The role of natural vegetation strips in sugarcane monocultures: Ant and bird functional diversity responses

Agriculture, Ecosystems and Environment 284 (2019) 106603

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The role of natural vegetation strips in sugarcane monocultures: Ant and bird functional diversity responses Leonardo Fabio Rivera-Pedrozaa, Federico Escobarb, Stacy M. Philpottc, Inge Armbrechta,

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a

Biology Department, Universidad del Valle- Meléndez, Calle 13 No 100-00. Cali, Ed. 320, Of. 3027, Colombia Instituto de Ecología, A.C., Carretera antigua a Coapetec 351, El Haya, Xalapa, C.P. 91070, Veracruz, Mexico c Environmental Studies Department, University of California, 1156 High Street, Santa Cruz, California, 95064, USA b

A R T I C LE I N FO

A B S T R A C T

Keywords: Associated biodiversity Conservation biological control Functional groups Landscape homogenization Tropical dry forest

Simplification of landscapes due to the increase of monocultures negatively impacts biodiversity and its functions. In tropical landscapes that are dominated by sugarcane monocultures, some small natural vegetation patches still exist, yet little is known about their capacity to harbor functional biodiversity that may complement agroecological management of the crop. We compared ant and bird diversity in natural vegetation strips to diversity within sugarcane monocultures at increasing distances from the vegetation strips. We also compared functional groups of ants and birds in order to evaluate the role of vegetation strips in regulating pests of economic importance. During two seasons between 2015 and 2016, we studied 12 sites in the Cauca Valley, Colombia, with both natural vegetation strips and sugarcane monoculture and then sampled ants and birds in natural vegetation strips and at four distances towards the interior of the sugarcane matrix (up to 150 m and 350 m respectively). Species richness of ants and birds differed in vegetation strips and sugarcane matrix with decreases in richness as the distance from vegetation strips increased. Furthermore, predatory functional groups of ants and birds were less abundant in the sugarcane matrix, with important implications for key predation services on key sugarcane pests (e.g., Diatraea spp. – Lepidoptera: crambidae). Our results provide evidence that even in highly modified landscapes dominated by monocultures, the conservation of small patches of natural vegetation favors functional biodiversity. Therefore, maintaining and promoting and natural vegetation strips is especially important in highly industrialized monoculture landscapes in order to promote beneficial biodiversity for ecosystem services without sacrificing production area.

1. Introduction Agricultural expansion and intensification are considered the main causes of ecosystem homogenization and global biodiversity loss (Millennium Assessment, 2007). This is worrisome, among other reasons, because biodiversity maintains the life support systems necessary for human existence on Earth (Chapin et al., 2000; Foley et al., 2005). Nonetheless, the increase of arable land for food and the energy demand for plant-based biofuels is augmenting the need for agricultural land worldwide (Christofoletti et al., 2017). In the tropics, some crop areas will be expanded to meet energy demand as well as demands for other supplies (i.e., sugarcane, African palm and soy); most of these crops already occupy large tracts of fertile land, and are intensively managed in monocultures that require use of heavy machinery and high agrochemical application.

At the landscape scale, agricultural expansion generates patches of natural habitat immersed in a matrix dominated by one or few crops (Inclán et al., 2016). The resulting natural vegetation remnant patches become reservoirs for biodiversity (Fahrig et al., 2011) and are fundamental for the maintenance of key ecosystem services such as pest control, microclimate regulation, and water and soil protection within agricultural landscapes (Millennium Assessment, 2007). In addition, loss of remnant vegetation generates greater homogeneity in the landscape and, in turn, can directly influence the top-down effects of predators, affecting trophic networks (Philpott et al., 2008, 2009). In contrast, maintenance of natural vegetation in agricultural landscapes contributes to increased productivity, sustainability, and resilience (Pacheco et al., 2013). In the future, appropriately designed landscapes promise to be an economically sustainable and viable alternative, and will reduce the use of pesticides in crops (Letourneau et al., 2011;

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Corresponding author. E-mail addresses: [email protected] (L.F. Rivera-Pedroza), [email protected] (F. Escobar), [email protected] (S.M. Philpott), [email protected] (I. Armbrecht). https://doi.org/10.1016/j.agee.2019.106603 Received 31 December 2018; Received in revised form 6 May 2019; Accepted 12 July 2019 Available online 05 August 2019 0167-8809/ © 2019 Elsevier B.V. All rights reserved.

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2. Methods

Shields et al., 2018). Further, the presence of natural vegetation contiguous with crops can allow the existence of a variety of niches and support interactions between species, increasing the apparent functional redundancy (insurance hypothesis) for different critical processes in the ecosystem (Tscharntke et al., 2012). Patches of natural vegetation support natural enemies by supplying alternative food resources, prey or hosts, and oviposition or refuge sites (Walker, 1992), decreasing the abundance of undesirable species within the productive systems for conservation biological control (natural enemies’ hypothesis, Vandermeer, 1989; Schweiger et al., 2005; Shields et al., 2018). Differences in productivity (i.e., supply and availability of resources) between natural and agricultural habitats can promote ‘spillover’ or flow of nutrients or organisms along a productivity gradient (Polis et al., 1997). Spillover processes explain how degraded habitats can maintain metapopulations dynamics of some species (e.g., predators and parasites) due to their functional connection with adjacent habitat patches rich in species (Tscharntke et al., 2005; Rand et al., 2006). Notably, spillover has been studied to examine how it might contribute to biological control of insect pests of economic importance (Landis et al., 2000). Some studies have highlighted the important role that spatters or predator incursions can play in determining persistence within patched dams (Schneider, 2001). However, a bidirectional spillover of organisms of any trophic level may occur from managed to natural habitats (Tscharntke et al., 2005; Blitzer et al., 2012; Frost et al., 2015). Increases in plant complexity (weeds and usable substrates for nesting and foraging) is positively associated with greater diversity of predatory species such as ants (Philpott et al., 2008; Offenberg, 2015) and birds (Kirk et al., 1996; Perfecto et al., 2004; Dietsch et al., 2007), two taxa of great functional importance in agroecosystems such as shade coffee and other cash crops. In this sense ants are actively promoted for pest control (Perfecto and Castiñeiras, 1998), with a greater effect in crops with high plant complexity (Philpott et al., 2008). Similarly, for birds, arboreal vegetation in agricultural landscapes not only provides suitable habitat for bird species that exert important control of insect herbivorous pests, but it also sustains flocks of both migratory and local species (Wunderle and Latta, 1996; Greenberg et al., 1997). In megadiverse tropical countries, such as Colombia (Terborgh and Winter, 1983), the industrial cultivation of sugarcane occupies a large area of what was once tropical dry forest – considered to be the most threatened of the large tropical ecosystems (Janzen, 1988; Banda-R et al., 2016). Extensive monocultures, such as sugarcane, do not provide sufficient food, shelter or breeding places for species that can act as natural enemies (Rabb et al., 1976), but a possible spillover of a diversity of predatory species from remnant vegetation patches into sugarcane-dominated landscapes has not been evaluated. An understanding of the relationships between agricultural intensification, biodiversity, and natural enemies of pests is essential for improving biological control and other ecosystem services in agricultural landscapes (Crowder and Jabbour, 2014). The practical implications of such studies range from biological conservation to possible management recommendations with important economic impacts for the sugarcane industry. In this study, we evaluated the diversity of ants and birds present in natural vegetation strips, determined their capacity as reservoirs of biodiversity and their contribution in functional groups both in natural vegetation and in the cultivated matrix, and discuss the implications for conservation and the regulation of pest species, a key ecological processes in agricultural landscapes dominated by sugarcane. Specifically, we ask the following questions: (1) Is the diversity of birds and ants in the natural vegetation strips different from that of the sugarcane matrix?, (2) How does the diversity and composition of ants and birds vary as the distance from the natural vegetation strip to the matrix increases?, and (3) How does species richness of functional groups of ants and birds change from vegetation strip to agricultural matrix?

