Are Dung Beetles Driving Dung-Fly Abundance in Traditional Agricultural Areas in the Amazon?
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- Braga, R.F., Korasaki, V., Audino, L.D. et al. Ecosystems (2012) 15: 1173. doi:10.1007/s10021-012-9576-5
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We evaluated the effects of different land-use systems on the ability of dung beetles to control the population of detritus-feeding flies. We tested the hypotheses that intensification of land use will reduce dung beetles richness, abundance and biomass and, consequently, their dung burial ability, affecting the interaction between dung beetles and flies and reducing its effectiveness as a natural biological control. In the Brazilian Amazon we sampled dung beetles, fly larvae and adults; and recorded the rate of dung removal by dung beetles across a gradient of land-use intensity from primary forest, secondary forest, agroforestry, agriculture to pasture. Our results provide evidence that land-use intensification results in a reduction of the richness, abundance and biomass of dung beetles, and this in turn results in lower rates of dung removal in the most simplified systems. We found no significant differences in the abundance of fly larvae between the different systems of land use. However, the number of adult flies differed significantly between land-use systems, presenting higher abundance in those sites with greater intensity of use (pasture and agriculture) and a lower abundance of adult flies in forested systems (primary and secondary forests, and agroforestry). Information-theoretic model selection based on AICc revealed strong support for the influence of land-use systems, dung removal rates and dung beetle abundance, biomass and richness on adult dung-fly abundance. Our results also reveal that dung beetles are not solely responsible for fly control and that other factors linked to land use are influencing the populations of these detritus-feeding insects.
Keywordsbiological controlconservation biologyecosystem functionhabitat changeScarabaeinaetropical forest
Scarabaeinae dung beetles are known for their great potential to reduce detritus-feeding fly populations (Hanski 1991; Nichols and others 2008). This biological control process results from competition between dung beetles and flies for dung and carrion, because both use this resource for feeding and breeding (Hanski 1991). Dung beetles have both direct and indirect negative effects on flies through exploitative competition and by causing mechanical damage to both eggs and larvae during the dung removal process (Bornemissza 1960; Ridsdill-Smith and Hayles 1990; Bishop and others 2005; Horgan 2005; Nichols and others 2008; Wu and Sun 2010). In addition, dung beetle action on dung pats can promote changes in the microclimatic and increase access for predators, reducing the development and survival of immature flies (Ridsdill-Smith and Hayles 1987).
Anthropogenic systems in the tropics can provide an ideal context for blood-sucking and detritus-feeding fly outbreaks. These flies may act as vectors of human and domestic animal diseases, resulting in a social, economic, and public health problem, especially in poor areas (Miller 1954; Miller and others 1961; Byford and others 1992). In the last decades, dung beetles have been successfully introduced into countries such as Australia, the USA, and Brazil to increase the biological control of blood-sucking flies of veterinary importance (Waterhouse 1974; Bornemissza 1979; Koller and others 2007). The biological control of flies associated with dung removal is estimated at 130 million dollars per year in North American pastures alone (Losey and Vaughan 2006).
The destruction of tropical ecosystems as a result of agricultural and logging activities has reached alarming levels in South America, Africa, and Asia (Geist and Lambin 2002; Gardner and others 2009; Gibbs and others 2010). In this context, the natural control of flies provided by dung beetles may be modelled by land-use changes, because the replacement and over-simplification of natural ecosystems are the main causes of dung beetle biodiversity loss (Nichols and others 2007; Gardner and others 2008; Shahabuddin and others 2010) and the functions/services associated with them (Klein 1989; Horgan 2005; Slade and others 2007; Barragán and others 2011; Slade and others 2011).
Materials and Methods
The regional climate ranges from humid to super humid Af (Köppen), lacks a dry season, and has an annual mean temperature and rainfall of 25.7°C and 2,562 mm, respectively. Rainfall in the driest month is greater than 100 mm, and the greatest levels of rainfall occur from December to April. A recent and detailed soil survey demonstrated that Inceptisols were the dominant soil class (Coelho and others 2005).
Seventy-five sampling points were distributed across six grids, approximately 9 ha each, to include all the major regional land-use systems (LUSs). Each sampling point was geo-referenced and was part of a pre-established grid, following the institutional norms of the project for all of the countries involved (Fidalgo and others 2005). The distance between points was generally 100 m, but was reduced to 50 m in some cases where more replicates per LUS were necessary.
