Benthic macroinvertebrates and degradation of phytomass as

indicators of ecosystem functions in flooded rice cropping

Lilian Terezinha Winckler(1), Angélica Konradt Güths(2) and Pâmela Rodrigues Gayer(3)
(1)
Embrapa Clima Temperado, Rodovia BR-392, Km 78, 9o Distrito, Monte Bonito, CEP 96010-971 Pelotas, RS, Brazil. E-mail:
lilian.winckler@embrapa.br (2)Universidade Federal de Pelotas, Rua Gomes Carneiro, no 01, Campus Porto, CEP 96010-610 Pelotas,
RS, Brazil. E-mail: angelica-kg1@hotmail.com (3)Instituto Federal Sul-rio-grandense, Praça Vinte de Setembro, no 455, Campus Pelotas,
CEP 96015-360 Pelotas, RS, Brazil. E-mail: pamrgayer@hotmail.com

Abstract – The objective of this work was to evaluate the ecosystem functions of a natural wetland and of artificially
flooded rice areas, managed under organic and conventional systems, by phytomass degradation and by the
colonization of this material by benthic macroinvertebrates. The experiment was carried out in a natural wetland
area, and in two flooded rice areas managed under organic and conventional systems. Twenty-five decomposition
bags filled with 10 g of dry vegetation were installed in each site. At 14, 28, 42, 56, and 70 days after the beginning
of the experiment, five bags from each site were collected. Macroinvertebrates were identified and classified
by functional trophic group. The number of species of benthic macroinvertebrates increased: natural wetland >
organic system > conventional system. The Chironomidae group was present in all areas, confirming its food
plasticity and adaptability to different substrates and environmental stress situations. The Amphipoda group was
present only in the artificially flooded rice area, and the Acari, only in the natural wetland. The diversity of species
in the natural wetland area was higher than in the artificially flooded rice area. Nutrient cycling, provided by
phytomass decomposition, is affected by the management system, and the delay in this process causes a reduction
of the ecosystem functions in the conventional system.
Index terms: Oryza sativa, Aqualf, biomass degradation, ecosystem services, nutrient cycling, paddy soils.

Macroinvertebrados bentônicos e degradação da fitomassa como

indicadores de funções ecossistêmicas em arroz irrigado por inundação
Resumo – O objetivo deste trabalho foi avaliar as funções ecossistêmicas de um banhado natural e de lavouras
de arroz irrigado por inundação, manejadas nos sistemas convencional e orgânico, por meio da degradação
da fitomassa e da colonização desse material por macroinvertebrados bentônicos. O experimento foi
realizado em um banhado natural e em duas áreas de arroz irrigado por inundação, manejadas em sistemas
orgânico e convencional. Vinte e cinco bolsas de decomposição, cada uma preenchida com 10 g de palha
seca, foram instaladas em cada local. Aos 14, 28, 42, 56 e 70 dias após o início do experimento, cinco bolsas
de cada local foram retiradas. Os macroinvertebrados foram identificados e classificados por grupo trófico
funcional. O número de espécies de macroinvertebrados bentônicos aumentou: banhado natural > sistema
orgânico > sistema convencional. O grupo Chironomidae estava presente em todas as áreas, o que confirma
sua plasticidade alimentar e adaptabilidade a diferentes substratos e situações de estresse ambiental. O grupo
Amphipoda esteve presente somente nas lavouras de arroz artificialmente inundadas, enquanto o grupo Acari,
somente no banhado natural. A diversidade de espécies no banhado natural foi maior do que nas áreas de arroz
artificialmente inundadas. A ciclagem de nutrientes, por meio da degradação da fitomassa, é influenciada pelo
sistema de manejo, e o atraso nesse processo reduz as funções do ecossistema no sistema convencional.
Termos para indexação: Oryza sativa, Planossolos, degradação da biomassa, serviços ecossistêmicos,
ciclagem de nutrientes, solos de várzea.

Introduction degradation ensures a gradual supply of significant

amount of nutrients to crop in succession in well
managed systems (Massoni et al., 2013). In addition,
Remaining flooded rice straw and post-harvest if the area is replanted, a rapid elimination of straw is
sprouts (traditionally developed in rice regrowth, in necessary in rice cultivation, to allow of planting to be
the southern end of Rio Grande do Sul) are important carried out in a timely manner within the recommended
as fodder for livestock (Monks et al., 2002). Straw period (Massoni et al., 2013).

