Introduction

Reconciling biodiversity conservation with farming production is presently one of the great challenges of mankind [1,2]. This reconciliation has been discussed from two distinct perspectives: (1) the land-sparing approach, based on agriculture intensification, so that larger areas of native vegetation can be set aside for conservation [3,4] and (2) the land-sharing approach, based on wildlife-friendly agricultural systems [5,6]. One of the main production systems associated with the land-sharing approach is agroforestry, a system of extensive management where agricultural products are cultivated in association with native or exotic trees [7]. Nowadays, extensive areas of native forests in the tropics have been converted into cacao and coffee agroforests [8,9]. Several studies have suggested that these agroforestry mosaics may favor the reconciliation of agricultural production and biodiversity conservation [6,10,11], but worldwide management intensification of agroforests may limit such benefits. [11,12]. To increase short term income levels, agroforests shaded by native trees have been converted into plantations shaded by few species of exotic trees or unshaded monocultures [11,13].

Agroforests shaded by native trees harbor a significant component of native faunas [1415–16], especially in comparison to more intensively-managed areas. However, given that disturbance facilitates colonization by invasive species [17,18], agroforests, especially those more intensively-managed, should be more susceptible to invasion than native forest remnants. This greater susceptibility may limit the conservation value of agroforestry systems. Biological invasions have been growing worldwide [19,20], and are today the second greatest threat to biodiversity [21,22], affecting different levels of ecological organization, from individual behavior [23] to ecosystem processes [24]. It has already been shown that native generalist species tend to increase and forest specialist species decrease in agroforests compared to native forests [25,26]. Although scarce, evidence in the literature indeed indicates that these systems are more susceptible to invasions than native forests [2728–29].

The domestic dog - the most abundant carnivore in the world [30], introduced wherever man has settled [31] - can be considered an invasive species by all three perspectives on biological invasions [32]: biogeographical, ecological-evolutionary, and nature conservation. The first is based on the breakdown of geographic barriers to dispersal, which in the case of dogs was indeed only possible after their association with humans [33]. The second focuses on novel interspecific interactions resulting from the spread or even the increase in the dominance of a species in a community. Because domestic dogs explore natural environments and interact with native fauna [30,34,35], they also fit the ecological-evolutionary perspective of invasive species. Finally, the nature conservation perspective specifically requires a negative impact of the invasive species on native species, and this is well-established for domestic dogs, which impact native species through lethal and non-lethal effects of predation [36,37], competition [38,39], and disease transmission [40,41].

Indeed, it has been proposed that, although considered a domesticated species, dogs are better understood as a subsidized predator, which is maintained at much higher population density than native predators by its association with humans [37]. This is because in vast areas where it now occurs, especially rural landscapes, dogs are free-ranging, occupying home ranges that include areas of native vegetation and preying upon wildlife [42].Moreover, because dogs in these rural landscapes usually follow men at work [43], frequency of occurrence in different habitats may be influenced by human activities. In agroforests, the presence of domestic dogs may thus be facilitated by human activities, which are more frequent in more intensively-managed systems.

However, although recent studies have shown that domestic dogs frequently use native vegetation in the tropics [e.g. 44–46], little is known about the presence of dogs in agroforestry mosaics. In a previous study conducted in one of the most important agroforestry regions in Brazil, we found that the number of records of domestic dogs better explains the decline of native mammals in agroforests than either the reduction of native forest cover in the surroundings or the local vegetation simplification [47]. Despite this evidence that dogs pose a threat to wildlife in agroforests, we still do not know which factors drive the distribution and abundance of dogs in agroforestry mosaics. We address this knowledge gap by investigating three interrelated hypotheses: (1) the conversion of native forests into agroforests and (2) management intensification in agroforests favor the invasion by domestic dogs, and (3) the invasion by these exotic animals is more associated with human activity in agroforests than in native forests. We draw on a standardized sampling protocol with camera-traps in 30 cacao agroforests and nine native forests throughout a 64,000-ha agroforestry mosaic. With this dataset, we examined whether the number of domestic dogs and the mean number of visits per dog (1) are higher in agroforests than in native forests and (2) increase in agroforests as management intensifies, and (3) whether days and times of visits by dogs are more concentrated in the periods of greater human activity in agroforests than in native forests.