2.1. Study area We conducted this study in the flat area of the geographic valley of the Cauca River (Department of Valle del Cauca), in southwestern Colombia, where more than 70% of the land area is dedicated to sugarcane monoculture. According to Holdridge (1967), the vegetation type corresponds to tropical dry forest of which only 1% is conserved in small, highly isolated forest fragments (Arcila-Cardona et al., 2012; Alvarado-Solano and Otero Ospina, 2015). The elevation varies between 900 and 1200 m a.s.l., the average annual temperature is greater than 24 °C, and the precipitation fluctuates between 1000 and 2000 mm annually (Arcila-Cardona et al., 2012). The rainfall distribution regime is bimodal, with two dry seasons (January-February and July-August) and two rainy seasons (April-May and October-November) (Cenicaña, 2016). 2.2. Study design We selected 12 sites each containing narrow, irregularly shaped natural vegetation strips accompanied by small bodies of running water (e.g., irrigation canals, small rivers, streams, or ditches) embedded within sugarcane monocultures. The vegetation strips selected were largely representative of the types of vegetation strips present in the landscape and consisted of natural or native riparian vegetation with arboreal, shrub, and herbaceous strata, between 5 and 280 m wide (details in supplementary material, Table S1). Vegetation composition in the strips is the result of remnants of original forests, of secondary successions or reforestation. We sampled ants and birds within the vegetation strips and towards the interior of the sugarcane crop (herein, referred to as the matrix) (Fig. 1). Sampling for each taxonomic group consisted of a pitfall trap for ants or observation point for birds, by site and by season. We sampled in two seasons: February-April 2015 (50–200 mm of rain and 22–25 °C) and November 2015-February of 2016 (< 50-100 mm, 24–25 °C). Both seasons had abnormal (dry) rain regimes due to the El Niño event of 2015 (Cenicaña, 2016). 2.2.1. Ant sampling At each site, we established four ant sampling transects, separated by a minimum of 100 m, along a spatial gradient from the vegetation strip towards the center of the sugarcane monoculture field. Along each transect we placed one pitfall trap (9 cm diameter plastic cup with soap solution, ± 2 g powder soap/150 ml water) at each of five locations: at the interior (center) of the vegetation strip, at the edge of the vegetation strip (0 m) and 8 m, 45 m, and 150 m away from the vegetation strip for a total of five pitfall traps per transect and 20 pitfall traps per site (Fig. 1). We emptied traps once after 24 h. We stored collected specimens in 96% ethyl alcohol and later identified them to genus (with Fernández, 2003) and to species or morphospecies (with virtual keys from AntWeb; Ants of Bolton World Catalog; and Antwiki: Category: Neotropical species identification keys -http://www.antwiki.org/wiki/ Category:Neotropical_species_identification_keys, www.evergreen.edu/ ants). The reference collection was deposited in the Entomology Museum of the Universidad del Valle (MUSENUV), Colombia (Deposit No. 01 2016, March 3, 2016, allowed by the collection permit Resol_0120_240815 of the Ministry of Environment and Sustainable Development of Colombia-Ministerio de Ambiente y Desarrollo Sostenible de Colombia). 2.2.2. Bird sampling At each site, we established three bird sampling transects, separated by a minimum of 100 m, along a spatial gradient from the vegetation strip towards the center of the sugarcane monoculture field. Along each transect we established one fixed-radius point count location at each of 2

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Fig. 1. Maps showing (a) the location of the 12 sampling sites selected within the Cauca River Valley, Colombia and (b) the sampling design used for ants and birds. There were four sample locations for birds and four for ants in each site, although the figure just shows one. Solid black points correspond to the pitfall trap locations for ants; white points correspond to the fixed point-count locations and the circumferences at the observation radius (50 m) for birds. Numbers show distance (m) away from the edge of the vegetation strip.

five locations: at the edge of the vegetation strip (0 m) and 50 m, 150 m, 250 m, and 350 m away from the vegetation strip towards the center of the sugarcane field for a total of five point count locations per transect and 15 point count locations per site (Fig. 1). Every sampling point was visited once per sampling period, and observations for 10 min/two people per distance were facilitated with 8 × 42 binoculars. Bird calls were also recorded (Sony ICD-UX543 F recorder) and photographs of some specimens were taken (Nikon COOLPIX P600 camera). We included flying individuals if they performed some activity at the point-

count location. The distance from the observer to each individual was corroborated by a laser rangefinder (Nikon Aculon AL11 # 8397). The survey started at approximately 0600 h ( ± 15 min.) and lasted for 3 h. We identified birds using bird guides from Hilty and Brown (2001); Hilty (2002) and McMullan et al. (2014). The taxonomy was updated with the classification of bird species for South America (www. checklist.aou.org). We identified some birds from songs using the xeno-canto platform (www.xeno-canto.org) and by consultation with local experts. 3

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Fig. 2. Plots with GLMM means for (a) ants (n = 400) and (b) birds (n = 355) using richness per SU per distance; points indicate means and error bars indicate extreme values (means ± 3 ED). For (a) and (b) different letters indicate statistical differences between distances (ants: F 4,395 = 13.99, P < 0.0001) (birds: F 4,350 = 291.25, P < 0.0001); α = 0.05.

analysis; that is, we pooled all data for pitfall traps and point counts for specific distances at a given site (e.g., 0 m, 8 m, 350 m) rather than including transect as a random factor both to increase the likelihood of sampling completeness at a distance, and because of a potential lack of independence among traps or point counts at a site. We used Poisson or negative-binomial distributions for cases where overdispersion was detected. Then we selected best models based on the penalized Akaike (AIC) and Bayesian likelihood criteria (BIC). The models included multiple comparison tests with the Bonferroni correction. To detect differences between distances, the same procedure was performed with the number of guilds and the richness per SU of each functional group in ants and birds. We used Jaccard index between pairs of distances to determine similarity in species composition. All analyses were carried out using the R package (V. 3.1.3, R Development Core Team, 2015).

2.3. Groupings We grouped ant and bird species first into guilds and then functional groups (Silvestre et al., 2003), by food preference and foraging stratum (i.e., guilds are nested within functional groups). Although the pitfall collection method used for ants has a bias towards the ground-dwelling species, pitfalls also collect ants from other strata because the ground is a place of convergence for the arboreal, shrub and hypogaeic strata. A guild is defined as a group of species that exploits the same kind of resources, whereas a functional group is a group of species with a similar ecological function and includes several guilds (Silvestre et al., 2003). Each functional group was formed using guilds: 19 for ants following the proposal of Brandão et al. (2012) and 26 for birds following Martínez-Morales (2005) (Supplementary Material, Table S2). 2.3.1. Food preference The following functional groups were defined with the ant species: predators (large epigaeic species, mainly hunters), generalists (broadspectrum diet), and specialists (ground and leaf litter hunters, with specializations in their morphology and biology). The birds were grouped into the following functional groups: mainly insectivores (insects/arthropods as the main source of food), secondary insectivores (insects/arthropods as an optional food) and raptors.