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Irrigated soils for rice cultivation, comprising humid from damaging the production. Chemicals cause
or waterlogged environments, have a poor drainage ecological risks to different organisms, and the use
(Monks et al., 2002) which persists after harvest. In of conjugate products, which is common in cultural
those wet environments, decomposition can be divided practices, results in additive actions between them,
into the three following phases: leaching, which releases even for less toxic ones (Nakagome et al., 2007). This
water-soluble organic and inorganic compounds that technicalization arises from conventional rice growing
are important for microbial and phytoplanktonic systems, in contrast to organic production systems of
metabolism; conditioning or catabolism, which irrigated rice, which not only are performed without
involves colonization by microorganisms, mainly the use of pesticides and synthetic fertilizers, but also
bacteria and fungi that will macerate, metabolize, are based on crop rotation (Wilson et al., 2008).
and embed leaves for secondary production, as well Species diversity and functional redundancy of
as increase of the palatability and nutritional value the microorganisms responsible for providing these
of litter; and fragmentation that can be carried out processes are ecological strategy keys to bring stability
biologically by detritivorous macroinvertebrates, other to the system and sustainability to the crop (Thrupp,
microorganisms, or physical fragmentation (Cunha- 2000). Thus, the degradation process can provide
Santino & Bianchini Jr., 2006; Gimenes et al., 2010). important information on ecosystem functionality
In wetlands, benthic macroinvertebrates are (Telöken et al., 2011), and can help in the definition of
responsible for sediment biorevolving, releasing a sustainable management.
nutrients into water, and accelerating the cycling The objective of this work was to evaluate the
process. They have an important role in the trophic ecosystem functions of a natural wetlands and of
dynamics, and constitute the link between the artificially flooded rice areas, managed under organic
grower and the consumer, by performing filtering, and conventional systems, by phytomass degradation
fragmentation, and scraping of food, processing and by the colonization of this material by benthic
and converting it into phytomass available for other macroinvertebrates.
organisms, as well as assisting in the decomposition
process (Nin et al., 2009; Oliveira & Callisto, 2010). Materials and Methods
These organisms are components of the biological
diversity of natural as well as artificial wetlands, The experiment was carried out in the municipality
which include agroecosystems of flooded rice fields. of Santa Vitória do Palmar, RS, at 10 m altitude, Brazil
They perform important ecosystem functions (Melo et (32º45'00"S; 52º38'54"W), one of the largest flooded
al., 2015), by carrying through the ecosystem services rice growing areas in the country. The climate of the
in these areas. According to Groot et al. (2002), an region is characterized by a Cfa (humid subtropical),
ecosystem function is the ability of natural process and according to the classification by Köppen-Geiger,
components to provide goods and services that satisfy with an average annual temperature of 16°C, and
human needs either directly or indirectly. Therefore, precipitation between 1,800 and 2,200 mm (Kottek et
the nutrient cycling process is linked to the provision al., 2006).
of ecosystem regulation services. Studies conducted Rice is sown between September and November in
in different regions have shown the biodiversity the region. A minimum cultivation is applied under
importance of soil organisms on the maintenance conventional systems, which involves the previous
and distribution of other ecosystem services, which desiccation of vegetation by a nonselective herbicide
requires the understanding of occurrence patterns for direct seeding. The seeding occurred in October
of these mechanisms, in different ecosystems, and 2013, and seed were treated to prevent infestation by
the types of functional microorganisms (Bardgett & Oryzophagus oryzae. Organic farming requires soil
Putten, 2014; Handa et al., 2014). preparation in the planting period, which eventually
For Silveira et al. (2012), irrigated rice production causes delays, due to the possible entry of machinery
in Rio Grande do Sul is characterized by highly in the field. In the studied site, sowing occurred in
technicalized production; therefore, pesticides are late November 2013. In the conventional system,
used to prevent invasive plants, insects, and diseases 60 kg ha-1 P2O5 and K 2O were added in the planting,

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and, for fertilization, 150 kg ha-1 N was applied in and a natural wet site (natural wetland vegetation) in
the differentiation of the flowering event. There was the surroundings of the cultures (Figure 1). Seventy-
no fertilization in the organic system, except for the five decomposition bags were introduced – 25  bags
residual fertilization used on pasture, which consisted each system –, which were fixed at stakes and equally
of 200 kg ha-1 natural phosphate. Irrigation started for distributed in five points in each system.
both systems at the three-to-four leaf stage (V3/V4), At installation and during the collections of the
and water blade was kept around 10 cm. Rice under decomposition bags, four physical and chemical water
conventional system was harvested in February 2014, parameters were monitored: pH (pHmetro Digimed
and under the organic system, in March 2014. DM2P), conductivity (conductivity meter Digimed
To evaluate the proposed systemic functions DM3P), temperature (mercury thermometer), and
(Table 1), 20x15 cm decomposition bags were made height of water blade (graduated ruler).
with a combination of mesh spacing. One side was At 14, 28, 42, 56, and 70  days, five bags were
made of 0.5 cm mesh between knots, and the other, of individually removed from each site, and were warped
0.1 cm mesh, as proposed by Carvalho & Ueida (2009). with a 0.05 mm mesh to prevent loss of plant material
The bags were filled with 10 g rice straw, collected in and organisms. In the field, the bags were stored in
the experimental station site Terras Baixas of Embrapa plastic bags, and sent to a laboratory at Embrapa Clima
Clima Temperado, and straw was oven-dried at 60°C Temperado, where they were opened and washed in
until constant weight was obtained. running water in 850 µm and 250 µm sieves.
The experiment was conducted between May  26 Retained biomass in the 850  µm sieve was stored
and August 4, 2014, in three different management in paper bags, which were labeled and oven-dried
systems: organic rice farming; conventional farming; at 60°C until constant weight was attained; then,

Table 1. Ecosystem services obtained by processes and functions from organisms in the soil-water interface, assessed
according to Groot el al. (2002).
Ecosystem functions Ecosystem process Assessment Ecosystem goods and services
1. Regulation Nutrient cycling Biomass degradation Maintenance of soil health and productive
ecosystems
2. Habitat Habitat provision Diversity of families and functional trophic Maintenance of biological diversity
groups

Figure 1. Map of the experimental sites in Santa Vitória do Palmar, state of Rio Grande do Sul, Brazil: NW, natural wetland
area; CT, conventional systems; and OF, organic systems, and the points from which five units were sampled, in each site,
are described according to the collecting day after the incubation, at 14, 28, 42, 56, and 70 days.