Methods

Study area and sampling sites

The study was carried out in a 64,000-ha agroforestry mosaic in the Una and Arataca municipalities, in the cacao-growing region of southern Bahia, Brazil [48]. The climate is hot and humid, with no well-defined dry season [49]; average annual precipitation varies between 1,200 and 1,800 mm, and average annual temperature is 24.5°C [50]. The region was originally covered by Atlantic Forest, classified as “Southern Bahian Moist Forest” [51]. Nowadays 50% of the landscape is covered by native forests and 15% by cacao agroforests (Fig. 1). The studied agroforests, locally known as cabrucas, are cacao plantations where native trees from the original forest are left for shade; the understory is composed predominantly of cacao trees, and the herbaceous vegetation is absent or periodically removed [52]. The studied native forests are well-conserved old-growth forests, but may have suffered different levels of selective logging in the past.

Fig. 1.

Map of Brazil outlining the State of Bahia (a), map of Bahia showing the location of the study agroforestry mosaic (b), and land use in the study agroforestry mosaic, indicating the location of sampling sites (c).

Despite harboring a simplified mammal fauna, from which large felids (jaguar - Panthera onca, and puma - Puma concolor) and ungulates (tapir - Tapirus terrestris, and peccaries - Tayassu pecari and Pecari tajacu) are rare or locally extinct, the studied mosaic of native forests and agroforests is an important area for species of conservation concern, especially small primates (golden-headed lion tamarin - Leontopithecus chrysomelas, and Wied's marmoset - Callithrix kuhlii) [16].

We sampled 39 sites throughout the agroforestry mosaic, 30 in agroforests and nine in native forest remnants adjacent to nine of these agroforests (Fig. 1). The 30 agroforest sites were chosen to capture the variation in management intensification. Criteria for site selection were: (1) shaded cacao agroforests where exotic trees did not exceed 50 percent of the canopy layer (cabrucas), but which varied widely in management intensification associated with tree density and composition in the canopy layer, cacao density, and the clearance of herbaceous vegetation (these aspects were verified in the field, Appendix 1); (2) a minimum distance of 1.5 km between sites; and (3) sites that could be accessed (i.e., avoiding remote areas too far from any roads) [47]. For nine of these 30 agroforests sites, we sampled also an adjacent native forest in a paired design. Sites within a agroforest-native forest pair were between 200 and 450 m from each other, but a minimum distance of 100 m from the edge between native forest and agroforest. The nine agroforests with paired native forests were a minimum distance of 2.5 km apart; the sampled native forests were old-growth well-conserved forests, and the size of native forest and agroforest patches varied among the nine pairs.

Data collection

A camera-trap was installed in each of the 39 sampling sites, placed at 20–30 cm from the ground, baited with a small piece of sardine and bananas to increase the detection of dogs and ensure the precision of abundance estimates, while not affecting habitat use [53]. In all 39 sites, traps were active over four sampling sessions of ~ 30 days each, which occurred (for all sites) from July to October 2007 and 2008, and from January to April 2008 and 2009. Due to trap malfunctions, the sampling effort varied from 94 to 127 camera-days among the nine sites in native forest remnants, and from 90 to 126 camera-days among the 30 agroforests, totaling, respectively, 1,021 and 3,325 camera-days in each habitat and 4,346 camera-days in the agroforestry mosaic. Recorded dogs were identified from characteristics such as fur color, sex, size, breed, scars, and markings to obtain the number of individuals per sampling site, and the days and times of visits (Fig. 2). From a total of 716 photos of domestic dogs, only 23 (3.2%) did not allow individual identification.

Fig. 2.

Domestic dogs recorded in camera traps in cacao agroforests in southern Bahia, Brazil.

During camera-trap data collection, in all 30 agroforest sites we measured 14 vegetation structure variables to quantify management intensification (Appendix 1). Measurements were taken in four plots of 10 × 25 m, every 20 m, in an area of 25 × 100 m around the camera trap of each site.

Results

Agroforests versus adjacent native forests

In the nine agroforest-native forest pairs, we observed 80 dogs, with only three of them recorded in both habitats. Of this total, 65 dogs were recorded in agroforests and only 18 in adjacent native forests. Indeed, only the model with abundance as a function of habitat type and detectability as a function of sampling effort was selected (Appendix 2), indicating that the number of invading dogs is higher in agroforests than in native forest remnants (Figura 3a). The estimated number of invading dogs was 11 per site and 99 in the set of nine sites in agroforests, and seven per site and 63 in the set of nine sites in native forests. In contrast, the mean number of visits among individuals recorded at each site did not differ consistently between habitats (Figura 3b), with only the constant model being selected (Appendix 3).