3. Results In total, we collected 21,330 individual ants, grouped into seven subfamilies, 48 genera, and 121 species (recognizable taxonomic units). For birds, we recorded 1804 individuals grouped into 32 families, 84 genera and 98 species (Supplementary material, Table S3). 3.1. Is the diversity of the natural vegetation strips different from that of the sugarcane matrix?

2.3.2. Foraging stratum Ant functional groups included those that forage on the ground and in the litter (including dry twigs), on vegetation (present in arboreal, shrub or herbaceous vegetation) and in the hypogaeic stratum (underground species, some grow fungi or raise coccids). Bird functional groups include those that forage on the ground, in the herbaceous stratum (low vegetation, especially herbaceous) and in the arboreal stratum (trees and shrubs). The information used to form each grouping came from field observations and secondary information (e.g., Hilty and Brown, 2001; Hilty, 2002; Fernández, 2003; Silvestre et al., 2003; McMullan et al., 2014).

We found lower species richness (0D) of ants and birds in the sugarcane matrix compared with the natural vegetation strips (Fig. 2, Table 1). In general, the change was more evident in birds than in ants (Fig. 2). In the vegetation strips (including the edge), we collected 102 Table 1 Observed species richness values (species number), frequency/abundance (F/A) and number of guilds that make up the functional groups in the vegetation strips and the four distances towards the interior of the sugarcane matrix. The values of P (significance values in bold) are shown for the comparison between the natural vegetation strip and each distance according to the diversity order 0 D; α = 0.05. Ĉn = Completeness.

2.4. Data analyses

Distance

We used the sample coverage estimator (Ĉn) proposed by Chao and Jost (2012) to evaluate the completeness of inventory. To calculate this estimator, we grouped distances into two land uses: natural vegetation strips (including edges when considering ants) and cultivated matrix (8 m, 45 m and 150 m for ants and 50 m, 150 m, 250 m and 350 m for birds). Additionally, we calculate the completeness in each distance for both ants and birds. We fit generalized linear mixed models (GLMM) to evaluate the effect of distance (fixed effect), with site considered as a random effect, both to evaluate species richness (0D= species number), and to evaluate the effect of distance on the associations and functional groups. Samples from a single distance from a single site were pooled for the 4

Richness

F/A

No. guilds

Ants Strip Edge 8m 45 m 150 m

80 86 64 59 59

522 628 455 412 377

Birds Strip 50 m 150 m 250 m 350 m

92 37 30 27 24

1004 264 267 163 106

0

D

Cn

16 18 15 14 15

0 0.8103 a 0.0609 a 0.0017 b 0.0004 c

0,75 0,89 0,76 0,80 0,81

26 18 16 17 14

0 0.0200 0.0001 0.0001 0.0001

0,83 0,74 0,81 0,85 0,51

a b b b

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3.3. How does species richness of functional groups of ants and birds change from vegetation strip to agricultural matrix? We found significant differences in the number of guilds that formed each functional group, both for ants (F4, 395 = 23.02, p < 0.0001) and for birds (F4, 350 = 31.99, p < 0.0001), with the difference being more drastic as the distance from the natural vegetation strip (350 m) increased (Table 1). 3.3.1. Functional groups 3.3.1.1. Food preference. We observed differences in the species grouped by foraging stratum between the different distances for ants. Species richness tended to decrease with increasing distance from the vegetation strip, except for the generalist ants, which had greater species richness within the matrix than in the natural vegetation strips (Fig. 4). 3.3.1.2. Foraging stratum. We observed differences between distances based on foraging stratum for both ants and for birds. Species richness, in general, decreased towards the interior of the sugarcane matrix; however, bird species belonging to the herbaceous vegetation stratum were similar between the crop and natural vegetation strips (Fig. 5). 4. Discussion We examined the role of vegetation strips as a refuge for species diversity of ants and birds in a landscape highly dominated by the cultivation of sugarcane across two seasons of one year. We also addressed how the diversity of species and guilds changes as the distance to the vegetation remnants increases from the vegetation strips towards the cultivated matrix. Based on these results, we sought to determine if the fauna that enters sugarcane crops could provide ecosystem functions, considering their guilds and functional groups. We found that the species richness represents approximately 60% of the myrmecofauna and 70% of the avifauna for dry forest historically reported in the study area (Valle del Cauca: Chacón de Ulloa et al., 2012 and Álvarez-López, 1999, respectively), indicating that these natural vegetation strips associated with sugarcane crops, although narrow and isolated, have a high conservation value given that the original forests have been practically extirpated. This result is surprising considering that the strips studied are highly degraded, and also experience chronic disturbance due to the management of the sugarcane crop. In addition, the results are of value since there are few studies carried out on relicts of riparian vegetation, which, in the absence of large areas of tropical dry forest, are small "oases" for the relict fauna. The evidence suggests that certain species inhabiting the tropical dry forest have been able to survive with minimal habitat, although the extent of extinctions of forest species that occurred with the massive felling of forests several decades ago is not known. Although sampled during an abnormally dry year, we consider the data to be robust and important. We did not intend to examine how seasonal changes affect the differences in species richness and functional groups in vegetation strips and inside the sugarcane matrix explicitly, but chose to sample during two seasons, with standard sampling techniques to have a more complete data set. It may be that the differences between vegetation strips and the sugarcane matrix are exacerbated during dry periods, when more species retreat or seek refuge in natural vegetation with presumably more moisture and more resources. At the same time, it is evident that collecting during an abnormally dry year is indicative of actual conditions that remnant vegetation and associated species will experience under climate change. Tropical dry forests will increasingly experience “el Niño” and “la Niña” phenomena with climate change (Salisbury, 2018) with important implications for biodiversity in remnant habitats. Thus, if retaining this remnant vegetation may become even more important during dry times for maintaining biodiversity and for functionally important species and

Fig. 3. Comparisons of the compositional similarity of ants and birds between vegetation strips and distances into sugarcane monoculture fields. Similarity (shown in open circles) was calculated with the Jaccard Index and presence/ absence data α = 0.05. The number of species exclusive to vegetation strips is shown in black, exclusive to each distance shown in light grey, and species shared between vegetation strips and points at increasing distances inside sugarcane fields shown in dark grey.

