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Article

Indirect Effects of Cattle Trampling on the Structure of Fruit-Feeding Butterfly Assemblages Inhabiting Restinga Forests in Southern Brazil

by
Cristiano Agra Iserhard
1,*,
Taiane Schwantz
1,
Mariana Centeno Gallo
1,
Marco Silva Gottschalk
1 and
Kauane Maiara Bordin
2
1
Programa de Pós-Graduação em Biodiversidade Animal, Departamento de Ecologia, Zoologia e Genética, Instituto de Biologia, Universidade Federal de Pelotas, Pelotas 96010-900, Brazil
2
Departamento de Ecologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre 91501-970, Brazil
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(8), 467; https://doi.org/10.3390/d16080467
Submission received: 1 July 2024 / Revised: 31 July 2024 / Accepted: 31 July 2024 / Published: 3 August 2024
(This article belongs to the Special Issue Biogeography and Diversity of Butterflies and Moths)
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Abstract

:
The impacts of anthropogenic activities are increasing at alarming rates, leading to biodiversity loss and the displacement of native habitats. One of the main contributors to human disturbances is livestock farming, which degrades native habitats through cattle grazing and trampling. To understand these impacts, we investigated the effects of cattle trampling on the structure and diversity of fruit-feeding butterflies in Restinga forests of southern Brazil. We addressed questions regarding the effects of cattle raising on butterfly diversity and composition, identified indicator species, and examined the influence of environmental variables on butterfly richness, dominance, abundance, and species composition. Our dataset comprises the long-term monitoring of fruit-feeding butterflies in Restinga forests from 2014 to 2019, across sites with low, medium, and high levels of disturbance due to cattle trampling. We found that medium and high levels of disturbance increased butterfly richness and abundance, whereas low-level disturbance was associated with lower abundance. Additionally, the species composition of butterflies in medium to highly disturbed sites differed from that in preserved Restinga forests, indicating that any perturbation can markedly alter alpha and beta diversity parameters. These changes simplify the native forest structure, open the canopy, disrupt the understory, and favor butterfly species commonly associated with disturbed forests.