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they were weighed on an analytical balance. Benthic Results and Discussion

macroinvertebrates sorted from the material retained
in the sieves were identified under a stereomicroscope There was no difference (p>0.05) for water
using a suitable identification key (Mugnai et al., physicochemical parameters between the three
2010), and after this procedure, they were recorded, sampled sites. Electric conductivity showed a great
and stored in 70% alcohol. variation, and the highest values were observed in
Functional trophic groups (FTG) of the sampled the conventional farming (Table 2). Chemical inputs
used in conventional management may have affected
benthic macroinvertebrates were categorized according
this difference; the organic farming does not make use
to the classification proposed by Cummins et al. (2005)
of these inputs (Wilson et al., 2008). No correlation
and to supplementary bibliography (Mormul et al., 2006;
was observed between the physicochemical and biotic
Oliveira & Callisto, 2010; Barbola et al., 2011; Santos,
parameters (p>0.05) (Figure 2).
2014; Telöken et al., 2014; Santos & Rodrigues, 2015).
During the experimental period, 4,259 specimens
The diversity index of Shannon-Wiener was
of benthic macroinvertebrates were found, as follows:
calculated by the program Dives 3.0 (Rodrigues, 2014),
335 specimens in the conventional system, distributed
and the occurrence constancy was calculated by the
in 18 taxa (1 phylum, 1 class, 3 orders, and 13 families);
equation C = [(number of samples with species/total
630 specimens in the organic farming, distributed
number of samples) × 100]. Constant species occurred
across 14 taxa (1 phylum, 1 class, 1 subclass, 3 orders,
in 50% or more of the samples, accessory ones in the
and 8  families); and 3,294 specimens in the natural
range between 25 and 50% of samples, and incidental wetland, distributed in 27 taxa (1 phylum, 1 class,
species occurred in less than 25% of the samples. 1 subclass, 3 orders, and 21 families) (Table 3).
The model of Petersen & Cummins (1974) was Using decomposition bags in a lentic environment,
used to calculate the percentage of remaining biomass in the southern end of Rio Grande do Sul state, Telöken
(%R) and biomass decay coefficient (k), according to et al. (2011) found a greater abundance of organisms
the respective equations % R = (Wt/W0) × 100, and than that found in the present study. However, despite
k = - (1/t) × ln (Wt/W0), in which: Wt is the biomass the proximity of the sampled sites, this work was
weight at the time of observation; W0 is the initial conducted in the winter, while Telöken et al. (2011)
biomass weight, and the decay coefficients are classified performed theirs in the autumn with an average
as slow, when k<0.005 per day, or fast, when k>0.010 temperature of 23.95°C, which may have affected
per day. these differences, as well as the differences between
The correlation analysis between the physicochemical the evaluated plant species (Carvalho & Uieda, 2009;
parameters and the organisms in the studied sites Gimenes et al., 2010).
was conducted using the Mantel test, with the Multiv The abundance of benthic macroinvertebrates
program (Pillar, 2001), and the rope distance was was higher (p<0.05) in the natural wetland than in
considered as a similarity measure. The randomization the cultivated fields, which is opposite to what was
test (Pillar & Orlóci, 1996), carried out with the reported by Pires et al. (2015), who evaluated irrigated
Multiv program, was used to evaluate the differences rice farmings during the crop season, and reported
(p<0.05) of the physicochemical data of water, biomass drought problems at the time of the study. In the
degradation, abundance of benthic macroinvertebrates, present work, abundancy in the site of the organic
as well as the diversity index between the studied farming was higher (p<0.05) than in the conventional
sites. The Euclidean distance was used as a similarity one, in accordance with the results obtained by Wilson
measure for biotic parameters, and, the Gower index, et al. (2008) during the crop season.
for the abiotic parameters, without performing data The diversity index showed variation over the
transformation. The correlations between biomass decay period, and its were higher (p<0.05) at days 14, 28,
and the diversity index, biomass decay and abundance, and 56 than those observed at days 42 and 70. The
and biomass decay and the number of functional trophic management systems showed that the diversity index
groups were also evaluated for straw from organic and in the conventional cultivation was lower (p<0.05)
conventional farmings, and from the natural wetland than that observed for the natural wetland. However,
vegetation (p<0.05). the diversity index for the organic systems did not