We evaluated five different LUSs: Primary Forest (PF, n = 16) representing the original forest cover; Secondary Forest (SF, n = 15) composed of secondary vegetation in different successional stages after plant cropping; Agroforestry (AF, n = 15) formed by the naturally regenerating forest enriched with fruit trees; Agriculture (AG, n = 14) which were small areas (<1.5 ha) of slash and burn crops; and Pasture (PA, n = 15) which included areas for livestock rearing covered by native and introduced grasses.
Dung Removal Rate by Dung Beetles
We exposed 70 g of feces (1:1 human/pig dung) to the dung beetle community for 24 h at each sampling point. After 24 h the remaining dung was collected and weighed in UFAM’s (Universidade Federal do Amazonas) Laboratory of Ecology to record the rate of dung removal. We controlled for water loss by using a parallel control experiment which excluded all insect groups from the dung.
Larvae and Adult-Fly Sampling
We installed a trap to catch scavenging flies 1 m away from the experimental deposit of dung. We used a modified version of the flytrap proposed by Ferreira (1978) baited with 20 g of feces (1:1 human/pig dung). Flies entering through openings in the base of the trap are able to oviposit in the dung pad, but are trapped in a plastic-bag collector when they attempt to exit through the top of the trap. After 24 h of exposure the traps were removed from the field and taken to UFAM’s laboratory. The adults were sorted and counted, whereas the larvae were left in the dung sample for a 48-h period to increase in size and facilitate counting. Both adult and larval flies were used as a proxy for the fly community.
Dung Beetle Sampling
After removing the flytrap and experimental dung pad we installed pitfall traps to sample the dung beetle community. This was carried out after these two experiments were removed to prevent any possible interference on dung removal. We installed three human-dung baited pitfall traps (19 cm diameter, 11 cm deep) at the sample point in the corners of a triangle with sides of 2 m. Inside each trap 250 ml of saline plus detergent solution were added. The traps were exposed for 24 h and after this period the material was collected and sent to the Laboratory of Ecology and Conservation of Invertebrates, Universidade Federal de Lavras (UFLA). In the laboratory the beetles were sorted, identified and dried in an oven until a constant weight. Later, 30 individuals of each species were weighed on a balance (to 0.0001 g).
Effect of Land Use on Dung Beetles, Flies, and Dung Removal
To determine whether the different land uses differed with respect to richness, abundance and biomass of dung beetles, feces removal rate, and number of larvae, and adult flies, we performed a series of generalized linear models (GLMs). We used the categories of land use as fixed variables and community and ecosystem function variables as responses. Subsequently, we performed a contrast analysis to verify which systems were of distinct relation to the response variables. We used the structure of quasi-Poisson errors for abundance and biomass of dung beetles and for abundance of larvae and adult flies, Poisson errors for dung beetle richness and quasi-binomial errors for the dung removal rate. All GLMs were submitted to residual analysis to evaluate the adequacy of error distribution (Crawley 2002).
Effects of Dung Beetles on Dung Removal and on Flies
We used generalized linear mixed-effect models (GLMMs) to examine whether the land-use system and abundance, biomass, and richness of dung beetles affected the rate of dung removal and the abundance of adult flies. We used an information-theoretic approach based on the second-order Akaike’s information criterion corrected for small sample size (AICc—see Burnham and Anderson 2002) to rank the models. Mixed-effects models were also used to account for grid effects, entered as a random factor, with 14–16-independent samples nested within six grids, with five land-use systems (a total of 75 samples). Models were run using the “glmer” function in the “lme4” package in the R environment and fitted using Laplace approximation and Poisson errors (R. Development Core Team 2008). We used the “dredge” function from the “MuMIn” package to test models defined by all possible variable combinations and ranked them by the AICs-based model weight (Burnham and Anderson 2002). All analyses were performed using the software R (2008).
There were no significant differences in the abundance of fly larvae between the different systems of land use (F = 0.17, P > 0.05; Figure 3B). However, the number of adult flies differed between LUSs with higher abundance in those sites with greater intensity of use (pasture and agriculture) and a lower number of adult flies in forest ecosystems (primary forests, secondary and agroforestry) (F = 4.69, P < 0.05; Figure 3B).
AICc-Based Model Selection for Dung Removal and Adult Flies
Model ranks Total abundance
R + LUS
A + LUS
A + B + LUS
A + B + R + LUS
B + R + LUS
A + R + LUS
B + LUS
A + B + R + DR + LUS
B + R + DR + LUS
A + R + DR + LUS
R + DR + LUS
The model that best explained adult flies was based on the land-use system, dung removal rate, abundance, biomass, and richness of dung beetles (best model, ω = 1) (Table 1). Model 1 was the only one with strong support, because in this model ΔAICc was less than two. Thus, land-use system, dung removal rate, abundance, biomass, and richness of dung beetles are important in determining the abundance of adult flies. These five variables explained 20.5% of the total deviance in the data (Table 1).