1. Introduction

The environmental impact of anthropogenic actions is increasing at alarming rates, leading to biodiversity loss and the displacement of native habitats by exotic and introduced species [1]. Livestock farming, a vital human activity, often leads to native habitat degradation through grazing and trampling, thereby increasing the risk of extinction and the depletion of plant and animal populations [2,3]. On the other hand, some studies indicate a positive relationship of cattle activities resembling the extinct herbivore megafauna of the Pleistocene as ecosystem engineers in the present [4]. The movement of several animals, particularly through cattle trampling, is one of the adverse mechanisms altering habitat dynamics and structure [5]. This activity disrupts several ecological processes, such as reducing vegetative coverage, eliminating saplings, and damaging forest canopies [6,7]. Additionally, it leads to soil compaction or the destabilization and redistribution of the litter layer, thereby increasing areas of bare ground [8]. Moreover, the presence of large herbivores modifies vegetation architecture by creating forest gaps, which decrease the growth of shrubs and juvenile trees [9,10], thereby shaping the species composition, stability, and diversity [11,12,13,14,15,16,17,18].
Habitats exhibiting greater spatial heterogeneity tend to harbor more species due to the formation of diverse microhabitats and niches, encompassing variations in abiotic characteristics across distinct gradients [19]. The species richness and composition of plant communities linked with abiotic factors are correlated with animal diversity [20]. In this context, activities like cattle trampling play an important role in vegetation growth and structure, altering specific characteristics of microclimate and soil [3,21]. These dramatic changes in abiotic and biotic features do not allow for proper forest recovery, and ecological succession does not follow the expected trajectories [22]. Consequently, there is a reduction in resource availability and changes in interactions between invertebrates and plants, which impact diversity patterns and may lead to the biotic homogenization of ecosystems [23,24]. Thus, the introduction of large mammal herbivores may indirectly shape invertebrate biodiversity within such habitats [22,25,26,27,28,29], disrupting their dynamics and ecological processes.
Studies regarding the effects of cattle trampling on vegetation have mainly focused on grassland ecosystems and previously grazed areas with distinct types of management in the Northern Hemisphere [30,31]. These studies highlight that the effects of trampling may be either negative for forest vegetation recovery [30] or positive for avoiding biotic homogenization in grasslands [31]. However, studies testing the effects of trampling on insects yield contrasting results depending on the studied system [32,33,34,35]. While much research has focused on the effects of cattle trampling in grassland ecosystems, far less is known about its impact on forested habitats, particularly in tropical regions worldwide. This gap has been largely neglected, with studies primarily focusing on the effects on vegetation dynamics, such as forest recovery and regeneration [36,37,38,39]. Thus, over the last few decades, there has been a growing interest in the impacts of cattle activities on forest ecosystems [40], with a limited and little-explored evaluation of the indirect impacts on animal assemblages.
The effects of cattle trampling in forested habitats in austral South America depend on the forest habitat type and its attributes. For instance, grassland ecosystems often benefit from cattle grazing presence, as it increases the richness and abundance of arthropods under deferred grazing systems [41,42]. In contrast, several studies suggest that cattle trampling negatively affects the conservation and management of forest ecosystems [40] by benefiting light-demanding species due to canopy openness [6]. Additionally, understanding the patterns and processes influenced by cattle trampling on biodiversity in temperate and subtropical forests of the Southern Hemisphere is a recent area of study with significant knowledge gaps [40]. The Restinga forest (also considered a “sand forest”) is a remarkable ecosystem in South America. Despite its ecological importance, it has been suffering from several threats due to anthropogenic actions, such as the impacts of real estate development, agriculture, and cattle raising [40]. This unique forest ecosystem is characterized by phytophysiognomies that have developed on sandy dunes formed along the Brazilian Atlantic coast in the past [43,44,45,46], and the vegetation plays a central role in stabilizing the substrate, maintaining natural drainage, and preserving the resident and migratory fauna [47].
Several important actions for conserving Neotropical landscapes and ecosystems involve utilizing organisms with high sensitivity and rapid response to anthropogenic activities [48,49]. In this context, butterflies are excellent environmental indicators due to their strong association with microhabitats and specialization in specific environmental resources, enabling quick responses to perturbation gradients and ecosystem health [50,51,52,53]. Thus, populations and assemblages of butterflies are directly and indirectly affected by distinct levels of disturbances caused by habitat change. These disturbances impact the structure of forests, which affect abiotic conditions such as temperature, humidity, and light conditions, reducing the availability of resources that are essential for the survival of butterflies [52,54,55,56].
Fruit-feeding butterflies belong to Nymphalidae, including the subfamilies Satyrinae (Satyrini, Morphini, and Brassolini tribes), Charaxinae, Biblidinae (except for Dynamine), and Nymphalinae (Nymphalini and Coeini tribes), which, as adults, primarily consume decaying fruits, plant exudates, carnivore feces, and decomposing organic matter [57]. This guild offers practical advantages for sampling its assemblages: (i) they are easily captured using bait traps, and (ii) sampling can be conducted simultaneously, with a standardized effort across different sites and regions [57]. Thus, fruit-feeding butterflies represent the most suitable group within the Lepidoptera for studies concerning the diversity and structure of communities related to conservation in tropical ecosystems [58].
Our study aims to investigate the indirect effects of cattle trampling on the structure and diversity of fruit-feeding butterfly assemblages in Restinga forests in extreme southern Brazil. Specifically, we address the following questions: (i) Is there a segregation in butterfly species composition among these habitats, including identifying indicator species for each habitat? (ii) Are there differences in butterfly diversity parameters among Restinga forests with low levels of cattle trampling compared to those with medium and high levels of disturbance? (iii) How do the environmental variables and vegetation structure of Restinga forests affect the richness, abundance, and dominance of fruit-feeding butterfly assemblages due to indirect disturbances caused by cattle presence? We expect that (i) the species composition of fruit-feeding butterflies will differ between preserved and disturbed Restinga forests, with the latter characterized by generalist species commonly found in disturbed environments; (ii) the richness and equability of butterfly assemblages will be higher in low-level disturbed Restinga forests compared to those with medium and high levels of cattle trampling, which will exhibit higher dominance; (iii) habitats with low cattle trampling will have lower light incidence in the understory, greater vegetation height, and higher humidity, leading to increased richness and decreased abundance, with a more even distribution of species abundance compared to Restinga forests with medium and high levels of cattle disturbance.