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differ from that in the other sampled sites. The results The Amphipoda group was constant only in the
were different from those observed in rice fields conventional and organic systemss, while Acari
in Australia, where the organic cultivation showed occurred only in the natural wetland. For Nin et al.
higher diversity indices throughout the experimental (2009), colonization by amphipods starts in the first
period (Wilson et al., 2008). Keeping diversity is a hours of exposure, and it is later replaced by other
feature of more sustainable systems (Thrupp, 2000), groups, especially insects. Santos & Rodrigues
which increases redundancy of microorganisms (2015) observed that over time there is an increase
performing the same systemic functions (for example, of colonization and succession of smaller organisms,
more organisms of a single trophic group); this allows such as mites. Considering that the colonization by
of organisms to carry out the processes, and ensure shredders in the natural wetland occurred before
maintenance of the ecosystem functions, even if some the first collection, these herbivores (shredders)
of these organisms decrease, due to their sensitivity to were replaced by detritivores (collectors), and these,
some environmental factors. by carnivores (predators). From these predators,
According to Pires et al. (2015), the fauna recorded in Acari were the major representatives in the natural
the conventional system is usually rich and diversified; wetland, while Nematoda were predominant in the
however, it is characterized by a high ecological cultivated fields. Probably, this distribution is due to
dynamism, and by its composition of environmental Acari sensitivity to physical disorders (Di Sabatino
disturbance-tolerant groups, with a high capacity for et al., 2000), according to the sensitivity range of
colonization. During the sampling period, sensitive macroinvertebrate families of Costa Rica (Rizo-Patrón
organisms to environmental changes, such as V. et al., 2013). The comparison of the occurrence
Ephemeroptera (Kerans & Karr, 1994) were not found frequency (Table 4) with this scale showed that in the
in the conventional systems, which corroborates data conventional rice cultivation, accessory and constant
of Pires et al. (2015). families are the only ones classified as sensitivity 3.
The occurrence frequency (Table 4) showed that the In the conventional management, in addition to these
organisms were distributed in the fields as follows: in the families, Haliplidae with sensitivity 4 occurred. In the
conventional system, Chironomidae and Amphipoda; wetland, accessory and constant families were Acari
in the organic system, Hirudinea, Chironomidae, and Caenidae, with sensitivity 4.
Nematoda, and Amphipoda; and, in the natural Among the functional trophic groups (FTG),
wetland, Hirudinea, Acari, Chironomidae, Nematoda, removed from the bags at the day 14, the presence of
and Collembola. Chironomidae were present in all shredders was observed in the conventional system,
studied areas. Colonization in decomposition bags and predators were prevalent, followed by collectors
by this family has been observed by various authors, (Figure 2). During this period, the number of shredders
underscoring its dominance both in lotic and lentic in the conventional system increased, and FTG were
environments (Moulton & Magalhães, 2003; Mormul dominant in this management system, in comparison to
et al., 2006). This situation probably occurs because the others. FTG succession was apparently faster in the
Chironomidae show great food plasticity, and high organic farming and in the natural wetland than in the
adaptive power to different substrates, and to different conventional system. In the natural wetland, detritivores
situations of environmental stress. This group is appeared in a greater proportion at the day 14; and,
important for the leaf degradation processes in the litter in the organic management, they appeared at the day
with low nutritional value, and absence of shredders 28, gradually increasing after this period. For Telöken
(Moretti et al., 2007). et al. (2011), despite the high correlation of shredders

Table 2. Mean values and standard deviation of physical and chemical parameters by the time of sample collection(1).
Site Condutivity (µS cm-1) Temperature (°C) Water blade (cm)
Organic system 105.04a (39.56) 13.4a (1.35) 28.4a (10.46)
Conventional system 515.78a (292.35) 12.8a (1.85) 14.8a (4.05)
Natural wetland 142.36a (37.90) 14.10a (1.70) 14.1a (9.41)
Values followed by equal letters, in the lines, show no significant difference, at 5% probability. The standard deviation is described in parentheses.
(1)

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266 L.T. Winckler et al.

with foliar degradation rate in temperate regions, the

contributions of this FTG for the litter decomposition
in subtropical areas have been smaller than in areas of
higher latitudes. This was also observed in the present
study; however, the first evaluation occurred only at
the day 14. Shredders might have occurred in the first
two weeks, mainly in the organic cultivation and in
the natural wetland; however, in the late collection
period, they were not detected. After this period,
shredders were replaced by carnivores and omnivores
in the natural wetland and in the organic cultivation,
while detritivores reached a higher proportion between
FTG in the conventional system only at the day 70.
The great presence of predators and parasites occurs
probably by the availability of potential prey (Mormul
et al., 2006). The number of functional trophic groups
showed no significant correlation with decay of foliar
biomass, which is probably due to this dynamic in
colonization.
The different management systems were equivalent
as for biomass loss; however, there was interaction
between time and management systems. There was
difference between the conventional and the other
management system at 14 and 28 days after incubation
(p<0.05) (Figure 3). According to the decay coefficient,
proposed by Petersen & Cummins (1974), the results in
all periods and management systems were greater than
0.010 per day, which expresses a quick biomass decay.
In the present study, there was a fast biomass decay,
which was more expressive at the day 40, mainly in the
natural wetland that showed a greater richness during
this period, indicating that the action of these organisms
was effective for biomass decomposition. There was no
correlation between diversity and biomass degradation
in the organic cultivation and in the natural wetland,
while in the conventional system, this correlation was
significant. Probably the redundancy between groups
makes diversity greater than the minimum required to
keep this ecosystem functioning (Moulton et al., 2003),
both in the organic system and in the natural wetland.
However, for the conventional system, this diversity is
smaller, and any variation is related to losses in the
Figure 2. Percentual of functional trophic groups (predators;
ecosystem function. Our results on degradation agree
collector; filtering-collectors; scrapers; shredders; predators/
collectors-gatherers; collectors) found in the sampled
with those reported by Telöken et al. (2011), which
sites at 14, 28, 42, 56, and 70 days after the beginning of had greatest biomass losses in the initial phase, with a
incubation. CT, conventional system; OF: organic system; trend to stabilization that extends from the day 32 until
and NW, natural wetland. the end of the experiment, at day 71.