species of ants (35 exclusive), and the completeness of the inventory was 75%, whereas the matrix cultivated with sugarcane supported 84 species of ants (19 exclusive), with a completeness greater than 90%. For birds, we found 89 species (48 exclusive) in the vegetation strips, with an estimated completeness of 81%; but we found 51 species (nine exclusive), with a 95% completeness, in the matrix (Fig. 3, Table S3). The majority of species found inside the sugarcane monocultures were species shared with vegetation strips, and similarity between species found in vegetation strips and those found in the sugarcane declined precipitously for both ants and birds (Fig. 3). 3.2. How does the species richness and composition of ants and birds vary as the distance from the strip to the matrix increases? The GLMM comparing species richness between distances showed statistical differences between the vegetation strips (including the edge) and the matrix. Both ant and bird richness decreased significantly as the distance to the vegetation strip increased. For ants, significant differences were found in the species richness (0D) between the strip and all the distances to the interior of the crop (χ2 85 = 53.177, P < 0.0001), except that no differences were detected in the species richness (0D) between strip-edge and strip-8 m. For birds, statistically significant differences were found between the strip and all distances within the sugarcane matrix (χ2 90 = 32.868, P < 0.0001) (Table 1). 5

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Fig. 4. Change in the richness of functional groups according to food preference for (a) ants [most abundant species of each group, from left to right: Pachycondyla ferruginea, Solenopsis geminata, Pyramica sp. (photos: Alex Wild)] y (b) birds [species from left to right: Tyrannus melancholicus, Zonotrichia capensis, Falco sparverius (photos: Leonardo Rivera)], with increasing distance to the natural vegetation strip, according to GLMM using richness per SU per distance; distances are expressed in meters. Different letters indicate statistical differences for ants: predators: (F 4,395 = 16.11, p < 0.0001), generalists: (F 4,395 = 7.36, p < 0.0001), specialists: (F 4,395 = 23.02, p < 0.0001); and for birds mainly insectivores: (F 4,350 = 31.81, p < 0.0001), secondary insectivores: (F 4,350 = 11.9, < 0.0001), raptors: (F 4,350 = 1.28, p = 0.0138); (α = 0.05).

important groups is imperative due to the importance of maintaining a mosaic landscape with different types of arboreal vegetation that guarantees the persistence of the populations (Devictor and Jiguet, 2007; Firbank et al., 2008; Fahrig et al., 2011). In actuality, small and isolated patches of native vegetation are being evaluated as being critically important to rescuing rare biodiversity, restoring ecosystems, providing stepping stones for mobile wildlife, purifying water, filtering out pollutants, reducing silt, lowering soil erosion, and providing valuable opportunities for recreation and nature education (Lindenmayer, 2019; Wintle et al., 2019).

groups.

4.1. Differences in diversity between natural vegetation and cultivated matrix The results confirm the existence of two sets of species in the landscape: those that live in natural vegetation (strips) and those of the cultivated matrix (monoculture of sugarcane), corroborated by the number of species shared between the natural vegetation strips and each of the distances (Figs. 2 and 3, Table S3). The results suggest that a high percentage of species (43% of ants and 73% of birds) come from the strips of natural vegetation, this percentage comes from comparing the diversity of the greatest distance within the matrix with the diversity present in the strips (150 m in ants and 350 in birds). In addition, the cultivated matrix prevents passage for an important fraction of the ant (30%) and bird (49%) fauna that are exclusive to the natural vegetation; an effect that was stronger for birds than for ants (Figs. 2a and b). In addition, a percentage of non-exclusive species (45% ants and 58% birds) move between the two land uses, and these species tend to depend more on natural cover than on cultivated land (Tscharntke et al., 2005; Santos et al., 2018). This implies that an appreciable percentage of ants and birds are restricted to the remnants of natural vegetation, whose habitat is more stable than that of the matrix. The matrix suffers repeated disturbances in the sowing events (tilling, ploughing) and harvesting (the sugarcane is usually burned before harvesting), which limits the establishment of permanent populations. Thus, understanding impacts on biodiversity and functionally

4.2. Spillover of species on the cultivated matrix? The general decrease in the species richness of ants and birds with the increase in distance to the remnants of natural vegetation, suggests a decrease in species spillover towards sugarcane crops (Table 1, Fig. 2). Therefore, our results suggest this spillover is very limited and restricted to areas near the vegetation strip. Although the results apparently show two sets of species in the landscape: those that live in natural vegetation and those of the cultivated matrix, there are more species shared closer to the vegetation strip, and we interpret this result as increased movement from the strip to the matrix at close distances. Due to their flying ability, a greater spillover towards the cultivated matrix was expected for birds than for ants. However, in this landscape with few remnants of arboreal vegetation, the birds were more affected since most of the species seem to be more associated with natural vegetation and therefore vulnerable to landscape homogenization. 6

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Fig. 5. Change in the richness of functional groups with the increase in distance to the natural vegetation strip, according to foraging stratum for (a) ants [representative species for each group, from left to right: Ectatomma ruidum, Pseudomyrmex gracilis, Acropyga goeldii (photos: Alex Wild)], (b) birds [species from left to right: Sicalis flaveola, Sporophila schistacea, Thraupis episcopus (photos: Leonardo Rivera)], in terms of GLMM averages using richness per SU per distance; distances are expressed in meters; Different letters indicate statistical differences for ants: ground and leaf litter (F 4,395 = 4.87, p = 0.0008), vegetation (F 4,395 = 30.95, p = 0.0124), hypogaeic (F 4,395 = 6.12, p < 0.0001); and for birds of ground: (F 4,350 = 14.78, p < 0.0001), herbaceous: (F 4,350 = 3.24, p = 0.0124), arboreal: (F 4,350 = 65.99, p < 0.0001); (α = 0.05).

species, such as generalist ants and birds that forage in herbaceous vegetation, can survive and adapt to the matrix.

Possibly, the sugarcane matrix is favorable for a portion of generalist ant species that exploit sugary substances and resources such as invertebrates that establish between the periods of each harvest (13 to 15 months) (Lang-Ovalle et al., 2011). Tscharntke et al. (2005) suggest that the distance to the natural vegetation and the amount of habitat (remnant size) are factors that affect the diversity of each ecosystem at a smaller or more local scale. However, changes in species richness and composition are not always influenced by the landscape context (Firbank et al., 2008), so the presence or absence of certain species in the matrix could also be related to the behavior of the species itself or to the scale at which some organisms perceive change (Schweiger et al., 2005; Jackson and Fahrig, 2012). In addition, it has been noted that the transboundary side effects of mobile antagonists, as competitors and natural enemies, come from the habitats of the surrounding matrix can exert strong negative effects on resident species within the remaining natural habitats (Blitzer et al., 2012). Therefore, we interpret the differential response of both taxonomic groups as being mainly due to the differential capacity that some species have for taking advantage of the resources provided by the matrix and their capacity for adapting to their conditions.

