Although studies have shown enhancement of insects, birds, and plants in organically managed agroecosystems, information on arthropod diversity and abundance in conventional and organic sugarcane farms is scarce. This research was conducted to analyze and compare the diversity and abundance of edaphic arthropods in organic and conventional sugarcane by using pitfall traps. The study was conducted during 2 growing seasons in Jaboticabal, São Paulo, Brazil. In total, 13,244 individuals belonging to 190 morphospecies were collected. In the conventional system, 4,964 specimens were collected, representing 122 morphospecies distributed in 15 orders and 50 families. In the organic system, 8,280 individuals were captured, representing 142 morphospecies in 13 orders and 45 families. Ants of the genera Pheidole Westwood, Dorymyrmex Mayr, Camponotus Mayr, and Crematogaster Lund (Hymenoptera: Formicidae) were predominant. Higher abundance and richness of arthropods (especially predators and omnivores) were found in the organic than the conventional system, which could be important in regulating key pests of sugarcane. Our results show that the organic management in sugarcane increased the abundance and diversity of arthropods.
Conventional agriculture has often caused the simplification of agricultural landscapes, mainly due to the establishment of monocultures (Pogue & Schnell 2001). These simplified agricultural practices and overuse of insecticides can lead to a reduction in biodiversity (Butler et al. 2007), and thus the reduction of ecological services. On the other hand, with the increase of organic farming, conservative biological control is also expected to increase due to the reduction in pesticide use and land management, which in turn enhance survival, fecundity, efficiency, longevity, and maintenance of natural enemies of arthropod pests (Eilenberg et al. 2001; Landis et al. 2005).
Current agricultural system management can be characterized by frequent and intense disturbances, which are unfavorable for conservation of natural enemies (Letourneau 1998). Thus, development and maintenance of an ecological infrastructure to provide food resources, shelter, and alternative prey and hosts are the basis of environmental management. Consequently, it is possible to expand natural biological control by preserving and increasing existing populations of beneficial arthropods in crops (Gurr et al. 2000; Landis et al. 2000; Wilkinson & Landis 2005).
Environmental problems associated with conventional sugarcane agriculture due to the use of fire prior to harvest (forbidden in certain Brazilian regions since 2014), and use of pesticides, are well documented (Nunes et al. 2006). However, few studies have characterized the soil-dwelling arthropods that could be affected by these disturbances in sugarcane agroecosystems (Castelo Branco et al. 2010; Pasqualin et. 2012; Abreu et al. 2014). Consequently, the objective of this work was to analyze and compare the diversity and abundance of edaphic arthropods in conventional and organic sugarcane fields.
Materials and Methods
CHARACTERIZATION OF THE AREA
The experiment was conducted in 2 sugarcane areas in Jaboticabal municipality, São Paulo, Brazil. The sugarcane variety RB5536 was used in each of 2 seasons. Each area was about 10 ha. In the conventional field (21.1978°S, 48.2897°W, altitude 589 m), agricultural practices included pre-harvest burning and herbicide use for weed control but no insecticide application. In the organic field (21.1858°S, 48.2450°W; altitude 623m), sugarcane has been harvested without burning for about 10 yr (green cane) and grown without use of any pesticide. In the 1st growing season (2011/2012, 7th ratoon), the experiment started when plants were in the 4th month of development, whereas in the 2nd growing season (2012/2013, 8th ratoon), the experiment started just after harvest.
In each plot, 3 parallel transects distanced 10 m apart from each other were established. Five pitfall traps (700 mL plastic cups buried and adjusted to ground level) were installed every 10 m on each transect, with the 1st trap installed 20 m from the edge of the plot. The traps received 100 mL of solution (98 mL water + 2 mL detergent) to prevent captured arthropods from escaping.
Sample collections began 24 h after installation of traps to reduce the effect of disturbance caused by soil excavation and trap installation (Araújo et al. 2005). The traps remained for 48 h in the experimental areas. Collected arthropods were taken to the laboratory for sorting and identification. Fifteen monthly collections were conducted during the 2011/2012 (Dec 2011 to May 2012) and 2012/2013 (Oct 2012 to Mar 2013) growing seasons.