2. Materials and Methods

2.1. Study Area

Our study was carried out at Horto Botânico Irmão Teodoro Luis (HBITL), a 25 ha protected area, and at adjacent Restinga forest sites located in the Coastal Plain of Rio Grande do Sul State, extreme southern Brazil (Figure 1A,B). The study area is located in the Pampa biome, and its vegetation is classified as Pioneer Formations influenced by the Atlantic Forest biome [59] (Figure 1C,D). These forests are interspersed with native grasslands influenced by cattle trampling at distinct levels of disturbance, ranging from isolated areas with minimal use (such as HBITL) to sites with moderate to high interference (Figure 1D–G). Cattle use these forested areas to move among distinct grassland areas, rest, and care for their offspring. In this region, the Restinga vegetation consists of communities over sandy deposits, commonly composed of a high density of short plants (up to 12 m) with emergent tree species forming three strata: arboreal, shrubby, and herbaceous [60] (Figure 1C). The arboreal component of the Restinga forests includes some fresh-fruit tree species with the potential to attract fruit-feeding butterflies, such as Allophylus edulis Niederl., Cupania vernalis Cambess. (Sapindaceae), Psidium cattleianum Sabine, Eugenia myrcianthes Nied., Eugenia uniflora L. (Myrtaceae), Ficus enormis (Mart. ex Miq) Mig., Ficus organensis (Mig.) Miq. (Moraceae), Vitex megapotamica (Spreng.) Moldenke (Lamiaceae), Ocotea pulchella (Ness) Mez (Lauraceae), Erythroxylum argentinum O.E.Schulz (Erythroxylaceae), Cereus hildmannianus K.Schum., Opuntia monacantha (Willd.) Haw. (Cactaceae), and Syagrus romanzoffiana (Cham.) Glassman (Arecaceae). The climate is humid subtropical with hot summers and four well-defined seasons, according to Köppen’s classification [61]. The region’s annual mean temperature and relative humidity are 17.8 °C and 80.7%, respectively, with precipitation around 1365 mm per year [62].

2.2. Determination of Disturbance Level

We conducted previous field expeditions to select the studied Restinga forests and to evaluate the disturbance level caused by cattle trampling on the vegetation. The sites were chosen based on criteria such as isolation (with or without fencing to exclude cattle) and the quantity of feces and cattle tracks, determining the distinct disturbance levels: low, medium, and high (Figure 1E–G).
We selected nine Restinga forest sites (sampling units—SU) across a gradient of cattle trampling disturbances, with each SU separated by at least 300 m from others to ensure independent replicates (Figure 1B). The sites were grouped into three categories based on the level of cattle trampling disturbance: two sites with low-level disturbance, three with medium-level disturbance, and four with high-level disturbance (Figure 1). To evaluate and validate the three categories of cattle trampling disturbance in the Restinga forests, we conducted quantitative measurements of feces density across all seasons during the first year in each SU within the area occupied by the five placed traps (the distribution of the traps followed a conformation of a square resembling the number five of a dice), totaling approximately 100 m2. This enabled us to determine the levels of disturbance by assessing the intensity of cattle presence by visually counting the number of feces. We further obtained the density of feces in each sampling unit and transformed it into a proportion related to each disturbance level (Table 1).

2.3. Environmental and Structural Variables

To fully characterize the structure of the distinct Restinga forests, we measured the temperature and humidity at each site on all sampling days using a digital thermo-hygrometer (THAL-300) (Table 1). Additionally, we evaluated the vertical structure of the understory vegetation of each site. Measurements were taken using a banner measuring one meter in width and two meters in height, divided into 50 squares of 20 cm × 20 cm, alternating in black and white to facilitate the observations of vegetation height. The banner was randomly positioned based on cardinal directions (North, South, East, and West) and stretched eight meters in front of each trap. An observer measured the understory height, including all five traps in the SU. Thus, each site had five measurements of understory height, assessed by counting the square numbers obstructed by the vertical vegetation structure [63] (Table 1).
Canopy coverage measurements were carried out using a Lemmon convex spherical densiometer (D) [64]. Readings were taken in the four cardinal directions to obtain a complete representation of canopy openness, all performed by the same observer. The densiometer consists of a convex mirror divided into 24 quadrants, each further subdivided into four parts (totaling 96). The number of parts reflecting light in each quadrant was systematically counted, and the total count was summed and multiplied by 1.04 to estimate canopy coverage as a percentage [64] (Table 1). All environmental variables were used as predictors in the analyses, assessed through average values, and showed no significant correlation according to Pearson’s correlation test (Figure S1).

2.4. Sampling Design

We conducted standardized monthly samplings from December 2014 to November 2019, resulting in five years of data collection. In each SU, we placed five Van Someren-Rydon bait traps ten meters apart from each other, totaling 45 traps suspended 1.5 m above the ground in the vegetation [57] (Figure 1E–G). Each trap consisted of a white cloth cylinder with 110 cm high and 35 cm in diameter, opened at the bottom and closed at the top. The cylinder is attached to a base with a gap of approximately 5 cm between the base and the cylinder opening, in which a small plastic pot holds the bait [57]. Traps were set on the first day of each sampling occasion and checked daily for three consecutive days, remaining in the field for four days. The bait consisted of mashed banana fermented in sugar cane juice, prepared 48 h before the beginning of a sample occasion, and replaced every 24 h [57]. It is important to highlight that cattle feces do not attract fruit-feeding butterflies under any conditions because it is herbivore fecal matter. Captured fruit-feeding butterflies were identified to the species levels and marked with a permanent pen before release to avoid counting the same individual twice. Specimens not identified in the field were collected for mounting and identification in the laboratory. All collected individuals are deposited in the Lepidoptera collection of the Laboratório de Ecologia de Lepidoptera associated with the Museu de Ciências Naturais Carlos Ritter, Instituto de Biologia, Universidade Federal de Pelotas, Brazil.

