |
29.63±0.57b |
9.63±0.89b |
94.73±3.79a |
|
Control |
28.23±0.57ab |
1.95±0.89a |
102.63±3.79a |
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Julio M. Sanz ( |
Entrance |
26.50±0.11a |
2.67±0.89ab |
59.93±2.03a |
Outlet |
27.40±0.11b |
5.06±0.89bc |
60.95±2.03a |
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Control |
27.30±0.11b |
2.21±0.89a |
58.00±2.48a |
A total of 2820 macroinvertebrates in 27 samples were collected from the three localities. Insects represented 41.5% of total macroinvertebrates collected and Maxillopoda (Crustacea), Branchiopoda (Crustacea) and Arachnida were the most abundant macroinvertebrates classes collected after insects (Table
Relative abundance of macroinvertebrates (no insects) collected with a Surber net in the rice agroecosystem, in Treinta y Tres, Uruguay.
Class |
Order |
Family |
Genus/morpho species |
Relative abundance (%) |
Maxillopoda |
Cyclopoida |
Cyclopidae |
Cyclopidae morphospecies 1 |
22.50 |
Branchiopoda |
Anomopoda |
Daphniidae |
Daphnia morphospecies 1 |
18.14 |
Arachnida |
Trombidiformes (subclass Acarina) |
Hydrachnidae Hydrozetidae^ undetermined |
Hydrachna morphospecies 1 Hydrozetidae morphospecies 1 Acarina morphospecies 1 |
8.00 |
Gastropoda (snails) |
Caenogastropoda |
Ampullariidae |
Pomacea and other spp. |
4.88 |
Oligochaeta |
Tubificida |
undetermined |
Tubificida morphospecies 1 |
1.80 |
Malacostraca |
Amphipoda |
Hyalellidae |
Hyalella morphospecies 1^ |
1.39 |
Arachnida |
Araneae |
Allocosinae, Lyniphiidae, Anyphaenidae |
juveniles |
0.33 |
Clitellata |
Hirudinea |
undetermined |
unidentified leech |
0.29 |
^ indicates uncertain identification at Genus level.
From the total macroinvertebrates collected, 1170 were insects, belonging to 10 orders, 39 families and 50 species/morphospecies (Table
Insects collected with a Surber net in the rice agroecosystem at the entrance, outlet and control zones of water in Treinta y Tres. Uruguay.
Order |
Family |
Genus/Species/morphospecies |
Ephemeroptera |
Baetidae |
Americabaetis morphospecies 1^ |
Caenidae |
Caenis morphospecies 1 |
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Odonata |
Libellulidae |
Libellulidae morphospecies 1 |
Coenagrionidae |
Acanthagrion morphospecies 1 ^ |
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Trichoptera |
Hydroptylidae |
Oxyethira morphospecies 1 |
Hemiptera |
Belostomatidae |
Belostoma morphospecies 1 |
Corixidae |
Sigara chrostowskii |
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Corixidae morphospecies 1 |
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Notonectidae |
Notonectidae morphospecies 1 |
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Nepidae |
Ranatra morphospecies 1 |
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Aphididae |
Rhopalosiphum padi* |
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Cicadellidae |
Cicadellidae morphospecies 1 (nymph)* |
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Pentatomidae |
Pentatomidae morphospecies 1 (nymph)* |
|
Lygaeidae |
Nysius simulans* |
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Cercopidae |
Cercopidae morphospecies 1 (nymph)* |
|
Hymenoptera |
Formicidae |
Solenopsis morphospecies 1* |
Coleoptera |
Hydrophylidae |
Berosus morphospecies 1 |
Tropisternus morphospecies 1 |
||
Dytiscidae |
Enochrus morphospecies 1 |
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Laccophillus morphospecies 1 |
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Rhantus morphospecies 1 |
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Desmopachria morphospecies 1^ |
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Curculionidae |
Oryzophagus oryzae |
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Hypselus ater |
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Scarabaeidae |
Ataenius morphospecies 1 |
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Aphodius morphospecies 1 |
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Haliplidae |
Haliplus morphospecies 1 |
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Carabidae |
Meotachys morphospecies 1^* |
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Elmidae |
Elmidae morphospecies 1 |
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Ptinidae |