4.3.1. Principal food items 4.3.1.1. Ants. The predatory group composed of large species such as the “poneromorph” ants (except Hypoponera spp.) and army ants decreased as the distance to the natural vegetation strips increased (Fig. 4a, Tables S2 and S3). In particular, the genus Pachycondyla (Formicidae: ponerinae), mainly predatory large scavenging ants, decreased by 66% at the distances farthest from the natural vegetation (45 and 150 m), whereas at closer distances, it only decreased by 33% (8 m) (Tables S2 and S3). This result is consistent with studies that show that hunting ants are sensitive to the presence or absence of natural vegetation (Sanabria-Blandón and Chacón de Ulloa, 2011; Rivera et al., 2013), a phenomenon possibly associated with the decrease in nesting substrates in the soil of the matrix (i.e., ground, litter and fallen trunks) (Lattke, 2003). Because the loss of hunters can affect the ecosystem services of biodiversity in the matrix by eliminating effective predators, having natural vegetation strips every 100 m would be beneficial for the farmers. Similarly, leaf litter ant species decreased towards the interior of the matrix, as did the predators. Leaf litter ants depend on the cover of litter and dry twigs that they use for nesting and foraging, for which they have specialized morphology and biology (Fernández, 2003; Brandão et al., 2012) and that prevents them from adapting to unnatural conditions (i.e., industrialized sugarcane). The generalist species, unlike the predators and specialists, tended to increase with distance from the vegetation

4.3. Effect of the matrix on functional diversity In agreement with what was found for the diversity of species, a more drastic response was evident in the functional groups of birds than in those of ants in terms of the change from natural vegetation strip towards the matrix (Figs. 4 and 5). This result corroborates that certain 7

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suitable for the establishment of seedlings (Levey and Byrne, 1993; Folgarait, 1998). Likewise, species that forage on vegetation decrease once they enter the matrix (8, 45 and 150 m), despite the high density and relative height (2.5–4 m) of the sugarcane before harvest, showing that the fauna not only needs available biomass but also plant diversity to survive and that the presence of the trees affects the flora around them.

strips (Fig. 4a, Table S2), which could be explained by the increase in their dominance in environments modified by human activity (Foucaud et al., 2009) and because of their eurytopic nature; possibly they evolved to survive in scenarios of catastrophic events in ecosystems (disturbances). For the worst pest of sugarcane, Diatraea spp., (Vargas et al., 2018), the finding of this work is of interest because a valuable potential exists in the different ant guilds to exercise biological control targeting the eggs, larvae and adults (Adams et al., 1981; Long et al., 1987; Ramírez et al., 2004; Rossi and Fowler, 2004; Souza et al., 2010; Oliveira et al., 2012), meaning that with ecologically sound designs, sugarcane landscapes can exist at a very low cost since only growth of natural vegetation around the edges of the sugarcane plots is required.

4.3.2.2. Birds. The results of this study show that the species of birds that forage on the ground and the shrub/arboreal strata are reduced as the distance in the matrix increases. For arboreal birds, this reduction is immediate; that is, a significant portion of species from the natural vegetation strips do not enter the crop. On the other hand, the species that seek their food in the herbaceous stratum segregated into two groups: one that prefers to be closer to the natural vegetation strips (50 m), and another one closer to the interior of the matrix (350 m) (Fig. 5b, Tables S2 and S3). It is possible that some granivorous species obtain their food from grasses, other weeds and small arthropods in the interior of the matrix, but they require vegetation strips to complement their diet and to obtain other essential resources (e.g., nesting materials or mating sites). Species of the families Cuculidae, Emberizidae, Fringillidae, Furnariidae, Thamnophilidae and Thraupidae, which are capable of exploiting resources such as seeds and small insects, belong to this group. They also tolerate the negative effects of the matrix and maintain their populations and even increase in degraded environments, with the subsequent effect on the community structure within the fragments of remaining habitat (Pearson, 1993). For tropical bird communities, the reduction in the structural complexity of habitat and the multiple loss of ecological heterogeneity caused by the intensification of agriculture are factors that affect the diversity of species in multiple temporal and spatial scales (Benton et al., 2003; Firbank et al., 2008), especially those that prefer to forage on the ground and in the shrub/arboreal stratum. The degradation of fertile soils previously occupied by dry forest and the displacement of water from the soil interior to the surface, decreases their productivity, reducing the amount of available prey that inhabit the soil (Watson, 2011). This phenomenon is aggravated by the use of agrochemicals and by the continuous modification of the soil, which is critical for the bird communities of the landscape at different strata.

4.3.1.2. Birds. The decrease in diversity in all groups of predatory birds within the sugarcane matrix is associated with a decrease in the complexity of the vegetation generated by the matrix (Fig. 4b, Table S2). In the case of secondary insectivores, different species of this group have been found preying on larvae of Lepidoptera, especially Diatraea spp. and other borer species in the corn and sugarcane crops (Black et al., 1970; Baskauf, 2003; Perfecto et al., 2004). This decrease in the matrix corresponds to a decrease in the potential to prey on pests of commercially important crops. The raptors, on the other hand, consume large arthropods and small vertebrates that circulate inside the matrix. In Guatemala, Chile, Costa Rica and Mexico, species from this group are used as biological control methods for field rats (Muñoz-Pedreros, 2004; Quintero-Romanillo et al., 2009; Sánchez-Soto, 2016). A reason why a reduction of these predatory birds can generate health problems is due to the increase in rodents and other potentially harmful species in sugarcane crops. Empirical studies have documented increased avian nest predation or parasitism near habitat edges in fragmented landscapes in agricultural habitats, providing strong empirical support to the idea that anthropogenic land-use systems may provide important subsidies to generalist predators, resulting in a greater impact on prey populations within adjacent habitats (Rand et al., 2006). In general, the predatory species of both taxonomic groups tend to be polyphagous, with specific habitat requirements, so a greater diversity of alternative prey and heterogeneous microhabitat landscapes is expected to promote them (Root, 1975). Although this study does not provide evidence that the predators actually feed inside the matrix, there is an enormous potential for biological control if they are proved so. In this scenario, the conservation of the natural vegetation strips contiguous to sugarcane crops could be a strategy for the planning of crop management.

5. Conclusions This study shows that the remnants of natural vegetation, in the form of narrow strips immersed in agricultural landscapes dominated by sugarcane, contribute to sustaining a greater diversity of species and functions than the matrix. These remnants also support a high diversity of functional groups of animals such as ants and birds, in particular of the species that can act as biological controllers or second-order consumers. This study did not directly investigate whether predator guilds actually feed in the sugarcane crop. However, since these strips maintain a high diversity of functional groups, their presence could favor the biological control of pest species such as Diatraea spp., which is effectively predated by predatory ants and birds (e.g., Black et al., 1970; Long et al., 1987; Baskauf, 2003; Oliveira et al., 2012). Therefore, planning for productive landscapes with immersed natural vegetation would allow, without sacrificing cultivation area, a more ecologically sound model favoring the conservation of vegetation remnants adjacent to the water bodies and living fences present in the landscapes for the maintenance of biodiversity and its functioning.