2.5. Data Analysis

To evaluate whether there is a segregation in butterfly species composition among the habitats (i.e., low, medium, and high-level disturbance, question i), we performed a Non-Metric Multidimensional Scaling (NMDS, metaMDS function, vegan package [65]), using the species abundance per SU across all sampled years and the Bray–Curtis dissimilarity index. To assess the significance of the distinct clusters in the ordination space, we employed a PERMANOVA with the same resemblance measure and 999 permutations (adonis2 function, vegan package). We calculated the indicator value analysis (IndVal) to verify possible butterfly species indicators of Restinga forests at low, medium, and high-level disturbances [66]. We assessed the IndVal by choosing species to a minimum of five individuals. Thus, we used the relationship between species abundance to evaluate the species specificity (A) and fidelity (B) of each habitat. Values of specificity equal to 1 indicate that the species were present in all sites and sampling occasions of one disturbance level. In contrast, fidelity values equal to 1 indicate a 100% probability of finding the species in all samples in locations with the same disturbance level [66]. We included species as indicators when, besides the significant p-value (≤0.05), the IndVal statistic was more than 0.75. The IndVal was calculated using the indicspecies package [67].
To answer question ii, we analyzed the rarefied richness, abundance, and species composition of fruit-feeding butterflies in each Restinga forest’s distinct levels of cattle trampling disturbance. The representativeness of the butterfly assemblages for each habitat was assessed by sample coverage based on the sampling completeness (q statistic) [68] with abundance data and 1000 permutations [69]. The alpha diversity of butterfly assemblages in each habitat was evaluated through an empirical diversity profile (999 permutations) employing the q statistic obtained by Hill numbers with 95% Confidence Interval [68,70]. The Hill numbers were calculated based on the q order, in which q = 0 indicates a species richness index; q = 1 is analogous to the Shannon equability index; and q = 2 indicates the Simpson dominance index [70,71]. These analyses were performed in iNEXT online [72]. The species abundance distribution curves for all disturbance levels were plotted to evaluate the dominance of fruit-feeding butterfly species.
Finally, to answer question iii and test whether the environmental and vegetation structure variables affect the rarefied species richness, abundance, and dominance of fruit-feeding butterflies, we fitted generalized linear mixed models. We considered a normal distribution in the residuals for the rarefied richness and dominance and a Poisson distribution for abundance. Once we detected overdispersion in the abundance model, we fitted the model using a negative binomial model structure [73]. We used the lmer function to test the rarefied richness and dominance models and glmer.nb to test the abundance model (lme4 package) [74]. Finally, we tested the relationship among the environmental and structural variables with the variation in species composition extracted from the first and the second axes of the NMDS using the envfit function (1000 permutations, vegan package). We considered the year of sampling (1 to 5) as a random intercept within the models. The NMDS, PERMANOVA, IndVal, and GLMM analyses were conducted in the R environment [75].

3. Results

After 113,400 h of sampling effort, we recorded 2059 individuals distributed across 32 species belonging to the four subfamilies of Nymphalidae fruit-feeding butterflies. The Restinga forest sites with high-level disturbance had 1195 individuals and 26 species, followed by sites with medium (718 individuals and 26 species) and low disturbance levels (146 individuals and 18 species). Satyrinae was the richest subfamily with 16 species, followed by Biblidinae (9), Charaxinae (4), and Nymphalinae (3). Sampling coverage indicated that all habitats had over 97% completeness, showing that the fruit-feeding butterfly assemblages were well-represented.
The NMDS summarized the fruit-feeding butterfly assemblages’ dissimilarity across the distinct Restinga forest disturbances, indicating distinct species composition according to the different levels of cattle trampling disturbance (Figure 2). The PERMANOVA indicated differences in species composition among the studied Restinga forests (F = 6.286; p = 0.001), in which the pairwise comparisons showed no differences between medium and high-level disturbances (F = 1.581; p = 0.140). Conversely, the low-level disturbance had a distinct species composition of butterflies compared to medium (F = 8.324; p = 0.0001) and high-level (F = 8.894; p = 0.0001) disturbed Restinga forests. In addition, the species composition across the low-level disturbed area is mainly determined by a high mean humidity, understory height, and higher percentage of canopy cover (Figure 2, Table 2). The mean temperature did not affect the species composition in the studied areas (Table 2).
The IndVal analysis identified one fruit-feeding butterfly species as an indicator of high-level disturbance and five indicators in the combination of medium and high levels of disturbance (Table 3, Figure 3). These species belong to the Biblidinae, Satyrinae, and Charaxinae subfamilies (Table 3). The low and medium levels of disturbance did not present any indicator species (Table 3).
Regarding alpha diversity parameters through the empirical diversity profile, Restinga forests with medium and high levels of cattle trampling had higher species richness than low-level disturbance (Figure 4A). On the other hand, the evenness (q = 1) and dominance (q = 2) among all habitat types did not differ (Figure 4A). Despite these results, there is a trend toward a more equitable distribution of butterflies in low-level disturbance sites according to the species abundance distribution curve compared with the more disturbed sites (Figure 4B).
Both the rarefied species richness and dominance were not predicted by the environmental and structural variables tested in this study (Table 4). On the other hand, the abundance was negatively related to structural variables (i.e., canopy cover and understory height, Table 4), meaning that open areas with lower understory coverage have a higher abundance of fruit-feeding butterflies inside the Restinga forests.