Fig. 3.

Number of individuals of domestic dogs (a) and mean number of visits among individuals (b) recorded in nine pairs of agroforests and adjacent native forests. Values of adjacent sampling sites are interconnected. Squares in (a) represent estimates obtained by the selected abundance model (Appendix 2).

In both habitats visits by dogs were not homogeneously distributed during the day (Rayleigh test: for native forests p<0.01; for agroforests p<0.01), concentrating at 13:14 h in native forests and 12:43 in agroforests (Fig. 4), and the time of visits did not differ between habitats (Watson homogeneity test: p=0.15). Similarly, in both habitats (and not only in the agroforests as predicted) visits by dogs tend to be concentrated on working days (marginally significant result of Chi-square tests in both cases; native forests ϧ²=0.70; p=0.08; agroforests ϧ²= 0.67; p=0.08) (Appendix 4).

Agroforests with varying management intensification

The first axis of the PCA explained 27.3% of the variation in vegetation structure among the 30 agroforest sites, and represented a gradient of increasing management intensification associated with a decrease in tree shading and an increase in the frequency of clearance of the herbaceous vegetation and in the density of cacao shrubs and banana stems (Appendix 5). The second axis of the PCA explained 20.9% of the variation in vegetation structure and seems less directly related to management intensification, and more associated with the age of agroforests. Higher values of this axis represent mainly agroforests with smaller native trees, but with larger cacao shrubs (Appendix 5).

In total, we observed 145 dogs in the set of 30 agroforest sites, with none of them recorded in more than one agroforest. Only the model with detectability as a function of sampling effort and abundance constant was selected (Appendix 6). The estimated average number of dogs that use each agroforest was 12 individuals, with 360 dogs estimated to use the set of all 30 agroforests. It is noteworthy, however, that although not among the selected models, the model with abundance as a function of management intensification (PCA1) is ranked second (Appendix 6), indicating that management intensification has a positive, although weak, effect on the number of invading dogs (Figura 5a). In contrast, the two models that were selected to describe the mean number of visits among individuals recorded at each site contained management intensification (PCA1) as an independent variable (Appendix 7), indicating that the number of visits per dog increases in more intensively-managed agroforests (Figura 5b).

Fig. 4.

Time of visits by domestic dogs to nine pairs of agroforests and adjacent native forests. Arrow: time at which visits concentrate; triangles: number of visits per 2-hour interval.

Discussion

The observed and estimated numbers of domestic dogs suggest that the intensity of invasion in agroforestry mosaics is high, representing a potential threat to the fauna of these landscapes. Not only dogs have been shown to impact native species through lethal and non-lethal effects of predation [36,37], competition [38,39], and disease transmission [40,41], but also we found in a previous study that the number of records of dogs was the main driver of the decline of native mammals in the studied agroforestry mosaic [47].

More importantly, our results corroborate the hypothesis of this study that the conversion of native forests into agroforests, as well as management intensification in agroforests, favor the invasion by domestic dogs. On the other hand, despite evidence that visits by dogs are associated with times and days of greater human activity, this association is not stronger in agroforests than in native forests, as we expected. Because only three of the 80 dogs recorded in the nine agroforest-native forest pairs were recorded in both habitats, this association of the presence of dogs with human activity is not just an artifact of the proximity of the sampled agroforest-native forest sites. Rather, despite the smaller number of dogs in native forests than in agroforests, the presence of dogs in native forests seems to be associated with human activity, although not necessarily with the activity of workers in the adjacent agroforests. Below we discuss each of these main results and their implications.

Fig. 5.

Number of individuals of domestic dogs (a) and mean number of visits among individuals (b) as a function of management intensification (PCA1, Appendix 5) throughout 30 agroforests. Empty dots: observed numbers; solid line and filled dots: estimates from models with management intensification as a co-variable (Appendices 6 and 7); black bars and black dashed lines: standard deviations of these estimates.

As expected, the number of invading dogs was higher in agroforests than in native forests. In contrast, the mean number of visits per individual did not vary between the two habitat types. As in other studies [44,61], most individuals were recorded only once, both in native forests and in agroforests. Thus, the higher number of records of dogs in agroforests than in native forests in the study region [16] results mainly from the entrance of a larger number of dogs, rather than from more frequent visits by the same individuals. The higher the number of individuals, the larger the probability of disease transmission to wild animals, adding to the expected negative effects of competition and predation by dogs [34,35,62,63].