4.3.2. Foraging stratum 4.3.2.1. Ants. In this study, the decrease in species inside the sugarcane crops was obvious. However, the effect was more intense with greater distance from the natural vegetation (150 m), showing a negative impact on the richness generated by the matrix to different vertical strata (i.e., the species that forage on the ground and litter, those that forage on the vegetation and the ones in the hypogaeic stratum) (Fig. 5a, Table S2). Several studies have indicated that agriculture reduces the richness and composition of ground and leaf litter ant species by adding chemicals to the crops that change the structure of populations (Ishizaki et al., 2014; Schweiger et al., 2005; Christofoletti et al., 2017). In addition, the removal of litter in the monocultures and the removal of possible refuges and food sources also have impacts on the predatory ants and ground and leaf litter specialists (Armbrecht and Perfecto, 2003; Philpott et al., 2008). Likewise, the decrease in hypogaeic species within the matrix demonstrates the impact of the industrial (mechanized) management of the crop when the deepest layers of the soil are modified (Ramírez et al., 2012). Hypogaeic ants play an important role in the transformation of the physical and chemical properties of the soil and in the formation of microsites

Acknowledgements We thank Kimberly Navarro for help during field work and sampling; Carlos Santamaría, Elizabeth Jiménez, and Anderson Arenas for ant identification; Humberto Álvarez López for bird identification; Alex Wild for ant photos in the graphs; Wilmar Torres and Biology-Graduate 8

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program for statistical analyses; Armando González, Yolanda Gutiérrez, and Jorge Tafur for logistical help; thanks to the sugar processing plants Mayagüez, Manuelita, Providencia, Pichichí, La Cabaña y RiopailaCastilla; to the owners of the sugarcane crops for allowing samplings; to Cenicaña for logistical support in the field. This study was financed by the Research Vicerrectory, at Universidad del Valle, Cali, Colombia, through the scholarship “Bolsa Concursable para Fomento a la Publicación de Resultados 2017” and the “convocatoria de apoyo a estudiantes de Doctorado-2018”, project CI 71141-2017 (LFRP) – Franjas con vegetación natural dentro del paisaje cañero como estrategia para aumentar servicios ecológicos” –.

Siriwardena, G.M., Martin, J.L., 2011. Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol. Lett. 14, 101–112. Fernández, F., 2003. Introducción a las hormigas de la región Neotropical. IAvH, Bogotá, Colombia XXVI + 398 p. Firbank, L., Petit, S., Smart, S., Blain, A., Fuller, R.J., 2008. Assessing the impacts of agricultural intensification on biodiversity: a British perspective. Phil. Trans. R. Soc. B. 363, 777–787. Foucaud, J., Orivel, J., Fournier, D., Delabie, J.H.C., Loiseau, A., Le Breton, J., Cerdan, P., Estoup, A., 2009. Reproductive system, social organization, human disturbance and ecological dominance in native populations of the little fire ant, Wasmannia auropunctata. Mol. Ecol. 18, 5059–5073. Foley, J.A., DeFries, R., Asner, G.P., Barford, C., Bonan, G., Carpenter, S.R., Chapin, F.S., Coe, M.T., Daily, G.C., Gibbs, H.K., Helkowski, J.H., Holloway, T., Howard, E.A., Kucharik, C.J., Monfreda, C., Patz, J.A., Prentice, I.C., Ramankutty, N., Snyder, P.K., 2005. Global consequences of land use. Science 309, 570–574. Folgarait, P.J., 1998. Ant biodiversity and its relationship to ecosystem functioning: a review. Biodivers. Conserv. 7, 1221–1244. Frost, C.M., Didham, R.K., Rand, T.A., Peralta, G., Tylianakis, J.M., 2015. Communitylevel net spillover of natural enemies from managed to natural forest. Ecology 96, 193–202. Greenberg, R., Bichier, P., Angón, A.C., Reitsma, R., 1997. Bird populations in shade and sun coffee plantations in central Guatemala. Cons. Biol. 11, 448–459. Hilty, S.L., 2002. Birds of Venezuela. Princeton Univ. Press. Hilty, S.L., Brown, W., 2001. Guía de las aves de Colombia. Princeton University Press, American Bird Conservancy-ABC, Universidad del Valle, Sociedad Antioqueña de Ornitología-SAO, Cali, pp. 1030. Holdridge, L.R., 1967. Life Zone Ecology. Tropical Science Center, San José, Costa Rica, pp. 206. Inclán, D.J., Cerreti, P., Marini, L., 2016. Spillover of tachinids and hoverflies from different field margins. Basic Appl. Ecol. 17, 32–42. Ishizaki, J.N., Barros, N.S., Costa, M.S., Santos, M.S.M., Batistote, M., Silva, R.F., 2014. Comunidade microbiana em solo adubado com vinhaça e cultivado com milho safrinha sob plantas de cobertura. Cad. Agroecologia. 9, 1–5. Jackson, H.B., Fahrig, L., 2012. What size is a biologically relevant landscape? Landscape Ecol. 27, 929–941. Janzen, D.H., 1988. Tropical dry forests. The most endangered major tropical ecosystems. In: Wilson, E.O. (Ed.), Biodiversity. National Academy Press, Washington D.C, pp. 130–137. Kirk, D.A., Evenden, M.D., Mineau, P., 1996. Past and current attempts to evaluate the role of birds as predators of insect pests in temperate agriculture. Curr. Ornithol. 13, 175–269. Landis, D.A., Wratten, S.D., Gurr, G.M., 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 45, 175–201. Lang-Ovalle, F.P.A., Pérez, V.J.P., Martínez, D.D.E., Platas, R.L.A., Ojeda, E., Gonzáles, A., 2011. Macrofauna edáfica asociada a plantaciones de mango y caña de azúcar. Terra Latinoam. 29, 169–177. Lattke, J.E., 2003. Subfamilia Ponerinae. In: Fernández, F. (Ed.), Introducción a las hormigas de la región neotropical. Instituto de Investigación de recursos Biológicos Alexander von Humboldt, Bogotá, Colombia, pp. 261–276. Letourneau, D.K., Armbrecht, I., Rivera, B.S., Lerma, J.M., Carmona, E.J., Daza, M.C., Escobar, S., Galindo, V., Gutiérrez, C., López, S.D., Mejía, J.L., Rangel, A.M., Rangel, J.H., Rivera, L., Saavedra, C.A., Torres, A.M., Trujillo, A.R., 2011. Does plant diversity benefit agroecosystems? A synthetic review. Ecol. Appl. 21, 9–21. Levey, D.J., Byrne, M.M., 1993. Complex ant-plant interactions: rain-forest ants as secondary dispersers and post-dispersal seed predators. Ecology 74, 1802–1812. Lindenmayer, D., 2019. Small patches make critical contributions to biodiversity conservation. Proc. Natl. Acad. Sci. 116 (3), 717–719. Long, W.H., Nelson, L.D., Templet, E.J., Viator, C.E., 1987. Abundance of foraging ant predators of the sugarcane borer in relation to soil and other factors. J. Am. Soc. Sugarcane Technol. 7, 5–14. Martínez-Morales, M.A., 2005. Nested species assemblages as a tool to detect sensitivity to forest fragmentation: the case of cloud forest birds. Oikos 108, 634–642. McMullan, M., Donegan, T.M., Quevedo, A., 2014. Guía de campo de las aves de Colombia. Colombia. pp. 226. Millennium Assessment, 2007. A Toolkit for Understanding and Action. Protecting Nature`s Services. Protecting Ourselves. Island Press, Washington: DC. Muñoz-Pedreros, A., 2004. Control biológico con aves rapaces. In: Muñoz-Pedreros, A., Rau, J., Yáñez, J. (Eds.), Aves Rapaces de Chile, eds. CEA, pp. 386. Offenberg, J., 2015. Ants as tools in sustainable agriculture: the case of weaver ants and beyond. J. Appl. Ecol. 52, 1197–1205. Oliveira, R.F., Almeida, L.C., Souza, D.R., Munhae, C.B., Bueno, O.C., Morini, S.C., 2012. Ant diversity (Hymenoptera: formicidae) and predation by ants on the different stages of the sugarcane borer life cycle Diatraea saccharalis (Lepidoptera: crambidae). Eur. J. Entomol. 109, 381–387. Pacheco, R., Vasconcelos, H.L., Groc, S., Camacho, G.P., Frizzo, T.L.M., 2013. The importance of remnants of natural vegetation for maintaining ant diversity in Brazilian agricultural landscapes. Biodivers. Conserv. 22, 983–997. Pearson, S.M., 1993. The spatial extent and relative influence of landscape-level factors on wintering bird populations. Landscape Ecol. 8, 3–18. Perfecto, I., Castiñeiras, A., 1998. Deployment of the predaceous ants and their conservation in agroecosystems. In: Barbosa, P. (Ed.), Conservation Biological Control. Academic Press, San, Diego, CA, USA, pp. 269–289. Perfecto, I., Vandermeer, J.H., López-Bautista, G., Ibarra-Núñez, G., Greenberg, R., Bichier, P., Langridge, S., 2004. Greater predation in shaded coffee farms: the role of resident neotropical birds. Ecology 85, 2677–2681. Philpott, S., Perfecto, I., Vandermeer, J., 2008. Effects of predatory ants on lower trophic

Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.agee.2019.106603. References Adams, C.T., Summers, T.E., Lofgren, C.S., Focks, D.A., Prewitt, J.C., 1981. Interrelationship of ants and the sugarcane borer in Florida sugarcane fields. Environ. Entomol. 10, 415–418. Alvarado-Solano, D.P., Otero Ospina, J.T., 2015. Distribución espacial del Bosque Seco Tropical en el Valle del Cauca, Colombia. Acta Biol. Colomb. 20, 141–153. Álvarez-López, H., 1999. Guía de las aves de la Reserva Natural Laguna de Sonso. CVC, Cali, Colombia. Arcila-Cardona, A.M., Valderrama, A.C., Chacón de Ulloa, P., 2012. Estado de fragmentación del bosque seco de la cuenca alta del río Cauca, Colombia. Biot. Col. 13, 82–101. Armbrecht, I., Perfecto, I., 2003. Litter-twig dwelling ant species richness and predation potential within a forest fragment and neighboring coffee plantations of contrasting habitat quality in Mexico. Agric. Ecosyst. Environ. 97, 107–115. Banda-R, K., Delgado-Salinas, A., Dexter, K.G., Linares-Palomino, R., Oliveira-Filho, A., Prado, D., Pullan, M., Quintana, C., Riina, R., Rodriguez, M., Weintritt, J., AcevedoRodriguez, P., Adarve, J., Alvarez, E., Aranguren, B.A., Arteaga, J.C., Aymard, G., Castano, A., Ceballos-Mago, N., Cogollo, A., Cuadros, H., Delgado, F., Devia, W., Duenas, H., Fajardo, L., Fernandez, A., Fernandez, M.A., Franklin, J., Freid, E.H., Galetti, L.A., Gonto, R., Gonzalez-M, R., Graveson, R., Helmer, E.H., Idarraga, A., Lopez, R., Marcano-Vega, H., Martinez, O.G., Maturo, H.M., McDonald, M., McLaren, K., Melo, O., Mijares, F., Mogni, V., Molina, D., Moreno, Nd.P., Nassar, J.M., Neves, D.M., Oakley, L.J., Oatham, M., Olvera-Luna, A.R., Pezzini, F.F., Dominguez, O.J.R., Rios, M.E., Rivera, O., Rodriguez, N., Rojas, A., Sarkinen, T., Sanchez, R., Smith, M., Vargas, C., Villanueva, B., Pennington, R.T., 2016. Plant diversity patterns in neotropical dry forests and their conservation implications. Science 353, 1383–1387. Baskauf, S.J., 2003. Factors influencing population dynamics of the southwestern corn borer (Lepidoptera: crambidae): a reassessment. Environ. Entomol. 32, 915–928. Benton, T.G., Vickery, J.A., Wilson, J.D., 2003. Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol. Evol. 18, 182–188. Black, E.R., Davis, F.M., Henderson, C.A., Douglas, W.A., 1970. The role of birds in reducing overwintering populations of the southwestern corn borer, Diatraea grandiosella (Lepidoptera: crambidae), in Mississippi. Ann. Entomol. Soc. Am. 63, 701–706. Blitzer, E.J., Dormann, C.F., Holzschuh, A., Klein, A.M., Rand, T.A., Tscharntke, T., 2012. Spillover of functionally important organisms between managed and natural habitats. Agric. Ecosyst. Environ. 146, 34–43. Brandão, C.R.F., Silva, R., Delabie, H.C.J., 2012. Neotropical ants (hymenoptera) functional groups: nutritional and applied implications. In: Panizzi, A.R., Parra, J.R.P. (Eds.), Insect Bioecology and Nutrition for Integrated Pest Management. CRC Press, pp. 213–236. Cenicaña, 2016. Mapas meteorológicos: red meteorológica automatizada (RMA). (accessed 2 December 2016). http://www.cenicana.org/clima_/index.php. Chacón de Ulloa, P., Osorio-García, A.M., Achury, R., Bermúdez-Rivas, C., 2012. Hormigas (Hymenoptera: formicidae) del Bosque seco Tropical (Bs-T) de la cuenca alta del río Cauca, Colombia. Biot. Col. 13, 165–181. Chao, C., Jost, L., 2012. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 9, 2533–2547. Chapin, F.S., Zavaleta, E.S., Eviner, V.T., Naylor, R.L., Vitousek, P.M., Reynolds, H.L., Hooper, D.U., Lavorel, S., Sala, O.E., Hobbie, S.E., Mack, M.C., Díaz, S., 2000. Consequences of changing biodiversity. Nature 405, 234–242. Christofoletti, C.A., Pereira de Souza, C., Guedes, T., Ansoar-Rodríguez, Y., 2017. O emprego de agrotóxicos na cultura da cana-deaçúcar. In: Fontanetti, C.S., Bueno, O.C. (Eds.), Cana-de-açúcar e seus impactos: uma visão acadêmica. Canal 6, pp. 51–62. Crowder, D.W., Jabbour, R., 2014. Relationships between biodiversity and biological control in agroecosystems: current status and future challenges. Biol. Control 75, 8–17. Devictor, V., Jiguet, F., 2007. Community richness and stability in agricultural landscapes: the importance of surrounding habitats. Agric. Ecosyst. Environ. 120, 179–184. Dietsch, T.V., Perfecto, I., Greenberg, R., 2007. Avian foraging behavior in two different types of coffee agroecosystem in Chiapas, Mexico. Biotropica 39, 232–240. Fahrig, L., Baudry, J., Brotons, L., Burel, F.G., Crist, T.O., Fuller, R.J., Sirami, C.,

9

Agriculture, Ecosystems and Environment 284 (2019) 106603

L.F. Rivera-Pedroza, et al.