4. Discussion

This study is the first assessment of the responses of fruit-feeding butterfly assemblages to varying intensities of cattle trampling disturbance in the Restinga forests of a subtropical region in southern Brazil. We found that medium and high-level disturbances increased butterfly species richness and abundance. In contrast, areas with low-level disturbance, characterized by a more structured forest interior with a closed canopy and higher understory height, had lower butterfly abundance. Additionally, the species composition of fruit-feeding butterflies in disturbed sites differed from that in preserved Restinga forests, indicating that any perturbation can markedly alter alpha and, mainly, beta diversity parameters. These changes are likely due to the simplification of the native forest structure, which opens the canopy, disrupts the understory, and favors butterfly species commonly associated with perturbed or open forests.
The species composition of fruit-feeding butterfly assemblages differed between preserved and disturbed Restinga forests, as beta diversity and the IndVal analyses indicate species turnover and segregation into two main groups. One group showed a subset of species associated with low-level disturbance, while the other one presented a pronounced effect of cattle trampling on species composition. The increasing disturbance due to cattle in the Restinga forests generates environmental conditions that filter for indicator species of medium and high-level disturbance. These species often have high abundance and commonly use the canopy (such as Zaretis strigosus (Gmelin, 1788)), as well as the forest edge, open forests, and/or perturbed environments, like the small-brown satyrines Cissia phronius (Godart, [1824]), Paryphthimoides poltys (Prittwitz, 1865), and Capronnieria galesus (Godart, 1824) [56,76], and the biblidine Eunica eburnea (Fruhstorfer, 1907). These species are common in various habitat types due to the more suitable conditions in open and sunny areas [50]. Thus, the studied disturbed Restinga forests presented numerous clearings, allowing the edge environmental conditions to penetrate harshly the core of forest fragments, creating conditions unsuitable for most forest-dwelling species.
The evenness and dominance of fruit-feeding butterflies in the distinct levels of cattle trampling disturbance do not differ, despite a trend of a more equitable species distribution in the low-level disturbance. Conversely, the rarefied richness was higher in disturbed forests, and some environmental and structural variables influenced the abundance of fruit-feeding butterflies. Increased canopy openness, as a result of cattle indirect impacts, allows more entry of light within the forest, possibly reducing environmental heterogeneity and leading to higher species richness and abundance, indicating that high solar radiation increases the daily activity of butterflies [77]. This may help the colonization of a few generalist and eurytopic species with a high number of individuals [20,78,79] because small-scale disturbance can increase in both richness and abundance, encompassing species of the regional pool able to use distinct perturbed habitats [80].
Conversely, forest-dwelling butterflies with low and evenly distributed abundances cannot survive in disturbed forests because they need a well-structured understory with distinct microclimates and niches [52,56,81]. For instance, butterflies inhabiting the preserved Restinga forest require shaded environments and are highly sensitive to humidity [82,83]. Therefore, these environmental conditions reflect a better quality and quantity of resources, increasing their survival [84]. Abrupt modifications in the canopy layer and light penetration possibly influence microclimatic variables with marked effects on host-plant quality [85] directly affecting adult and immature stages of forest-dweller butterflies. Consequently, the effects of cattle trampling may decrease the decomposer’s activities, modifying the soil–plant balance [22,86], which indirectly influences the composition of plant species and the use of these plants as hosts for butterflies. These results underscore that medium and high levels of disturbance may cause the local extinction of some species inhabiting the forest interior, while only the common species well-adapted to disturbed and open habitats may persist [56].
The simplification of vegetation structure may serve as corridors for certain butterfly species linked with forest canopies, which adapt by moving to the ground in perturbed areas for dispersal [52,53]. In our study, some species associated with the canopy may be able to use forest gaps within Restinga forests. Generally, gaps resulting from small-scale disturbances may act as suitable areas for reproduction, increasing predation intensity and enhancing survival [87], primarily used by opportunistic butterflies [85]. Females of certain canopy and edge species use host plants at the ground level [88,89], such as the grass-feeding Satyrini species and the vine-feeding Biblidinae [52]. Thus, the effects of cattle trampling may filter specific plant species, modifying the composition of vegetation [90,91], and, therefore, favor the oviposition of these generalist butterflies.