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Abundance did not correlate with biomass decay wetland, showing that the benthic macroinvertebrates
in the systems, but it was significant for the natural in cultivation areas were probably affected, having

Table 3. Abundance of benthic macroinvertebrates found in bags of foliar degradation in the areas of conventional (CT)
and organic systems (OF) residues, and on the area of the natural wetland (NW), at 14, 28, 42, 56, and 70 days after the
introduction of degradation bags, and their respective functional trophic group (FTG).
Taxon FTG(1) DAY 14 DAY 28 DAY 42 DAY 56 DAY 70
CT OF NW CT OF NW CT OF NW CT OF NW CT OF NW
Nematode P 8 19 108 0 4 10 0 0 11 14 89 65 1 88 107
Diptera
Ceratopogonidae P/Cc 0 0 1 0 0 0 0 0 8 0 0 0 0 0 0
Chaoboridae P 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Chironomidae Cc 0 19 270 15 19 331 14 19 109 20 86 11 47 100 7
Culicidae C 0 0 3 11 0 6 0 0 0 0 0 0 0 0 0
Sciomyzidae P 0 0 0 5 0 0 0 0 0 0 0 0 0 0 0
Syrphidae Cf 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0
Tabanidae P 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0
Tipulidae P 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0
Coleoptera
Dytiscidae P 1 1 2 1 0 0 3 0 0 0 0 0 0 0 0
Elmidae (immature) Cc 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1
Elmidae (adult) R 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0
Gyrinidae P 0 0 0 0 0 6 0 0 0 0 0 1 0 0 0
Haliplidae Cf 0 0 0 0 2 0 1 1 0 0 12 0 0 3 0
Hydrophilidae (immature) P 0 0 0 0 0 2 0 0 0 0 0 0 1 0 0
Hydrophilidae (adult) Cc 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0
Hydropsychidae Cf 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0
Hemiptera
Corixidae R 0 0 25 0 0 0 0 0 0 0 0 0 0 0 0
Hebridae P 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0
Hydrometridae P 0 0 0 0 1 0 1 0 0 0 0 0 0 0 0
Mesoveliidae P 0 0 0 0 0 7 0 0 0 0 0 1 0 0 0
Saldidae P 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0
Veliidae P 0 0 2 0 0 1 0 0 0 0 0 0 0 0 0
Odonata
Calopterigidae P 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0
Libellulidae P 0 1 1 0 0 2 1 0 0 0 0 0 0 0 0
Ephemeroptera
Baetidae Cc 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0
Caenidae Cc 0 5 7 0 2 15 0 0 3 0 0 3 0 0 0
Leptohyphidae Cc 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0
Trichoptera
Xyphocentronidae Cc 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0
Collembola Cc 6 8 877 4 0 186 0 1 1 0 0 2 0 0 0
Hirudinea P 8 7 28 5 7 21 0 11 34 2 12 34 6 9 28
Amphipoda F 4 65 22 89 3 0 1 0 0 30 14 0 2 10 3
Decapoda
Palaemonidae F 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0
Acari P 4 4 274 5 0 46 1 0 232 1 2 89 0 0 263
Bivalvia Cf 0 0 1 0 4 1 0 0 0 0 0 5 0 0 1
Gastropoda
Planorbidae R 3 0 1 1 0 3 1 0 0 2 0 0 1 0 0
Physidae R 0 0 9 0 0 1 0 0 0 0 0 1 0 0 0
Total 37 129 1641 137 42 643 23 32 398 69 217 212 59 210 410
(1)
P, predators; C, collectors; Cc, collector-gatherer; Cf, filtering-collectors; F, shredders; and R, scrapers.