IDENTIFICATION OF COLLECTED ARTHROPODS
The arachnids were sent to Instituto Butantan (São Paulo, Brazil) for identification. The other arthropods collected were identified to lowest possible taxonomic level by using specialized literature (Loureiro & Queiroz 1990; Borror et al. 1992; Baccaro 2006; Suguituru et al. 2015). Unidentified species were differentiated into morphospecies (Oliver & Beattie 1996).
Data were analyzed using the software ANAFAU (Moraes & Haddad 2003), and the faunistic indices dominance, abundance, frequency, and constancy were obtained for each system. Moreover, the program performs residual analysis of discrepant data that can be classified into exclusive categories known as super-dominant, super-abundant, and super-frequent. The dominance was calculated by the equation DL = (1 / S) × 100, where DL = dominance limit and S = total number of species per sample. The abundance was calculated using the standard deviation and confidence interval of the arithmetic mean at 1 and 5% probabilities. For frequency, the equation F = (n / N) × 100 was adopted, where F = frequency (%), n = number of specimens of each species collected, and N = total number of specimens of the collected species. For constancy, the equation C = (P / N) × 100 was used, where C = constancy, P = number of samples containing the species, N = total number of samples collected (Silveira Neto et al. 1976).
Diversity was assessed using the species diversity indices of Shannon—Wiener (H′) and Margalef (α). The equitability index (E) was calculated to evaluate the uniformity of the captures and how the individuals are distributed in the sample, using the ANAFAU software (Moraes & Haddad 2003). The similarity index assessed the number of species shared between the 2 cropping systems.
To estimate the total species richness for each system, the software EstimateS® 9.1 was used to generate species accumulation curves and to compare the conventional and organic system (Colwell 2006). Samples were randomized 100 times, without replacement, using the non-parametric estimator first order Jackknife (Jack 1), which uses the number of unique species or species occurring only once in a sample to produce richness estimates (Heltshe & Forrester 1983). Also, principal component analysis (STATISTICA, StatSoft, Inc., Tulsa, Oklahoma) was performed separately on the collection from each month. Thus, 15 samples (= months of evaluation) were used in the analysis for each area.
ARTHROPOD RICHNESS AND ECOLOGICAL ANALYSIS
In total, 13,244 individuals belonging to 190 morphospecies were collected in sugarcane. The number of individuals collected during the 2 growing seasons in the conventional system was 4,964 (37.48%), and was represented by 122 morphospecies distributed in 15 orders and 50 families. In the organic system, 8,280 individuals (62.52%) were captured, corresponding to 142 morphospecies in 13 orders and 45 families (Table 1). The number of individuals collected in the organic crop was 66.8% higher, although the numbers of taxonomic orders and families observed were slightly lower than in the conventional crop.
The Shannon—Wiener index (H′), used to estimate the diversity of arthropods considering the uniformity of abundance of species, was 2.3 for the conventional system and 2.5 for the organic system (Table 1). The Margalef index (α), calculated by the number of species and the logarithm of the total number of individuals, was 14.1 for the conventional system and 17.1 for the organic system. The equitability or uniformity parameter, which varies from 0 to 1 (the closer to 1 the greater the equality of species abundance), was approximately 0.49 for both production systems, suggesting that the arthropod community sampled tends to coexist in both systems with some dominance of certain species. The similarity between the areas was 0.687.
In total, 2 and 17 morphospecies in the conventional system and 4 and 30 morphospecies in the organic system were observed to be super-dominant and dominant, respectively (Table 2). The number of non-dominant species was about 7% lower for the conventional system (103 morphospecies) in comparison with the organic system (108 morphospecies) (Table 2).
Among the 43 super-dominant and dominant morphospecies, which represented 23.5% of the total number of morphospecies, 10 (23.3% of the super-dominant and dominant) were collected in both systems. The numbers of individuals of the dominant and non-dominant morphospecies were 1,577 and 367 (conventional system) and 1,825 and 345 (organic system), respectively. However, the number of individuals of the super-dominant morphospecies in the organic system (6,110) was twice that observed in the conventional system (3,020) (Table 2).