Our findings should also be contextualized within the broader debates on Pleistocene defaunation [92,93,94] and the role of large herbivores as ecosystem engineers [4,95]. The current conditions in Restinga forests may reflect a long-term ecological shift following the extinction of native megafauna around 10,000 years ago. These ecosystems evolved under the influence of large herbivores, and the absence of such animals may have led to denser forests. Cattle, while non-native, might partially fulfill the ecological roles once played by extinct megafauna, creating conditions resembling pre-defaunation ecosystems, suggesting that the disturbed Restinga forests might be closer to their historical state. Our results indicate that these conditions support higher butterfly richness and abundance, potentially benefiting species adapted to open habitats. However, these diversity parameters do not suggest increasing diversity; therefore, it is important to pay attention to the species abundance distributions and composition, where forest-dwelling butterflies occurred with low frequencies in the disturbed Restinga forests. Thus, considering the increasing occupation of native habitats by extensive cattle farming and the human modifications across all of Earth’s ecosystems, caution must be crucial with such comparisons. The present conditions are vastly different from those observed thousands of years ago. The habitat simplification observed today, such as in the studied Restinga forests, may contribute to the degradation of important insect refuges, as highlighted in our study.
In recent decades, human impacts on land use due to forest fragmentation, exotic species’ introduction, and extensive pasture intensification have increased greatly. Currently, more than 45% of the land worldwide has been replaced by some livestock practice [96]. In Brazil, livestock farming is a major economic activity, often conducted without proper management, leading to the replacement of native habitats by large farms with monocultures from agribusiness creating anthropogenic landscapes. While most studies on cattle grazing and trampling focus on grassland ecosystems [32,35], it is crucial to compare diversity patterns in forested sites interspersed with grasslands to provide conservation strategies and actions for maintaining the grassland–forest mosaic dynamics [97] without compromising either ecosystem. It is widely known that grasslands may benefit from the presence of cattle and other introduced herbivores [41,42], but these positive effects are not present in forest ecosystems, as highlighted by this study. In this way, the increase in livestock farming in forest ecosystems in Brazil (like Amazonia and Atlantic Forest biomes) leads to the disruption of forested habitats because of the large number of cattle raised intensively leading to deforestation, forest suppression, fragmentation [98], and the complete modification of the forests biotic and abiotic characteristics [99,100]. Thus, our study demonstrates that the dramatic modification of forested areas because of anthropogenic actions such as cattle raising causes severe alterations in fruit-feeding butterfly assemblages.
As underscored by the results presented here, it becomes imperative to increase knowledge to address the debate about the effects of distinct levels of cattle trampling on subtropical and tropical forested habitats across the Southern Hemisphere [40]. The loss of biodiversity driven by cattle trampling and its interactions can destabilize food chains and community diversity [86]. Although Restinga forests are often neglected in livestock systems, they are equally vulnerable to such impacts. We recommend implementing rational and effective management practices to minimize livestock activities within Restinga forests. This approach will help preserve these ecosystems and prevent the gradual and irretrievable loss of their ecological processes and services. The exclusion of cattle from forest habitats is mandatory, as well as the establishment of more public Protected Areas that preserve native grasslands and forests [97]. Another feasible suggestion for assessing the indirect effects of cattle in this forest–grassland mosaic is the establishment of partnerships with farmers. These partnerships would combine livestock practices with academic studies, thereby maintaining the economic activity of the property while conducting long-term ecological research focused on this important issue. These appointments will promote the conservation of a more heterogeneous landscape with native habitats, facilitate scientific research, and integrate conservation strategies into public policy. Such actions urge us to prevent cattle raising from causing negative consequences for biodiversity and ecosystem functions.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d16080467/s1, Figure S1: Pearson’s correlation test in vegetation structure and environmental variables collected in each distinct level of Restinga forest disturbance.

Author Contributions

Conceptualization, C.A.I. and M.C.G.; methodology, C.A.I., T.S. and M.C.G.; validation, C.A.I., T.S., M.C.G., M.S.G. and K.M.B.; formal analysis, C.A.I., M.S.G. and K.M.B.; investigation, C.A.I.; resources, C.A.I.; data curation, C.A.I.; writing—original draft preparation, C.A.I.; writing—review and editing, M.S.G. and K.M.B.; visualization, C.A.I., M.S.G. and K.M.B.; supervision, C.A.I.; project administration, C.A.I.; funding acquisition, C.A.I. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Data are contained within the article.