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their contribution this process decreased in this (2009), palatability depends on the hardness of leaves,
changed environment. Degradation stability and and on concentrations of secondary compounds that
decrease of the macroinvertebrate abundance, from confer resistance to tissues, which causes a slower
day 42 after incubation on, may be related to rice straw litter decomposition. In addition, according to Cunha-
composition. From that period on, straw may contain Santino & Bianchini Jr. (2006), decomposition varies
compounds of difficult degradation, such as lignin and both because of factors related to litter – as the C:N:P
polyphenols, which would prevent the direct action ratio, material and origin, among others –, and because
of macroinvertebrates. According to Moretti et al. of external factors such as nutrient concentration,
temperature, and pH of the environment.
The systems studied had a lower abundance of
Table 4. Occurrence frequency of benthic macroinvertebrates benthic macroinvertebrates than natural wetlands; and
found in foliar degradation in the areas of conventional (CT) the diversity of these organisms was also reduced in
and organic (OF) systems, and natural wetland (NW). the conventional system. The evaluation of phytomass
Taxon CT OF NW degradation was sensitive to this differentiation of the
Nematode Ad Co Co environmental management, showing its effects on the
Ceratopogonidae - - Ad
functionality of this agroecosystem.
Chaoboridae Ad - -
Chironomidae Co Co Co
The reduction of ecosystem functions causes the
Culicidae Ad - Ad declining of nutrient availability, affecting the natural
Sciomyzidae Ad - - processes and other services, as the maintenance of
Syrphidae - - Ad plant and animal biodiversity, thus increasing crop
Tabanidae Ad - -
production costs; this way, the use of the organic
Tipulidae - - Ad
Dytiscidae Ad Ad Ad management or other less impactful systems, as
Elmidae (immature) - 0 Ad water management for invasive plants and integrated
Elmidae (adult) - - Ad pest management, are recommended to provide the
Gyrinidae - -0 Ad maintenance of the evaluated processes that may
Haliplidae Ad Ac -
Hydrophilidae (immature) Ad - Ad
improve gains from cultivation sustainability.
Hydrophilidae (adult) - - Ad
Hydropsychidae - Ad -
Hebridae - - Ad
Hydrometridae Ad - -
10 0.025
Mesoveliidae - - Ad
Saldidae - - Ad
Remaining phytomass (g)

Veliidae - - Ad 8 0.02

Decay coefficient (k)

Calopterigidae - - Ad
Libellulidae Ad Ad Ad 6 0.015
Baetidae - Ad -
Caenidae - Ad Ac 4 0.01
Leptohyphidae - - Ad
Xyphocentronidae - - Ad 2 0.005
Collembola Ad Ad Co
Hirudinea Ac Co Co
0 0
Amphipoda Co Co Ad 0 14 28 42 70
Palaemonidae Ad - - Days after incubation
Acari Ad Ad Co
Bivalvia - - Ac CT phytomass OF phytomass NW phytomass
Planorbidae Ac - Ad k CT k OF k NW
Physidae - - Ad
Figure 3. Decay coefficient of phytomass degradation and
Ad, accidental species (present in less than 25% of the collections); Ac,
incidental species (present in less than 50%, and more than 25% of the
amount of remaining phytomass during the experiment of
collections); and Co, constant species (present in more than 50% of the the studied management systems. CT, conventional system;
collections). OF, organic system; and NW, natural wetland.

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 Benthic macroinvertebrates and degradation of phytomass 269