Scydmaenus morphospecies 1 * |
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Chrysomelidae |
Epitrix morphospecies 1* |
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Mycetophagidae |
Mycetophagidae morphospecies 1* |
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Staphylinidae |
Staphylinidae morphospecies 1* |
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Noteridae |
Suphisellus morphospecies 1 |
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Diptera |
Chironomidae |
Chironomidae morphospecies 1 |
Chironomidae morphospecies 2 |
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Chironomidae morphospecies 3 |
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Chironomidae morphospecies 4 |
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Chironomidae morphospecies 5 |
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Syrphidae |
Eristalinae morphospecies 1 |
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Ceratopogonidae |
Bezzia morphospecies 1 |
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Culicidae |
Anopheles morphospecies 1 |
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Simuliidae |
Simuliidae morphospecies 1 |
|
Empididae |
Empididae morphospecies 1 |
|
Lepidoptera |
Piralidae |
Parapoynx morphospecies 1 |
Hesperidae |
Hylephila morphospecies 1 |
|
Orthoptera |
Tettigoniidae |
Conocephalus morphospecies 1* |
Acridoidea |
subfamily Acridinae morphospecies 1* |
|
Thysanoptera |
Thripidae |
Thripidae morphospecies 1* |
Psocoptera |
Psocoptera morphospecies 1* |
* terrestrial groups not included in analysis.
^ indicates uncertain identification at this level.
The Cumulative Species Curve for insects shows that there are still species pending collection. Richness estimators show that at least 58.8% of expected species were sampled (Jackknife 2: 58.8%, Chao 1: 59.8%, Chao 2: 60.4%, ACE: 62.1%, Jackknife 1: 66.4%, Bootstrap: 74.4%, corresponding to an estimated number of species of 49, 48, 48, 47, 44 and 39, respectively) (Fig.
The physicochemical properties of water were correlated with functional groups according to the Mantel Test through Euclidean distances (r = 0.48 p = 0.019), but due to the number of samples, it was not possible to correlate each property to a particular functional group.
The Kruskal-Wallis Test for total arthropods number showed the higher values from the water outlet and control zone, with a lower count for the water entrance (H = 18.47, p = 0.0178). Following the same analysis and comparing at family level, there were also differences found between water sources for Syrphidae larvae, with higher abundances in the water outlet (H = 20.34, p = 0.006) (Table
Abundance of Syrphidae larvae and total number of arthropods according to water source (Entrance, Outlet and Control) in the rice agroecosystem in Treinta y Tres. Uruguay.
Water source |
Syrphidae larvae |
Total number of arthropods |
Entrance |
0.67 ± 1.32a |
40.78 ± 6.87a |
Outlet |
15.56 ± 11.54b |
89.11 ± 16.61b |
Control |
1.22 ± 1.30a |
145.78 ± 18.56c |
The same letter within each column means no significant differences LSD Fisher Test (p ˃ 0.05).
Taxa distributions by site and water source are shown as a heat map (Fig.
Heat map of taxon relative abundance and hierarchical clustering of samples. References:
Sites: CH: La Charqueada, JMS: Julio María Sanz, ET: El Tigre;
Water source: E: entrance, O: outlet, C: control;
Taxonomic group: Co: copepods, Da: Daphnia, Ch: Chironomidae, Ep: Ephemeroptera, Oa:
Other aquatics, Am: Amphipoda, Hy: Hydrophilidae, Sy: Syrphidae, Mi: Mites, Ga: Gastropoda, Cx: Corixidae.
Values are scaled by taxon relative abundances across each site and water source.
The ANOSIM Test showed differences according to locality and water source (R = 0.388, p = 0.0013 and R = 0.615, p = 0.0001, respectively). According to the SIMPER Test through Bray-Curtis distances, 80% of the differences between localities was explained by seven species, while differences between water sources were explained by six species (Table
SIMPER Test with species accomplishing 80% dissimilarity between localities and between water circulation in the rice agroecosystem in Treinta y Tres, Uruguay.