Data Availability Statement

The processed data and R codes are available at https://zenodo.org/records/12980854 (accessed on 01/08/2024).

Acknowledgments

The authors thank colleagues in the Laboratório de Ecologia de Lepidoptera and other friends who helped with the field expeditions. The authors are grateful to the staff of EMBRAPA for assisting during the sampling periods, to Luc Legal for the organization of the Special Issue “Biogeography and Diversity of Butterflies and Moths”, to two anonymous reviewers for critically reviewing and providing valuable contributions to the manuscript, and to André Victor Lucci Freitas and Thamara Zacca for help in the identification of Satyrini butterflies. Samples were procured under the ICMBio permanent license number 45673-1. This publication is part of the RedeLep National Network for Research and Conservation of Lepidoptera.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Map showing (A) Rio Grande do Sul State in southern Brazil and the studied area, highlighted in red; (B) the location of studied Restinga forests in Capão do Leão municipality; (C,D) the phytophysiognomy of the Restinga forest interspersed with native grasslands and cattle raising; (E) Restinga forest with low-level cattle trampling disturbance; (F) Restinga forest with medium-level cattle trampling disturbance; (G) Restinga forest with high-level cattle trampling disturbance.
Figure 1. Map showing (A) Rio Grande do Sul State in southern Brazil and the studied area, highlighted in red; (B) the location of studied Restinga forests in Capão do Leão municipality; (C,D) the phytophysiognomy of the Restinga forest interspersed with native grasslands and cattle raising; (E) Restinga forest with low-level cattle trampling disturbance; (F) Restinga forest with medium-level cattle trampling disturbance; (G) Restinga forest with high-level cattle trampling disturbance.
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Figure 2. Non-metric multidimensional scale analysis (stress = 0.182) of fruit-feeding butterfly assemblages in distinct levels of cattle trampling disturbance in Restinga forests, southern Brazil, showing the effects of vegetation structure and environmental variables.
Figure 2. Non-metric multidimensional scale analysis (stress = 0.182) of fruit-feeding butterfly assemblages in distinct levels of cattle trampling disturbance in Restinga forests, southern Brazil, showing the effects of vegetation structure and environmental variables.
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Figure 3. Fruit-feeding butterfly species indicators of distinct disturbance levels of cattle trampling in Restinga forests through the IndVal analysis. D, dorsal view; V, ventral view.
Figure 3. Fruit-feeding butterfly species indicators of distinct disturbance levels of cattle trampling in Restinga forests through the IndVal analysis. D, dorsal view; V, ventral view.
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Figure 4. (A) Fruit-feeding butterfly diversity in distinct levels of cattle trampling disturbance in Restinga forests through diversity profile calculated based on rarefied species richness (q = 0), evenness (q = 1), and dominance (q = 2). (B) Species abundance distribution curves of fruit-feeding butterflies in low, medium, and high levels of cattle trampling disturbance in Restinga forests. The colors refer to the different assemblages from high (orange), medium (blue), and low (pink) disturbance.
Figure 4. (A) Fruit-feeding butterfly diversity in distinct levels of cattle trampling disturbance in Restinga forests through diversity profile calculated based on rarefied species richness (q = 0), evenness (q = 1), and dominance (q = 2). (B) Species abundance distribution curves of fruit-feeding butterflies in low, medium, and high levels of cattle trampling disturbance in Restinga forests. The colors refer to the different assemblages from high (orange), medium (blue), and low (pink) disturbance.
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Table 1. Relative frequency of feces and average values for vegetation structure and for environmental variables in Restinga forests with distinct levels of cattle trampling disturbance in southern Brazil. The values are accompanied by the ± standard deviation.
Table 1. Relative frequency of feces and average values for vegetation structure and for environmental variables in Restinga forests with distinct levels of cattle trampling disturbance in southern Brazil. The values are accompanied by the ± standard deviation.