Given that the number of people entering managed systems such as agroforests is much higher than in unmanaged native forests, the higher number of dogs in this agricultural system may be simply linked to the behavior of dogs following their owners to work [43]. This hypothesis is supported by our finding that there is an association between dog presence and the time of the day and the days of the week with greater human activity. Beyond the association with workers, however, the higher number of dogs in agroforests than in native forests may also be related to environmental factors. Compared to native forests, agroforests present a simplified vegetation structure, which may facilitate the access and movement of dogs, since these animals move preferentially through open habitats [64,65]. Also, vegetation thinning in agroforests may influence native fauna, with several native species becoming less frequent in agroforests than in native forests [16,29]. If large predators that may chase or kill domestic dogs are more susceptible to vegetation thinning than mid-sized and small vertebrates (preys), simplification of the native fauna may also contribute to the higher number of dogs in agroforests than in native forests.

By contrast, in agroforests the positive effect of management intensification was stronger on the mean number of visits per individual than on the number of invading dogs. More intensively-managed plantations, associated with a higher frequency of herbaceous vegetation clearance and a higher number of cacao shrubs, require a higher frequency of workers or longer working periods, and result in more open vegetation close to the ground. Both characteristics may lead to the increase in the number of visits per dog in more intensified agroforests, either because they follow their owners who enter more frequently or stay longer in these plantations, or because their movement is facilitated in more open environments [64,65]. However, these characteristics do not necessarily affect the number of dogs that visit agroforests, which may also depend on other factors, such as the quantity of dogs raised in surrounding areas (i.e. propagule pressure [66,67]) or on the number of workers, probably more associated with plantation size and other socioeconomic factors than with management intensification per se. It is important that future studies on the distribution and impacts of dogs in agroforestry mosaics focus on these socio-economic dimensions.

In summary, our findings suggest that the higher number of invading dogs in agroforests compared to native forests is associated with the larger number of people who enter and stay in these managed systems, while the higher number of visits in more intensively-managed agroforests may be associated with a higher frequency/length of stay of workers. Although both conversion of native forests into agroforests and management intensification in agroforests affect invasion by domestic dogs, they influence distinct aspects, which may be associated with differences in the presence of people between these two habitats. In fact, in both environments (and not only in agroforests) visits by domestic dogs seem to be associated with the period of human activity, concentrating during the day, as observed in other studies [e.g.44,46], and on working days during the week. This suggests that the control of invasion rests on conscious efforts by workers and local residents to limit the movements of their dogs - by keeping them home instead of allowing or stimulating dogs to follow them into agroforests.

Implications for conservation

Our results, as well as previous studies [2728–29], indicate that, though permeable to wildlife [15,68], agroforests may act as trap or sink areas, given the higher intensity of invasion compared to native forests, which should restrict the conservation value commonly attributed to agroforests [6,10]. More importantly, our study suggests that agroforest management intensification, which is becoming more pronounced on a global scale [11,12], increases the risks of invasions, potentially limiting the value of this agricultural system for reconciling food production and biodiversity conservation. Indeed, the domestic dog record rate was one of the most important factors negatively associated with the distribution of wild mammals in agroforests of the study region [47].

Furthermore, our study suggests – both by the association of domestic dog visits with the periods of greater human activity, and by the fact that native forest conversion into agroforests led to an increase in the number of dogs while management intensification in agroforests led to an increase in the number of visits per dog - that there is a strong association between the invasion by domestic dogs and human activities. Yet, this association does not depend on the type of habitat, and apparently occurs also in unmanaged systems, such as native forests. Thus the value of agroforestry mosaics for conservation depends on the proper management of invasive species, and at least in the case of dogs, one of the most common and widely distributed invasive species, this management should focus on how workers and residents treat their dogs. In contrast to other aspects of agroforest management intensification that negatively affect wildlife (e.g. thinning of shade trees and higher frequency of herbaceous vegetation clearance [47]), increased invasion by domestic dogs can be avoided with no impairment to agroforest productivity. Although no management solution to avoid the impact of dogs on wildlife will be simple, awareness and education campaigns to discourage workers to allow their dogs to follow them into agroforests can be a step forward, and could be incorporated in action plans for increasing the conservation value of agroforestry mosaics.