Research Article |
Corresponding author: Fernando Ferreira de Pinho ( fernandopinho@biotropicos.org.br ) Academic editor: Diego Astúa
© 2017 Fernando Ferreira de Pinho, Guilherme Braga Ferreira, Adriano Pereira Paglia.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
de Pinho FF, Ferreira GB, Paglia AP (2017) Influence of vegetation physiognomy, elevation and fire frequency on medium and large mammals in two protected areas of the Espinhaço Range. Zoologia 34: 1-11. https://doi.org/10.3897/zoologia.34.e11921
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The objectives of this study were to determine the richness of medium and large mammal species in two protected areas of the Espinhaço Mountain Range, state of Minas Gerais, Brazil; and to investigate the factors affecting the occurrence of those species. To accomplish that we placed 49 camera traps activated by heat and motion at Rio Preto State Park (RPSP) and 48 at Sempre Vivas National Park (SVNP). We also collected data on three environmental variables: vegetation physiognomy, elevation and wildfire frequency, to evaluate the influence of these factors on species richness and use intensity (inferred from camera trap detection rate) by large mammals. We recorded 23 large mammal species in the two parks combined. The lowest species richness was found at the rupestrian habitat of RPSP, and in the open grasslands of SVNP. The forest and savannah physiognomies were used more intensively by large mammals. Species richness was higher and use was greater at lower elevations of RPSP. In SVNP, fire frequency did not affect species richness or use intensity. The savannah habitat had very similar richness compared to the forests of the two protected areas. The high species richness and use intensity observed in these forest habitats highlights the importance of riparian environments in the Cerrado biome. The highest species richness and use intensity observed at low elevation follows patterns found in the literature, probably due to variation in the vegetation, which results in greater resource availability. Although rupestrian habitats at high elevations of the Espinhaço Range are known to have a high degree of endemism for some taxa, large mammal richness and use were not high in this habitat. These results indicate that the protection of native vegetation at lower elevations is crucial for the long-term conservation of large mammals in the Espinhaço Range.
Cerrado, campo rupestre, species richness, use of habitat, wildfire
Understanding which factors affect species richness is a challenge for ecologists. Resource availability in the ecosystem, the degree of specialization of species and the coexistence of species that share the same resources are key determinants of local species richness (
Habitat heterogeneity also allows the coexistence of competitor species, therefore contributing to local species richness. For example,
Several studies have investigated how biotic and abiotic features affect mammal distribution (e.g.,
In the Brazilian Cerrado, gallery forests are known to play an important role in mammal distribution, as they provide unique resources within the ecosystem (
Considering the high environmental heterogeneity found in the Cerrado and the relevance of protected areas for the conservation of large mammals, the objectives of this study were to determine large mammal species richness in two protected areas (PAs) of the Espinhaço Mountain Range and to investigate the factors affecting the occurrence of these species. We hypothesized that large mammal species richness and intensity of use would be higher in more complex habitats, in lower elevation, and in areas that are less frequently affected by fires.