DisturbanceFeces (%)Understory Height (cm)Canopy Coverage (%)Temperature (°C)Humidity (%)
Low1 ± 0.4167.5 ± 11.181.4 ± 2.226.6 ± 1.972.1 ± 5.8
Medium32 ± 2.9115.5 ± 19.876.8 ± 1.125.5 ± 2.268.5 ± 3.7
High67 ± 2.942.5 ± 29.376.3 ± 1.327.3 ± 1.865.7 ± 4.6
Table 2. Associations among environmental and structural variables and species composition. The association of mean humidity with species composition is mainly positive (higher loadings on the MDS2 axis), while canopy cover and understory height are negatively related to the species composition (higher loadings on the MDS1 axis). Higher loadings, R2, and significant p-values are highlighted in bold.
Table 2. Associations among environmental and structural variables and species composition. The association of mean humidity with species composition is mainly positive (higher loadings on the MDS2 axis), while canopy cover and understory height are negatively related to the species composition (higher loadings on the MDS1 axis). Higher loadings, R2, and significant p-values are highlighted in bold.
Environmental and Structural VariablesMDS1MDS2R2p-Value
Mean temperature−0.30130.95350.08860.1339
Mean humidity−0.51130.85940.2780.002
Canopy cover−0.9213−0.38890.32330.002
Understory height−0.9987−0.05080.3610.001
Table 3. Indicator values for fruit-feeding butterfly species associated with the distinct disturbance levels of cattle trampling in Restinga forests in southern Brazil. A, specificity; B, fidelity; Bib, Biblidinae; Cha, Charaxinae; Sat, Satyrinae; Euni, Eunicini; Anae, Anaeini; Saty, Satyrini; Bras, Brassolini.
Table 3. Indicator values for fruit-feeding butterfly species associated with the distinct disturbance levels of cattle trampling in Restinga forests in southern Brazil. A, specificity; B, fidelity; Bib, Biblidinae; Cha, Charaxinae; Sat, Satyrinae; Euni, Eunicini; Anae, Anaeini; Saty, Satyrini; Bras, Brassolini.
Species (Subfamily, Tribe)IndValABp-Value
High level
 Eunica eburnea (Bib, Euni) 0.7590.7590.8870.001
Medium + high levels
 Cissia phronius (Sat, Saty)0.9710.9710.9420.001
 Zaretis strigosus (Cha, Anae)0.9400.9400.9650.001
 Opsiphanes invirae (Sat, Bras)0.8470.8470.8960.013
 Paryphthimoides poltys (Sat, Saty)0.8280.8280.9600.005
 Capronnieria galesus (Sat, Saty)0.8100.8100.9200.006
Table 4. Relationships among environmental and structural variables and the rarefied species richness, dominance, and abundance. Significant relationships are highlighted in bold. std. error = standard error; df = degrees of freedom.
Table 4. Relationships among environmental and structural variables and the rarefied species richness, dominance, and abundance. Significant relationships are highlighted in bold. std. error = standard error; df = degrees of freedom.
VariablePredictorEstimateStd. ErrorStatisticdfp-Value
RichnessMean temperature0.0180.0161.10812.8570.288
Mean humidity0.0060.0060.89426.5280.380
Canopy cover−0.0050.012−0.39037.2150.699
Understory height0.0000.001−0.43038.3420.670
DominanceMean temperature0.1610.1910.84422.7790.407
Mean humidity0.0810.0711.15235.3820.257
Canopy cover−0.1030.125−0.82736.8330.414
Understory height−0.0080.006−1.24237.3490.222
AbundanceMean temperature−0.0290.053−0.555 0.579
Mean humidity0.0460.0261.732 0.083
Canopy cover−0.1170.040−2.929 0.003
Understory height−0.0070.002−3.621 0.0003
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Iserhard, C.A.; Schwantz, T.; Gallo, M.C.; Gottschalk, M.S.; Bordin, K.M. Indirect Effects of Cattle Trampling on the Structure of Fruit-Feeding Butterfly Assemblages Inhabiting Restinga Forests in Southern Brazil. Diversity 2024, 16, 467. https://doi.org/10.3390/d16080467

AMA Style

Iserhard CA, Schwantz T, Gallo MC, Gottschalk MS, Bordin KM. Indirect Effects of Cattle Trampling on the Structure of Fruit-Feeding Butterfly Assemblages Inhabiting Restinga Forests in Southern Brazil. Diversity. 2024; 16(8):467. https://doi.org/10.3390/d16080467

Chicago/Turabian Style

Iserhard, Cristiano Agra, Taiane Schwantz, Mariana Centeno Gallo, Marco Silva Gottschalk, and Kauane Maiara Bordin. 2024. "Indirect Effects of Cattle Trampling on the Structure of Fruit-Feeding Butterfly Assemblages Inhabiting Restinga Forests in Southern Brazil" Diversity 16, no. 8: 467. https://doi.org/10.3390/d16080467

APA Style

Iserhard, C. A., Schwantz, T., Gallo, M. C., Gottschalk, M. S., & Bordin, K. M. (2024). Indirect Effects of Cattle Trampling on the Structure of Fruit-Feeding Butterfly Assemblages Inhabiting Restinga Forests in Southern Brazil. Diversity, 16(8), 467. https://doi.org/10.3390/d16080467

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