Ants (Hymenoptera: Formicidae) of the genera Pheidole Westwood and Dorymyrmex Mayr collected in the conventional system were super-dominant morphospecies whereas Camponotus Mayr and Crematogaster Lund were considered dominant. On the other hand, these 4 genera were super-dominant in the organic system. Superdominant species are native species that behave as invaders in a disturbed environment (Silva-Mattos & Pivello 2009). Other ant genera were important and classified as dominant. For example, leaf-cutting ants of the genus Atta F. are important pests in sugarcane crops and were found in both sugarcane fields. Moreover, other beneficial ant genera (Brachymyrmex Mayr, Ectatomma Smith, and Gnamptogenys Roger) were found in both organic and conventional systems. Also, we found dominant morphospecies of spiders (4 morphospecies in total) only in the organic system.
Number of individuals captured, faunistic indices (dominance, abundance, frequency, constancy) and functional groups of arthropods captured using pitfall traps in conventional and organic sugarcane systems in Jaboticabal, São Paulo, Brazil, during the 2011/2012 and 2012/2013 growing seasons.
Distribution of morphospecies in relation to faunistic indices of dominance, abundance, frequency, and constancy captured in pitfall traps in conventional and organic sugarcane systems in Brazil (2011/12 and 2012/13 growing seasons).
Similarly to the observed dominance, morphospecies of the genera Pheidole and Dorymyrmex were super-abundant in both the conventional and organic systems, but morphospecies of the genera Camponotus and Crematogaster were super-abundant only in the organic system. These 2 latter genera, on the other hand, were classified as very abundant in the conventional system. The super-abundant and very abundant species are native species that behave as invaders in a disturbed environment (Silva-Mattos & Pivello 2009). The conventional system presented a greater number of rare morphospecies (84) compared with common (16), very abundant (11), occasional (7), and abundant (2) morphospecies. A similar trend was observed for the organic system, in which a greater number of rare morphospecies (86) were observed compared with common (19), very abundant (19), and occasional morphospecies (9), as well as abundant (5) morphospecies. Therefore, 69.4% and 61.1% of the morphospecies were rare in the conventional and organic system, respectively. Twenty-eight morphospecies (14.7% of the total morphospecies) considered to be rare occurred on both systems.
The super-frequent morphospecies (i.e., species that occurred on all sampling dates) were the same as the super-abundant and the super-dominant morphospecies. Ants of the genera Camponotus, Crematogaster, Dorymyrmex, and Pheidole were the super-frequent morphospecies in the organic system, whereas only the last 2 genera were super-frequent in the conventional system (Tables 1 and 2).
Most morphospecies were considered uncommon, i.e., their occurrence was below 34% of the samplings, in both systems. In this category, 91 (47.9%) and 95 (51%) morphospecies occurred at low frequencies in the conventional and organic systems, respectively.
In this category, most morphospecies occurred accidentally. In the conventional system, 95 morphospecies were considered accidental, 16 accessories, and 11 constant, whereas in the organic system, there were 103 accidental, 23 accessories, and 16 constant morphospecies (Table 1). The most constant morphospecies were the ants with 30% and 40% of total morphospecies in the organic and the conventional system, respectively.
We also analyzed the specimens classified among the high faunistic values (super-dominant, dominant, super-abundant, very abundant, abundant, super-frequent, very frequent, frequent, and constant), and we found 22 (8 predators, 5 omnivores, 5 detritivores, and 4 herbivores) and 10 (5 predators, 3 omnivores, and 2 herbivores) species for organic and conventional systems, respectively. Among the morphospecies collected, 7 were common in both systems (3 omnivores [Brachymyrmex spp., Camponotus spp., Pheidole spp.], 3 predators [Crematogaster spp., Dorymyrmex spp., Ectatomma spp.], and 1 herbivore [Atta spp.]), 3 were found exclusively in the conventional system (2 predators and 1 herbivore), and 15 were found exclusively in the organic system (5 predators, 5 detritivores, 2 omnivores, and 3 herbivores).
Estimates of species richness were similar and close to the expected number of species as shown in Fig. 1. The species curves for both organic and conventional sugarcane systems tended to stabilize (plateau) when 15 samples were taken on a monthly basis. Thus, the number of monthly collections and traps adopted in the study was adequate for assessing species diversity in sugarcane agroecosystems.