SIMPER Test by LOCALITY |
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Taxon |
Dissimilarity |
% Contribution |
% Cumulative |
Mean by site |
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La Charqueada |
JM Sanz |
El Tigre |
||||
Chironomidae morphospecies 2 |
22.83 |
27.94 |
27.94 |
13.60 |
15.20 |
7.67 |
Sigara chrostowskii |
13.64 |
16.70 |
44.64 |
14.80 |
0.00 |
3.67 |
Eristalinae morphospecies 1 |
8.08 |
9.88 |
54.52 |
7.89 |
2.11 |
1.89 |
Caenis morphospecies 1 |
6.47 |
7.92 |
62.44 |
5.33 |
0.11 |
2.22 |
Americabaetis morphospecies 1 ^ |
6.12 |
7.50 |
69.93 |
3.11 |
1.11 |
4.33 |
Chironomidae morphospecies 3 |
6.07 |
7.43 |
77.36 |
1.89 |
3.11 |
1.00 |
Oryzophagus oryzae |
2.02 |
2.47 |
79.83 |
0.56 |
0.22 |
0.67 |
SIMPER Test by WATER SOURCE |
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Taxon |
Dissimilarity |
% Contribution |
% Cumulative |
Mean by water source |
||
Entrance |
Outlet |
Control |
||||
Chironomidae morphospecies 2 |
26.06 |
31.02 |
31.02 |
5.11 |
25.10 |
6.22 |
Sigara chrostowskii |
13.30 |
15.83 |
46.85 |
2.56 |
0.11 |
15.80 |
Eristalinae morphospecies 1 |
8.34 |
9.93 |
56.79 |
1.78 |
9.11 |
1.00 |
Caenis morphospecies 1 |
6.76 |
8.05 |
64.84 |
7.56 |
0.11 |
0.00 |
Americabaetis morphospecies 1^ |
6.40 |
7.62 |
72.46 |
4.11 |
4.11 |
0.33 |
Chironomidae morphospecies 3 |
6.26 |
7.45 |
79.91 |
3.33 |
2.33 |
0.33 |
^ indicates uncertain identification at Genus level.
The Principal Component Analysis (PCA) shows samples grouping according to the water source (Fig.
Richness and Diversity Indices are shown in Table
Richness and Diversity Indices for insects ± E.E, by locality (site) in water samples.
Diversity |
El Tigre |
J.M. Sanz |
La Charqueada |
Entrance |
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Richness (S) |
6.33 ± 1.53aA |
9.00 ± 1.73aB |
7.67 ± 1.53aA |
Shannon H |
1.55 ± 0.12aA |
1.54 ± 0.12aA |
1.64 ± 0.12aA |
Simpson 1-D |
0.76 ± 0.03aA |
0.74 ± 0.03aB |
0.76 ± 0.03aA |
Equitability J |
0.81 ± 0.03abA |
0.85 ± 0.03bB |
0.700 ± 0.03aA |
Outlet |
|||
Richness (S) |
13.33 ± 0.58bB |
4.67 ± 1.15aA |
5.33 ± 1.53aA |
Shannon H |
2.02 ± 0.07bB |
1.14 ± 0.07aA |
1.14 ± 0.07aA |
Simpson 1-D |
0.62 ± 0.04aA |
0.81 ± 0.04bB |
0.61 ± 0.04aA |
Equitability J |
0.70 ± 0.07aA |
0.78 ± 0.07aB |
0.77 ± 0.07aA |
Control |
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Richness (S) |
11.00 ± 2.65aB |
7.00 ± 1.73aAB |
7.33 ± 2.31aA |
Shannon H |
1.40 ± 0.15aA |
1.19 ± 0.15aA |
1.05 ± 0.15aA |
Simpson 1-D |
0.48 ± 0.08aA |
0.62 ± 0.08aA |
0.58 ± 0.08aA |
Equitability J |
0.56 ± 0.09aA |
0.59 ± 0.09aA |
0.62 ± 0.09aA |
The same capital letter within each column and same lower-case letter within each row means no significant differences in LSD Fisher Test (p ˃ 0.05).
Comparing values within each field according to water source, the major differences were registered for El Tigre. In J.M. Sanz, differences were registered only for richness with the higher value at the water entrance. On the other hand, for Charqueada, no differences were registered between water sources.