The Espinhaço Mountain Range is one of the most important Brazilian biogeographic regions. It extends over parts of three major ecosystems: Caatinga, Cerrado and Atlantic Rainforest, the last two being recognized as global biodiversity hotspots (
The Espinhaço Mosaic (Mosaico do Espinhaço: Alto Jequitinhonha-Serra do Cabral, as it is called in Portuguese) is composed of seven strict PAs (IUCN categories I–IV) and five multiple-use PAs (Area de Proteção Ambiental; IUCN category V) located in the southern portion of the Espinhaço Range. Most of this mosaic is within the Cerrado ecosystem, whereas the Atlantic Forest covers its eastern-most portion. Due to its irreplaceability, the Espinhaço Mosaic has been recognized as a priority area for conservation (
Established in 1994, RPSP encompasses an area of 121 km2 covered mostly by open vegetation such as ‘campos rupestres‘ (rocky outcrops covered by scattered herbs, grasses and shrubs) and savannah, but also with gallery forests bordering water courses. There is a broad elevational gradient in the park, ranging from 750 to 1,800 m asl. Due to the fact that this reserve was established two decades ago, and that it is very effectively managed (
Sempre-Vivas National Park was established in 2002 and covers an area of 1,241 km2 The main vegetation physiognomies in SVNP are campos rupestres and open grasslands, but there are also portions of savannah, veredas (a humid grassland dominated by the palm species Mauritia flexuosa L. f.), dry forests and gallery forests. The elevation ranges from 650 to 1,525 m asl. However, due to SVNP’s large area and logistical constraints, sampling was limited to between 1,000 and 1,400 m asl, including most of the park’s vegetation physiognomies, but not veredas and dry forests normally associated with lower elevation. Within the limits of SVNP there are several land-use issues that result in anthropogenic impacts (such as poaching, wildfire and fuelwood collection). Wildfires are frequently detected in this PA (
We used camera traps activated by heat and motion (Bushnell Trophycam) to study the large mammal community. The sampling design followed recommendations from
In the field, we used a GPS unit to navigate to the potential sites and establish the camera trap within a 100 m radius from the predetermined location, choosing the spots with the highest probability of recording medium and large mammal species. Due to difficult access conditions, in four occasions at RPSP and in two occasions at SVNP camera trap were established out of the 100 m radius, but within a 250 m radius. Additionally, we had to relocate two potential sites at RPSP, because we were unable to reach them (e.g. cliffs). As a result, these two sites were established at a distance of 1.2 km of the nearest neighboring site.
In total we set up 51 camera trap sites at RPSP (including three sites at an adjacent private reserve) and 55 at SVNP, however, due to malfunctioning of some camera trap units, the final number of sites used in the analysis was 49 at RPSP and 48 at SVNP (Fig.
Considering our hypothesis, we collected data on three environmental variables: (1) vegetation physiognomy, (2) elevation and (3) wildfire intensity. Physiognomy was assigned to four possible categories: forest (gallery forest or capão forest), savannah (small trees and shrubs with a herbaceous layer), open grassland (with or without scattered trees) and rupestrian habitat (campos rupestres or rock outcrops with scattered vegetation). Elevation was measured in the field using a GPS unit. Wildfire frequency was extracted from a Kernel Map provided by PA management team, which was produced using data available from
We built a matrix of independent camera trap records of large mammals for each PA. When there were two records of the same species in a single sampling site we assumed them to be independent if the observations were at least 24hs apart. We used the software EstimateS 9.1.0 (
To assess the effect of the Cerrado physiognomies on species richness, we grouped the records from each vegetation physiognomy (forest, savannah, grassland, rupestrian). Since there were large differences in sampling effort between physiognomies, the rarefaction function provided estimates with very broad CIs. For this reason, we decided to perform the comparison, controlling for the physiognomy with the smallest sampling effort (forest in both parks). Therefore, we obtained the average species richness in each physiognomy based on 452 and 420 sampling days/physiognomy at RPSP and SVNP, respectively. We checked for overlap between the 95% CI for each estimate to infer statistical significance. Additionally, as an overall measure of large mammal use, we grouped the independent records from all large mammal species within a physiognomy (overall photographic rate) and compared them through an analysis of variance (ANOVA). Although we cannot consider the overall photographic rate as a measure of abundance, we used this rate as a measure of the intensity of use by large mammals, in which a large number of independent records represents high use intensity of a given area. This analysis was performed for each park independently.