In the last few decades, the scientific community has faced a growing debate on how changes in biodiversity may result in a disruption to the functioning of an ecosystem (Tilman and others 1997; Chapin and others 2000; Schwartz and others 2000; Srivastava and Vellend 2005). Under natural conditions we evaluated the cascading effect of land-use system simplification on the relationship between dung beetles and detritivorous flies (Figure 1). This study highlights the complex nature of biodiversity functions in response to land-use intensification. Our results show that this intensification could interfere in the interaction between dung beetles and flies, mediated by dung removal, and also notes that other factors, such as the traits of each land-use system, could influence the population of flies.
Effect of Land Use on Dung Beetles
Our results showed that land-use intensification resulted in a reduction of richness, abundance, and biomass of dung beetles. In our study, the primary forest sustained the highest patterns of dung beetle diversity and the pasture had the lowest values. Secondary forest, agroforestry, and agriculture had similar patterns in dung beetle abundance. However, secondary forest presented higher values of biomass and species richness when compared with agroforestry and pasture.
Not all land-use changes have the same effect on dung-beetle communities. Several studies have documented that land-use systems that are more structurally complex present higher diversity and biomass of dung beetles when compared to simplified ecosystems (for example, Harvey and others 2006; Nichols and others 2007; Gardner and others 2008; Shahabuddin and others 2010). In our study, the patterns of the dung-beetle community were not sequentially disrupted with simplification of the land-use system, but corroborate the results of Nichols and others (2007). Their metaanalysis on the effects of different land-use systems on dung beetles verified that intact forests supported the highest dung beetle species richness, clear-cuts the lowest and all other habitats, such as secondary forest, agroforestry, tree plantations, supported an intermediate level of species richness.
Contrary to our expectations, abundance in agroforestry and agriculture was the same as the secondary forest. This can be explained due to the fact that the indigenous community remains longer in areas of agriculture and agroforestry, growing and harvesting food products for consumption, and defecating nearby, therefore providing a stable food resource for dung beetles (obs. pers.). Even though agriculture and agroforestry present the same rates of dung beetle abundance, the secondary forest showed a higher biomass of dung beetles. The high overall dung beetle abundance in agriculture and agroforestry was due to the high number of small-sized species, which contributed little in relation to total biomass. However, the high dominance of these species in agriculture and agroforestry resulted in an equal abundance of dung beetles in these systems with those observed in secondary forest. This result highlights the importance of dung beetles in the maintenance of ecosystems, especially in more intense land-use systems. Despite the loss of species richness and biomass in agroforestry, the large number of small individuals in these systems suggests that density compensation is occurring (Slade and others 2011).
Effect of Dung Beetle Community Structure on Dung Removal Rates
Land-use intensification resulted in a reduction of richness, abundance, and biomass of dung beetles, and this in turn resulted in lower rates of dung removal in the most simplified systems. Primary forest had the highest levels of dung removal rates, whereas pasture had the lowest values. Secondary forest, agroforestry and agriculture had intermediate values and similar patterns of dung removal. AICc-based model selection revealed that land-use system, abundance, biomass, and richness of dung beetles explained around 75% of dung removal data, suggesting that these variables are important in determining this ecological function.
It has been suggested by a number of authors that some functions performed by dung beetles, such as secondary seed dispersal, bioturbation and dung burial, are associated with species richness, abundance, and body size of beetles (for example, Halffter and Edmonds 1982; Edwards and Aschenborn 1987; Andresen 2002; Horgan 2005; Slade and others 2007). In addition, some studies have shown that human activities that negatively affect dung beetle communities can also influence their associated functions (for example, Klein 1989; Vulinec 2002; Andresen 2003; Horgan 2005; Slade and others 2007; Barragán and others 2011).
Dung removal followed the patterns found for dung-beetle community in relation to land-use system. However, secondary forest had the same dung removal rates as agroforestry and agriculture, while presenting higher values of species richness and biomass. Agriculture and agroforestry had a greater abundance of small beetles compared to secondary forest. This is probably due to the high number of small dung beetles in these three systems, which resulted in the same dung removal rate. Therefore in agroforestry and agriculture other equally important ecological functions may not be developed to the same intensity. For example, smaller species are generally less efficient in the secondary dispersal of large seeds (Vulinec 2002). Nichols and others (2007) reported that the functional contribution of small species, even in great abundance, is too reduced in relation to the functional contribution of larger species. Larger beetles need a greater quantity of food resources and thus bury disproportionally more dung and disperse more seeds than small beetles (Andresen and Feer 2005; Nichols and others 2007).