Conclusions DI SABATINO, A.; GERECKE, R.; MARTIN, P. The biology and

ecology of lotic water mites (Hydrachnidia). Freshwater Biology,
1. The management systems promote differences v.44, p.47-62, 2000. DOI: 10.1046/j.1365-2427.2000.00591.x.
in the colonization of rice straw by benthic GIMENES, K.Z.; CUNHA-SANTINO, M.B. da; BIANCHINI
macroinvertebrates. JR., I. Decomposição de matéria orgânica alóctone e autóctone
em ecossistemas aquáticos. Oecologia Australis, v.14, p.1036-
2. The need to maintain diversity of benthic
1073, 2010. DOI: 10.4257/oeco.2010.1404.13.
macroinvertebrates becomes clear when there is
GROOT, R.S. de; WILSON, M.A; BOUMANS, R.M.J. A
diversity loss, as observed in rice straw biomass in the typology for the classification, description and valuation of
site of conventional system. ecosystem functions, goods and services. Ecological Economics,
3. Nutrient cycling, provided by phytomass v.41, p.393-408, 2002. DOI: 10.1016/S0921-8009(02)00089-7.
decomposition, is affected by the management system, HANDA, I.T.; AERTS, R.; BERENDSE, F.; BERG, M.P.;
and the delay in this process causes a reduction of BRUDER, A.; BUTENSCHOEN, O.; CHAUVET, E.;
the ecosystem function in the conventional system, GESSNER, M.O.; JABIOL, J.; MAKKONEN, M.; MCKIE, B.G.;
MALMQVIST, B.; PEETERS, E.T.H.M.; SCHEU, S.; SCHMID,
thus affecting its sustainability; nevertheless, 70 days
B.; RUIJVEN, J. van; VOS, V.C.A.; HÄTTENSCHWILER,
after the phytomass incubation, the remaining straw S. Consequences of biodiversity loss for litter decomposition
is similar in all treatments, which shows a resilience across biomes. Nature, v.509, p.218-221, 2014. DOI: 10.1038/
ability. nature13247.
KERANS, B.L.; KARR, J.R. A benthic index of biotic
Acknowledgments integrity (B-IBI) for rivers of the Tennessee Valey. Ecological
Applications, v.4, p.768-785, 1994. DOI: 10.2307/1942007.
To Embrapa Clima Temperado, to Fundação KOTTEK, M.; GRIESER, J.; BECK, C.; RUDOLF, B.; RUBEL,
de Amparo à Pesquisa do Estado do Rio Grande F. World Map of the Köppen-Geiger climate classification
updated. Meteorologische Zeitschrift, v.15, p.259-263, 2006.
do Sul (Fapergs), and to Conselho Nacional de
DOI: 10.1127/0941-2948/2006/0130.
Desenvolvimento Científico e Tecnológico (CNPq), for
MASSONI, P.F.S.; MARCHESAN, E.; GROHS, M.; SILVA, L.S.
their support and scholarship granted.
da; ROSO, R. Nutrientes do solo influenciados por diferentes
manejos da palha após a colheita do arroz irrigado. Revista
References Ciência Agronômica, v.44, p.205-214, 2013. DOI: 10.1590/
S1806-66902013000200001.
BARBOLA, I.F.; MORAES, M.F.P.G.; ANAZAWA, T.M.; MELO, S.; STENERT, C.; DALZOCHIO, M.S.; MALTCHIK,
NASCIMENTO, E.A.; SEPKA, E.R.; POLEGATTO, C.M.; L. Development of a multimetric index based on aquatic
MILLÉO, J.; SCHÜHLI, G.S. Avaliação da comunidade macroinvertebrate communities to assess water quality of rice
de macroinvertebrados aquáticos como ferramenta para o fields in southern Brazil. Hydrobiologia, v.742, p.1-14, 2015. DOI:
monitoramento de um reservatório na bacia do rio Pitangui, 10.1007/s10750-014-1957-7.
Paraná, Brasil. Iheringia. Série Zoologia, v.101, p.15-23, 2011.
MONKS, P.L.; FERREIRA, O.G.L.; GOULART, E.Q.; TERRES,
DOI: 10.1590/S0073-47212011000100002.
A.L.S. Potencial forrageiro do arroz irrigado (Oryza sativa L.)
BARDGETT, R.D.; PUTTEN, W.H. van der. Belowground após a colheita dos grãos. Revista Brasileira de Agrociência,
biodiversity and ecosystem functioning. Nature, v.515, p.505– v.8, p.67-70, 2002.
511, 2014. DOI: 10.1038/nature13855.
MORETTI, M.S.; GONÇALVES JÚNIOR, J.F.; LIGEIRO,
CARVALHO, E.M.; UIEDA, V.S. Seasonal leaf mass loss R.; CALLISTO, M. Invertebrates colonization on native tree
estimated by litter bag technique in two contrasting stretches of a leaves in a neotropical stream (Brazil). International Review
tropical headstream. Acta Limnologica Brasiliensia, v.21, p.209- of Hydrobiologia, v.92, p.199-210, 2007. DOI: 10.1002/
215, 2009. iroh.200510957.
CUMMINS, K.W.; MERRITT, R.W.; ANDRADE, P.C.N. The MORETTI, M.S.; LOYOLA, R.D.; BECKER, B.; CALLISTO,
use of invertebrate functional groups to characterize ecosystem M. Leaf abundance and phenolic concentrations codetermine the
attributes in selected streams and rivers in south Brazil. Studies selection of case-building materials by Phylloicus sp. (Trichoptera,
on Neotropical Fauna and Environment, v.40, p.69-89, 2005. Calamoceratidae). Hydrobiologia, v.630, p.199-206, 2009. DOI:
DOI: 10.1080/01650520400025720. 10.1007/s10750-009-9792-y.
CUNHA-SANTINO, M.B.; BIANCHINI JR., I. Modelos MORMUL, R.P.; VIEIRA, L.A.; PRESSINATTE JÚNIOR,
matemáticos aplicados aos estudos de decomposição de macrófitas S.; MONKOLSKI, A.; SANTOS, A.M. dos. Sucessão de
aquáticas. Oecologia Brasiliensis, v.10, p.154-164, 2006. DOI: invertebrados durante o processo de decomposição de duas
10.4257/oeco.2006.1002.03. plantas aquáticas (Eichhornia azurea e Polygonum ferrugineum).

Pesq. agropec. bras., Brasília, v.52, n.4, p.261-270, abr. 2017

DOI: 10.1590/S0100-204X2017000300006
270 L.T. Winckler et al.