The effect of elevation on species richness was only assessed for RPSP, since the elevation variation of the sampling sites at SVNP only ranged from 1,041 to 1,369 m asl. In RPSP the difference between the lowest and highest sampling site was almost 1,000 m (range: 800–1,720 m asl). Following a well-established classification used by the park‘s management team, we divided the RPSP into two regions according to elevation: below 1,000 m asl and above 1,200 m asl. This division reflects markedly different environments, where low elevation sites are dominated by savannah and forest habitats and high elevation sites are normally located in grasslands or rupestrian habitats. We thus grouped data from all sites at low (<1,000 m) and high elevation (>1,200 m), eliminating those sites established between 1,000–1,200 m asl. Species richness estimates with 95% CI was obtained for each region controlling for differences in sampling effort. To evaluate the intensity of use by large mammals we grouped the independent records from all species in low and high altitudes and compared them through independent T-tests.
Finally, we used linear regression to assess the effect of wildfire frequency on species richness and use intensity (defined as average records of all species of medium and large mammals) at SVNP. We excluded RPSP from this analysis because wildfires are rare in this park and there have been no occurrences of it in at least the last five years. To represent wildfire frequency in the sampling site, we extracted the value derived from the Kernel Map (see Data collection) for the pixel where the camera trap had been set. The average species richness and use intensity at the site level, controlling for differences in sampling effort, were obtained for all sites surveyed for more than 30 days at SVNP.
We recorded 23 large mammal species in the two parks combined, 19 at RPSP after 2,865 sampling days and 18 at SVNP after 2,010 sampling days (Table
The observed species richness was statistically lower in rupestrian habitats than other vegetation physiognomies in RPSP (Fig.
At lower elevations, species richness (Fig.
Mammal species recorded at Rio Preto State Park (RPSP) and Sempre Vivas National Park (SVNP).
Taxonomic group | Popular name | RPSP | SVNP |
Pilosa | |||
Myrmecophagidae | |||
Tamandua tetradactyla (Linnaeus, 1758) | Southern-anteater | x | x |
Myrmecophaga tridactyla Linnaeus, 1758 | Giant-anteater | x | x |
Cingulata | |||
Dasypodidae | |||
Dasypus sp. | Armadillo | x | x |
Cabassous unicinctus (Linnaeus, 1758) | Naked-tailed armadillo | x | |
Euphractus sexcinctus (Linnaeus, 1758) | Yellow-armadillo | x | x |
Priodontes maximus (Kerr, 1792) | Giant-armadillo | x | x |
Carnivora | |||
Canidae | |||
Cerdocyon thous (Linnaeus, 1766) | Crab-eating fox | x | |
Chrysocyon brachyurus (Illiger, 1815) | Maned-wolf | x | x |
Lycalopex vetulus (Lund, 1842) | Hoary-fox | x | |
Mephitidae | |||
Conepatus semistriatus (Boddaert, 1785) | Striped hog-nosed skunk | x | x |
Mustelidae | |||
Eira barbara (Linnaeus, 1758) | Tayra | x | x |
Felidae | |||
Puma yagouaroundi (É. Geoffroy, 1803) | Jaguarundi | x | x |
Leopardus pardalis (Linnaeus, 1758) | Ocelot | x | x |
Leopardus tigrinus (Schreber, 1775) | Oncilla | x | x |
Puma concolor (Linnaeus, 1771) | Puma | x | |
Procyonidae | |||
Procyon cancrivorus (G. Cuvier, 1798) | Crab-eating raccoon | x | |
Nasua nasua (Linnaeus, 1766) | Coati | x | x |
Perissodactyla | |||
Tapiridae | |||
Tapirus terrestris (Linnaeus, 1758) | Tapir | x | |
Artiodactyla | |||
Cervidae | |||
Mazama gouazoubira (G. Fischer, 1814) | Gray-brocket | x | x |
Tayassuidae | |||
Pecari tajacu (Linnaeus, 1758) | Collared-peccary | x | |
Rodentia | |||
Cuniculidae | |||
Cuniculus paca (Linnaeus, 1766) | Spotted-paca | x | x |
Dasyproctidae | |||
Dasyprocta sp. | Agouti | x | |
Caviidae | |||
Hydrochoerus hydrochaeris (Linnaeus, 1766) | Capybara | x |
Total species richness recorded here represents 70% and 55% of all large mammals known to occur at the Espinhaço Range (
The high species richness and use intensity observed in forest habitats highlight the importance of riparian environments in the Cerrado, which may provide essential resources for mammals, especially during the dry season (
The species richness in savannah and forest habitats was very similar in the two PAs studied. Some studies show that the mammal community of riparian forests appears to be more similar to the savannah than to any other physiognomy of the Cerrado (