A comparison of the edaphic arthropods by using principal component analysis indicated that there was a difference between the sugarcane systems. Eleven samples (73.3%) out of 15 taken from the organic sugarcane field presented negative values, whereas 13 samples (86.7%) out of 15 from the conventional field presented positive values (Fig. 2). Therefore, the communities were different both quantitatively and qualitatively. Ants generally were the most abundant species found on both systems, but they were more abundant in the organic than the conventional system.
Twice as many soil-dwelling arthropods were captured in the organic cropping system, relative to conventional sugarcane production. Also, greater numbers of arthropod predators and omnivores and smaller numbers of herbivores were captured in the organic field. This is shown by the high dominance and frequency of coleopteran and hymenopteran predators in the organic system. These predators are reported reported as important natural control agents of several pests that occur in different stages of sugarcane development (Mendonça & Marques 2005; Costa et al. 2007; Silva et al. 2009).
Our results also suggest that compared with the conventional system, the organic system could provide greater availability and abundance of resources such as pollen, nectar, and alternative sources of food and shelter, which favor the abundance and diversity of species (Landis et al. 2000). Root (1973) noted that systems providing appropriate conditions (food and shelter) tend to have greater abundance of arthropod predators and omnivores, and therefore greater potential for biological control of herbivores.
Among the predators, ant and spider species occurred frequently in both systems. Several studies have shown ants in the genera Crematogaster, Dorymyrmex, Ectatomma, and Pheidole are effective control agents of pests in sugarcane (Rossi & Fowler 2002, 2004; Araújo et al. 2004, 2005; Pereira et al. 2004; Philpott et al. 2008; Schatz et al. 2008), but their population dynamics remain to be better understood. For spiders in the sugarcane agroecosystem, there is practically no published information about their diversity, although this work suggests that they are especially abundant elements in organic sugarcane production, and their contribution should be assessed.
Pheidole spp. and Dorymyrmex spp. ants were the only super-dominant species in the conventional system. Thus, even with the disruption caused by the use of fire in conventional harvesting, populations of these species were not affected, as also observed by Araújo et al. (2004). Ant species generally present rapid colony restructuring, wide foraging area, and social organization. These features may have contributed to the high abundance, frequency, and constancy in the conventional area (Rossi & Fowler 2002; Araújo et al. 2004, 2005). The fact that most super-dominant species were detected in the organic system (Pheidole spp., Dorymyrmex spp., Crematogaster spp., and Camponotus spp.) may be related to the nesting strategy of these species. According to Longino (2003), Crematogaster and Dorymyrmex ants have shallow nests and therefore may be more affected by the fire, so the reestablishment of colonies requires longer period of time.
However, it is not only the direct effects of fire that can lead to reduced biodiversity in the conventional system. Herbicides are used to control weeds whose elimination can indirectly affect the population of arthropods. Many herbivorous insects feed on the weeds that occur in crops (Chiverton & Sotherton 1991). Arthropod predators and parasitoids also can utilize these weeds to supplement their diet by feeding on pollen and nectar. Thus, herbicides can affect biodiversity, either by acting directly (on herbivores) or indirectly (on predators and omnivores).
In spite of the higher species richness in the organic than the conventional system, both the faunistic and diversity indices were generally similar. We hypothesize that this finding may be related to surrounding sugarcane areas, which may have been used as a shelter or refuge for some arthropods, especially beneficial arthropods, during harvest in the 2 systems. Although this needs to be further studied in this agroecosystem, harvesting the sugarcane at different times may facilitate the movement of arthropods between different areas, allowing the reoccupation of the disturbed environment more quickly.
The study of arthropod biodiversity may allow us to identify important naturally occurring beneficials in the agroecosystem. Despite having used only pitfall trapping, this study provided comparative information on biodiversity in the sugarcane agroecosystem under 2 management systems. This new information may assist future studies on biological control, or even risk assessment of genetically modified sugarcane, where it is essential to know the diversity of arthropods. Overall, our results indicated that the organic management of sugarcane improves the abundance and diversity of arthropods (especially predators and omnivores) relative to conventional management.
The authors are grateful to Antonio Brescovit and João Lucas Chavari, Instituto Butatan, São Paulo, Brazil, who kindly identified the spiders. Scholarship to the first author was provided by CAPES, Brazil.