Acta Scientiarum. Biological Sciences, v.28, p.109-115, 2006. RIZO-PATRÓN V., F.; KUMAR, A.; COLTON, M.B.M.;
DOI: 10.4025/actascibiolsci.v28i2.1017. SPRINGER, M.; TRAMA, F.A. Macroinvertebrate
MOULTON, T.P.; MAGALHÃES, S.A.P. Responses of leaf communities as bioindicators of water quality in conventional
processing to impacts in streams in Atlantic rain Forest, Rio de and organic irrigated rice fields in Guanacaste, Costa Rica.
Janeiro, Brazil – a test of the biodiversity-ecosystem functioning Ecological Indicators, v.29, p.68-78, 2013. DOI: 10.1016/j.
relationship? Brazilian Journal of Biology, v.63, p.87-95, 2003. ecolind.2012.12.013.
DOI: 10.1590/S1519-69842003000100012. RODRIGUES, W.C. DivEs - Diversidade de Espécies: an
MUGNAI, R.; NESSIMIAN, J.L.; BAPTISTA, D.F. Manual de ecological software: v3.0. 2014. Available at: ˂http://dives.ebras.
identificação de macroinvertebrados aquáticos. Rio de Janeiro: bio.br/downloads.aspx˃. Accessed on: Jan. 29 2016.
Technical Books, 2010. 174p.
SANTOS, I.G.A. dos; RODRIGUES, G.G. Colonização de
NAKAGOME, F.K.; NOLDIN, J.A.; RESGALLA JR., C. macroinvertebrados bentônicos em detritos foliares em um
Toxicidade aguda de alguns herbicidas e inseticidas utilizados em riacho de primeira ordem na Floresta Atlântica do Nordeste
lavouras de arroz irrigado sobre o peixe Danio rerio. Pesticidas: brasileiro. Iheringia. Série Zoologia, v.105, p.84-93, 2015. DOI:
Revista de Ecotoxicologia e Meio Ambiente, v.17, p.117-122, 10.1590/1678-4766201510518493.
2007. DOI: 10.5380/pes.v17i0.9186.
SANTOS, K.P. dos. Macroinvertebrados bentônicos e
NIN, C.S.; RUPPENTHAL, E.L.; RODRIGUES, G.G. Produção
parâmetros físico-químicos como indicadores da qualidade da
de folhiço e fauna associada de macroinvertebrados aquáticos em
água de microbacias utilizadas para o abastecimento público
curso d’água de cabeceira em Floresta Ombrófila do Estado do Rio
Grande do Sul, Brasil. Acta Scientiarum. Biological Sciences, da região metropolitana de Goiânia. 2014. 69p. Dissertação
v.31, p.263-271, 2009. DOI: 10.4025/actascibiolsci.v31i3.355. (Mestrado) - Universidade Federal de Goiás, Goiânia.

OLIVEIRA, A.; CALLISTO, M. Benthic macroinvertebrates SILVEIRA, V.M. da; ANTUNES, G.M.; DIAS, M.F.P. Inovação
as bioindicators of water quality in an Atlantic forest fragment. em sistemas de produção de arroz orgânico no Rio Grande do
Iheringia. Série Zoologia, v.100, p.291-300, 2010. DOI: 10.1590/ Sul. Revista de Administração da UFSM, v.5, p.715-728, 2012.
S0073-47212010000400003. Edição especial. DOI: 10.5902/198346597782.
PETERSEN, R.C.; CUMMINS, K.W. Leaf processing in a TELÖKEN, F.; ALBERTONI, E.F.; HEPP, L.U.; PALMA-SILVA,
woodland stream. Freshwater Biology, v.4, p.343-368, 1974. C. Invertebrados aquáticos associados a serapilheira de Salix
DOI: 10.1111/j.1365-2427.1974.tb00103.x. humboldtiana em um riacho subtropical. Ecología Austral, v.24,
PILLAR, V. de P.; ORLÓCI, L. On randomization testing in p.220-228, 2014.
vegetation science: multifactor comparisons of relevé groups. TELÖKEN, F.; ALBERTONI, E.F.; PALMA-SILVA, C. Leaf
Journal of Vegetation Science, v.7, p.585-592, 1996. DOI: degradation of Salix humboldtiana Willd. (Salicaceae) and
10.2307/3236308. invertebrate colonization in a subtropical lake (Brazil). Acta
PILLAR, V.D.P. MULTIV: multivariate exploratory analysis, Limnologica Brasiliensia, v.23, p.30-41, 2011. DOI: 10.4322/
randomization testing and tootstrap resampling: User’s Guide v. actalb.2011.016.
2.1. Porto Alegre: Universidade Federal do Rio Grande do Sul,
THRUPP, L.A. Linking agricultural biodiversity and food
2001. Available at: <http://ecoqua.ecologia.ufrgs.br/arquivos/
Software/Multiv/MultivManual.pdf>. Accessed on: Oct. 10 2015. security: the valuable role of agrobiodiversity for sustainable
agriculture. International Affairs, v.76, p.265-281, 2000. DOI:
PIRES, M.M.; KOTZIAN, C.B.; SPIES, M.R.; BAPTISTA, V. 10.1111/1468-2346.00133.
dos A. Comparative assessment of aquatic macroinvertebrate
diversity in irrigated rice fields and wetlands through different WILSON, A.L.; WATTS, R.J.; STEVENS, M.M. Effects of
spatial scales: an additive partitioning approach. Marine and different management regimes on aquatic macroinvertebrate
Freshwater Research, v.67, p.368-379, 2015. DOI: 10.1071/ diversity in Australian rice fields. Ecological Research, v.23,
mf14109. p.565-572, 2008. DOI: 10.1007/S11284-007-0410-z.

Received on June 7, 2016 and accepted on November 9, 2016

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DOI: 10.1590/S0100-204X2017000300006