Cascade Effect on Flies
Dung burial represents a starting point for all the other ecological functions performed by dung beetles (Halffter and Edmonds 1982; Andresen 2002; Horgan 2005; Slade and others 2007). The control of blood-sucking and detritus-feeding flies emerges as a direct consequence of dung removal (for example, Bornemissza 1960; Ridsdill-Smith 1981; Ridsdill-Smith and Hayles 1987; Bishop and others 2005; Wu and Sun 2010). Thus, evaluation of the dung removal performed by dung beetles in the different land-use systems is crucial to make inferences about the process behind the control of the fly populations.
As a general pattern we observed that the number of adult flies differed between land-use systems, presenting higher abundances in those sites with greater intensity of use (pasture and agriculture) and a lower abundance of adult flies in forested systems (primary and secondary forests, and agroforestry). The multiple model approach revealed a strong influence of dung-beetle abundance, biomass, and richness, dung removal rate, and land-use system on adult dung-fly abundance. Despite this, we did not observe a direct relationship between adult flies and the reduction in dung removal rate, not even between adult flies and the decrease in richness, abundance, and biomass of dung beetles. Agriculture, for example, had the same abundance of adult flies as pasture, but presented higher values of dung removal rates, species richness, abundance, and biomass. Similar results were found in primary forest that supported the highest diversity of dung beetles and dung removal rates, but presented the same abundance of adult flies as secondary forest and agroforestry. These results indicate that factors other than those presented in our work on dung-beetle communities are probably influencing the control of flies, for example, differences in the species composition of dung-beetle communities, interaction with other organisms and influences of different land-use systems (Axtell 1963; Bishop and others 2005; Horgan 2005; Nichols and others 2008; Wu and Sun 2010). The influence of different land systems on adult flies was shown in our work on AICc, as it was present in all of the top-ranked models, which shows that this variable is important in determining populations of flies. Different land-use systems present particular microclimatic features, such as temperature, solar radiation and humidity, and these abiotic factors interfere with the behavior and physiology of insects (Lobo and others 1998; Chown 2001), which may also impact fly abundance.
Unlike the adults, fly larvae did not differ between the land-use systems. This result shows that the biotic potential to produce new flies exists in all systems, but in forested systems this potential is not converted into new adults. This could be observed through adult fly data, because forested systems presented a smaller number of adult flies and those sites with greater intensity of use (pasture and agriculture) had a higher abundance. Horgan (2005) evaluating the emergence of adult flies from dung pads in the presence and the absence of dung beetles reported that the number and total biomass of emerging flies were constant in the absence of dung beetles, but declined where beetles were present.
Implications for the Local People
The research sites of this study are located on an Amazon reserve for indigenous people. Some scavenging flies are vectors of many animal (Byford and others 1992; Miller 1954) and human diseases (Miller and others 1961). Greater abundance of flies was found in areas where local people are present most of the time, performing extractivism, land cultivation, and animal husbandry. The increased presence of adult flies in these sites can produce both economic and public health problems (IBGE 2010). In addition to this increased vector presence, many people living in the Amazon lack basic public sanitation services, increasing the problem of fly transmission of parasite cysts and eggs. The presence of dung beetles can suppress helminth eggs and protozoan cysts and works as an important ecosystem service in poor isolated areas of the Amazon (Miller and others 1961).
Dung beetle richness, abundance, and biomass interact in the effect on dung removal rates and indirectly support the control of flies. Our results show that it is not only dung beetles that are responsible for control of flies but other factors must be influencing the population of these detritus-feeding flies, such as factors related to the intensification of land-use systems. Because dung removal is associated directly with other dung-beetle functions, such as bioturbation, secondary seed dispersal and parasite control (Amézquita and Favila 2010), all these functions can be changed by the over-simplification of habitat. Therefore, these parameters should be taken into account for maintaining the functionality provided by dung beetles in natural and disturbed systems.
We thank FAPEMIG and the project Conservation and Sustainable Management of Below-Ground Biodiversity (CSM-BGBD), coordinated by the Tropical Soil Biology and Fertility Institute of CIAT (TSBF-CIAT) with funding from the Global Environmental Facility (GEF) and implemented by the United Nations Environmental Program (UNEP), which is coordinated in Brazil by Dr. F. S. M. Moreira, Universidade Federal de Lavras (UFLA). RFB thanks CAPES for the scholarship granted (process 5081-11-4). VK thanks CNPq for the scholarship granted (process 140366/2007-5).