This study represents the first description of the aquatic macroinvertebrate community associated with rice crops in Uruguay and establishes a baseline for present and future studies on productivity and ecological sustainability of Uruguayan rice farms.
In relation to water physicochemical properties, the greatest differences were registered for dissolved oxygen with lower values in control zones from El Tigre and J.M. Sanz. Control zones are water bodies located in crop surroundings and with less area and without water flux compared with rice areas. In the case of La Charqueada, the control zone belongs to a more extensive water body. Less oxygen content in El Tigre and J. M. Sanz could be due to water body characteristics of these localities compared to La Charqueada control zone, such as the size and sun radiation or vegetable coverage, for example (
The Mantel Test demonstrated an effect of physicochemical properties on the guild composition in different water sources. Richness estimators show that there are still many species remaining to be collected and this work recorded at least 58% of the species, depending on the estimator considered. However, even under these conditions, from the 50 morphospecies collected, 36 were aquatic insects, showing a greater diversity than reported previously in tropical-subtropical rice fields of Brazil (34 morphospecies,
Insecta was the most represented Class in the samples, with Diptera, Hemiptera and Ephemeroptera as the most represented Orders. The most abundant aquatic insects found in the present work were Chironomidae (Diptera), the most ubiquitous family of aquatic flies with a worldwide distribution (
The ANOSIM Test proved that there were differences in morphospecies composition according to locality and water source (R = 0.388, p = 0.0013 and R = 0.615, p = 0.0001, respectively). Some groups showed association with a particular water source, so they could be analysed for their potential as water quality indicators for each source studied (Entrance, Outlet and Control zone). Caenis (Ephemeroptera) individuals are associated with the water entrance. It is well documented that Caenis individuals are sensitive to pollution (
Coleoptera was the most diverse order (18 morphospecies) and Dytiscidae was the most diverse family (four morphospecies). These results are in accordance with data reported by
The Shannon-Weaver Indices, calculated for locality and water source with aquatic insects species, did not show differences between water sources. However, richness values registered for aquatic insect species are higher than those registered in organic rice crops in Australia (
The higher richness and diversity registered in El Tigre could be due to different factors. From the point of view of the landscape where this crop is located, probably there is a better connectivity with native vegetation patches than in the other two sites (J.M. Sanz and La Charqueada), but this has to be confirmed. It is possible that this environment, with the largest area of native riverine vegetation of the three sampled sites, could be a better reservoir for species, supporting a higher diversity and richness (
Moreover, it should be emphasised that sampling was undertaken at the grain-filling stage, so there is no information about possible diversity fluctuation along the crop cycle, as reported previously (
The progress in aquatic macroinvertebrate community characterisation and agrochemical residues evaluations could enable the definition of indicators as relatively quick sampling tools for water quality screening, thus enabling the measurement of the impact of crop management activities.
The physicochemical properties of water had an effect on the composition of the guilds. Different morphospecies compositions were found according to locality and water source. Caenis individuals were associated with the water entrance, while Syrphidae and Chironomidae (morphospecies 2) larvae were associated with the water outlet. Some of these species could be useful indicators of water quality. Arthropods were more abundant in the water of control zones. More exhaustive sampling could register more diversity and potential bio-indicators. Richness and diversity indices registered in this work - even with an inventory of species pending registration - are higher than those reported for rice agroecosystems from Costa Rica, Italy and Australia.
Fellowship ANII POSNAC_2012_4459 to L. Bao. We thank María Caraballo for her collaboration in field sampling, to Héctor Da Fonseca and Raúl Servetto for the possibility of sampling in their fields and Marcelo Segovia for his assistance in crop selection and providing field management information.
Leticia Bao conceptualised the study; Leticia Bao, Mónica Urrutia and Lucía Seijas contributed to the methodology, Leticia Bao, Mónica Cadenazzi, Enrique Castiglioni and Sebastián Martínez carried out formal analysis and investigation; Leticia Bao, Enrique Castiglioni and Sebastián Martínez worked in writing, reviewing and editing. Leticia Bao supervised the study.
There are no financial support or relationships that may pose any conflict of interest.