abundance, diversity and species composition of predatory ants in sugarcane fields. Basic Appl. Ecol. https://doi.org/10.1016/j.baae.2018.08.009. Schweiger, O., Maelfait, J.P., Van Wingerden, W., Hendrickx, F., Billeter, R., Speelmans, M., Augenstein, I., Aukema, B., Aviron, S., Bailey, D., Bukacek, R., Diekötter, T., Dirksen, J., Frenzel, M., Herzog, F., Liira, J., Roubalova, M., Bugter, R., 2005. Quantifying the impact of environmental factors on arthropod communities in agricultural landscapes across organizational levels and spatial scales. J. Appl. Ecol. 42, 1129–1139. Shields, M.W., Johnson, A.C., Pandey, S., Cullen, R., González, M., Steve, C., Wratten, D., Gurr, G.M., 2018. History, current situation and challenges for conservation biological control. Biol. Contr. Control. Schneider, M.F., 2001. Habitat loss, fragmentation and predator impact: spatial implications for prey conservation. J. Appl. Ecol. 38, 720–735. Silvestre, C.R., Brandäo, F., Rosa Da Silva, R., 2003. Grupos funcionales de hormigas: el caso de los gremios del Cerrado. In: Fernández, F. (Ed.), 2003. Introducción a las hormigas de la región neotropical. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá, Colombia, pp. 113–148 XXVI + 398 p. Souza, D.R., Stingel, E., Almeida, L.C., Munhae, C.B., Mayhé-Nunes, A.J., Bueno, O.C., Morini, M.S., 2010. Ant diversity in a sugarcane culture without the use of straw burning in southeast, São Paulo, Brazil. Am. J. Agri. Biol. Sci. 5, 183–188. Terborgh, J., Winter, B., 1983. A method for sitting parks and reserves with special reference to Colombia and Ecuador. Biol. Cons. 27, 45–58. Tscharntke, T., Klein, A.M., Kruess, A., Steffan-Dewenter, I., Thies, C., 2005. Landscape perspectives on agricultural intensification and biodiversity - ecosystem service management. Ecol. Lett. 8, 857–874. Tscharntke, T., Tylianakis, J.M., Rand, T.A., Didham, R.K., Fahrig, L., Batáry, P., Bengtsson, J., Clough, Y., Crist, T.O., Dormann, C.F., Ewers, R.M., Fründ, J., Holt, R.D., Holzschuh, A., Klein, A.M., Kleijn, D., Kremen, C., Landis, D.A., Laurance, W., Lindenmayer, D., Scherber, C., Sodhi, N., Stefan-Dewenter, I., Thies, C., van der Putten, W.H., Westphal, C., 2012. Landscape moderation of biodiversity patterns and processes - eight hypotheses. Biol. Rev. 87, 661–685. Vandermeer, J., 1989. The Ecology of Intercropping. Cambridge University Press, Cambridge, UK 24p. Vargas, A.G., Gómez, L.A., Michaud, J.P., 2018. Sugarcane stem borers of the Colombian Cauca River Valley: current pest status, biology, and control. Fla. Entomol. 98, 728. Walker, B.H., 1992. Biodiversity and ecological redundancy. Cons. Biol. 6, 18–23. Watson, D.M., 2011. A productivity-based explanation for woodland bird declines: poorer soils yield less food. Emu. Austral Ornithol. 111, 10–18. Wintle, B.A., Kujala, H., Whitehead, A., Cameron, A., Veloz, S., Kukkala, A., Moilanen, A., Gordon, A., Lentini, P.E., Cadenhead, N.C.R., Bekessey, S.A., 2019. Global synthesis of conservation studies reveals the importance of small habitat patches for biodiversity. Proc. Natl. Acad. Sci. 116 (3), 909–914. Wunderle, J.M.Jr., Latta, S.C., 1996. Avian abundance in sun and shade coffee plantations and remnant pine forest in the Cordillera Central, Dominican Republic. Ornithol. Neotrop. 7, 19–34.

levels across a gradient of coffee management complexity. J. Anim. Ecol. 77, 505–511. Philpott, S., Soong, O., Lowenstein, J.H., Pulido, A.L., Lopez, D.T., Flynn, D.F.B., DeClerck, F., 2009. Functional richness and ecosystem services: bird predation on arthropods in tropical agroecosystems. Ecol. Appl. 19, 1858–1867. Polis, G.A., Anderson, W.B., Holt, R.D., 1997. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu. Rev. Ecol. Syst. 28, 289–316. Quintero-Romanillo, A.L., Barreras-Fitch, R.C., Orozco-Gerardo, J.A., Rangel-Cota, G., 2009. Determinación de especies de aves rapaces, en el área de abastecimiento de caña de azúcar (Sacharum officinarum) de la compañía azucarera de los Mochis S. A. de C. V., susceptibles de ser utilizadas como control biológico en el manejo integrado de plagas. Ra Ximhai. 5, 239–245. R Development core team, 2015. R: A Language and Environment for Statistical Computing. URL. R Foundation for Statistical Computing, Vienna, Austria. http:// www.R-project.org/. Rabb, R.L., Stinner, R.E., van den Bosch, R., 1976. Conservation and augmentation of natural enemies. In: Huffaker, C.B., Messenger, P.S. (Eds.), Theory and Practice of Biological Control. Academic Press, N.Y, pp. 233–254. Rand, T.A., Tylianakis, J.M., Tscharntke, T., 2006. Spillover edge effects: the dispersal of agriculturally subsidized insect natural enemies into adjacent natural habitats. Ecol. Lett. 9, 603–614. Ramírez, M., Armbrecht, I., Enriques, M.L., 2004. Importancia del manejo agrícola de la biodiversidad: caso de las hormigas en caña de azúcar. Rev. Colomb. Entomol. 30, 115–123. Ramírez, M., Chará, J., Pardo-Locarno, L.C., Montoya-Lerma, J., Armbrecht, I., Molina, C.H., Molina, E.J., 2012. Biodiversidad de hormigas hipogeas (Hymenoptera: Formicidae) en agroecosistemas del Cerrito, Valle del Cauca. Livestock Research for Rural Development 24, 15. http://www.lrrd.org/lrrd24/1/rami24015.htm. Rivera, L.F., Armbrecht, I., Calle, Z., 2013. Silvopastoral systems and ant diversity conservation in a cattle-dominated landscape of the Colombian Andes. Agric. Ecosyst. Environ. 181, 188–194. Root, R.B., 1975. Some consequences of ecosystem texture. In: Levin, S.A. (Ed.), Ecosystem Analysis and Prediction. SIAM, Philadelphia, Pennsylvania, pp. 83–92. Rossi, M.N., Fowler, H.G., 2004. Predaceous ant fauna in new sugarcane fields in the state of Sao Paulo, Brazil. Braz. Arch. Biol. Technol. 47, 805–811. Salisbury, C., 2018. Could El Niño and Climate Change Spell the End for Tropical Forests? (accessed 4 May 2019). https://news.mongabay.com/2018/06/could-el-nino-andclimate-change-spell-the-end-for-tropical-forests/. Sanabria-Blandón, M.C., Chacón de Ulloa, P., 2011. Hormigas cazadoras en sistemas productivos del piedemonte amazónico colombiano: diversidad y especies indicadoras. Acta Amazon. 41, 503–512. Sánchez-Soto, S., 2016. Aves rapaces asociadas a linderos arbóreos adyacentes a cultivos de caña de azúcar (Saccharum spp.) en la Chontalpa, Tabasco. Agroproductividad. 9, 3–7. Santos, L.A.O., Bischoff, A., Fernandes, O.A., 2018. The effect of forest fragments on

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