The species richness found in rupestrian habitats of RPSP was much lower than in the other vegetation physiognomies, whereas in SVNP species richness in this habitat was reasonably high – higher than in the grasslands and not varying significantly in relation to forest and savannah. This variation may be due to the specific characteristics of the PAs. Due to the greater elevational gradient of RPSP the rupestrian environments in this park are, in general, steeper, which can make it difficult for the animals to move. In SVNP the elevational variation between rupestrian environments and other vegetation physiognomies are milder and less steep (at least in the survey area), facilitating displacement in these environments in the PA. The variations in species richness between physiognomies (especially in RPSP) could be attributed to differences in productivity, habitat complexity, and protection against predators among them. Areas that are more productive tend to have higher species richness (
The frequency of records between physiognomies indicated clear variations in the use of different environments. The high amount of records in forests suggests that these environments are more intensely used by wild mammals. Forest habitats play an important role in mammal diversity in the Cerrado, as they provide refuge for several species and, generally, have more food and water available (
The higher species richness and intensity of use in lower elevations was expected. The decline in richness due to increasing elevation is widely accepted as a general standard (
Although the maximum elevation of RPSP (not exceeding 2,000 m) is insufficient for direct effects on the medium and large mammal fauna, it is certainly sufficient to change the vegetation structure and can thus indirectly influence their distribution. The elevational gradient has traditionally been used as a substitute for productivity, with the assumption that at higher elevation the environmental conditions contribute to lower productivity (
The absence of effects of wildfire frequency on species richness and use intensity is likely a result of the adaptation of Cerrado plant species to this characteristic of the biome.
Two main aspects need to be considered in order to understand the influence of fire on the fauna: frequency and intensity. Infrequent fires result in a large accumulation of biomass. When the area eventually catches on fire, it is much more intense, with larger flames, higher temperatures and lasts longer (
Even though the Espinhaço range is recognized as an important center for species endemism in Brazil (
A global analysis revealed that PAs networks are generally established on higher elevations, steeper slopes and greater distance from urban centers, limiting their ability to avoid natural habitat conversion (
In this study we found that the evaluated PAs are home to a significant portion of the known medium and large mammals of the Espinaco Range. The SVNP, however, is one of the PAs of the Espinhaço that still suffers from anthropogenic pressures. Because this national park is the largest PA in the Espinhaço Mosaic and the second largest in the Espinhaço Range, it is essential to eliminate these pressures in order to maintain the high diversity of mammals in the region. In recent years some groups have joined efforts for the re-categorization (downgrading) of SVNP from a strict PA to a multiple-use PA. From a conservation point of view, this would be a major setback for the biodiversity of the Espinhaço Range and we emphasize that priority must be given to effective regulation and implementation of the strict PAs for the conservation of numerous threatened species.
Funding was provided by CNPQ (SISBIOTA Program, process 563134/2010-0 and PPBIO Program, process 457434/2012-0). FAPEMIG provides a scholarship to FFP and CNPQ to GBF (process 207195/2014-5). FFP and APP are also affiliated to Programa de Pós Graduação em Ecologia de Biomas Tropicais at Universidade Federal de Ouro Preto. GBF is also affiliated to the Centre for Biodiversity and Environment Research at University College London and the Institute of Zoology at the Zoological Society of London. Marcell Soares Pinheiro assisted with fieldwork. We are grateful to staff of RPSP and SVNP for helping with field logistics, and IEF-MG and ICMBio for the research permit.