Large and medium-sized mammals in the urban park Cinturão Verde , Cianorte , northwestern Paraná

We surveyed the composition of large and medium-sized mammals in the urban park Cinturão Verde in the city of Cianorte, Paraná, Brazil. This urban reserve is an important regional corridor for wildlife. Data were collected monthly during seven months for six days with track plots, camera traps, and visual searches for animals and sign. Richness estimates were calculated using Chao 2 and ICE estimators. Nineteen species of mammals in seven orders and 14 families were recorded. Although the area displays a high degree of disturbance, it supports the presence of important species for the fauna of northwestern Paraná, including state, regional and globally threatened species.


INTRODUCTION
Faunal surveys remain critically important because any project linked to conservation or sustainable use requires a basic knowledge of the species composition and ecology of resident organisms (Scott et al. 1987).The ecological importance and elevated degree of threat of large and medium-sized mammals (Di Marco et al. 2014) make clear the need to include information about this group in inventories and environmental diagnostic studies (Pardini et al. 2003).Terrestrial mammals have a prominent role in the function of Neotropical ecosystems (Terborgh et al. 2001) and are essential to ecosystem processes even in small fragments.Herbivorous and frugivorous species play an important role in maintaining the diversity of forest trees as both seed dispersers and predators of seedlings (Dirzo and Miranda 1990), whereas carnivores regulate populations of herbivores and frugivores (Terborgh 1992;Terborgh et al. 2001).The loss of large and medium-sized mammals can provoke an entire series of trophic cascades (Estes et al. 2011).The main threats to terrestrial large and medium-sized mammals are habitat destruction, hunting, loss of critical resources and illegal trade (Schipper et al. 2008).Therefore the presence of viable populations of large and medium sized mammals may be excellent indicators of forest health.
There are 701 species mammals described for Brazil and 298 are found in the Atlantic Forest, 30% of them endemic (Paglia et al. 2012).This biome consists of multiple forested ecosystems, including tropical rain forest on the Atlantic slope, mixed Araucaria pine forests in the south, and deciduous and semideciduous forests to the west (Tabarelli et al. 2005).The entire biome has suffered significant deforestation and fragmentation (Ribeiro et al. 2009).
The semideciduous forests of southeastern Brazil, in particular in the state of Paraná, are among the most severely altered of this biome (Di Bitetti et al. 2003).There are few records of studies on mammal inventories in the forested fragments in the northwestern region of Paraná.Urban forest fragments are especially poorly studied; however, in the Atlantic Forest, these fragments may have higher richness and diversity of butterflies than urban parks and can serve as important reservoirs for more disturbance-tolerant species (Rodrigues et al. 1993).Research in temperate regions has shown the persistence of small and mid-body size predators in urban fragments (Crooks, 2002) which can help to maintain important ecosystem processes.
The Cinturão Verde Park in Cianorte, state of Paraná, is an important remnant of semideciduous forest, characterized by the absence of southern conifers and the partial loss of leaves in the dry season (SEMA 2010).In Paraná, this forest occurs in the western, northwestern and northern portions of the state (França and Archela 2008).The present study investigated the

Martins et al. | Paraná urban meso-mammals
Cfa, mesothermal humid subtropical, with hot summers, a concentration of rainfall in the summer months, winters with infrequent frosts, and no marked dry season (Cioffi et al. 1995).Data collection was focused on two modules within the park, the Fantasminha module which borders Rio Fantasminha and the Perobas module (Figures 1 and 2).The Perobas module is less disturbed than the Fantasminha module, however it is bordered and cut by several dirt roads (Figure 2), including one that links the city of São Tomé to Cianorte.

Data collection
In this study we considered as large and mediumsized mammals those weighing over 1 kg as adults, according to the system adopted by Chiarello (2000).
To survey mammals and estimate species richness we applied direct methods such as visual encounters and images on camera traps as well as indirect methods via recording tracks (Freitas and Silva 2005;Cullen Jr. et al. 2006;Oliveira et al. 2007;Srbek-Araujo and Chiarello 2007;Borges and Tomás 2008).We also examined specimens from the park deposited during the three years prior to this study in the Laboratory of Zoology, Universidade Paranaense, Campus Cianorte.Data collection for the survey of large and mediumsized mammals was conducted from September to December 2010 and from March to May 2011, with three days of sampling every 15 days, totaling six sample days each month.
species richness of terrestrial large and medium-sized mammals in the Cinturão Verde Park in Cianorte with intensive sampling to provide data for the conservation and maintenance of the park's natural ecosystems.

Study site
The Cinturão Verde Park in Cianorte, state of Paraná, southeastern Brazil, is a protected area composed of eight habitat fragments that surround the city of Cia norte, two of which were selected for this study (Figure 1).The park retains important components of regional biodiversity (Baldo and Silveira 2009).The area consists of approximately 312 ha around the coordinates 23°40ʹ S, 052°35ʹ W at 530 m elevation (Cianorte 2010).The park is one of the last regional remnants of typical seasonal submontane semideciduous forest with some influence of the Cerrado biome (Vazzoler et al. 1997).The vegetation has characteristics of modified mature forest in the interior but around the edges of the park there are many areas of highly degraded vegetation.Characteristic plant species in the park reflect a combination of components of the Brazilian Atlantic Forest and vegetation typical of disturbed areas with invasive species.Some typical species include Aspidosperma polyneuron, A. ramiflorum, Cedrella sp., C. brasiliensis, Nectandra puberula, Citrus sinensis, Tabebuia sp., Piper sp., Machaerium sp., Hyme naea sp., Achromia aculeata, Solanum sp., and Galesia sp.(Cioffi et al. 1995).The climate is classified as Köppen

Mammal track methods
We established sand plots and sampled the sand banks on the Fantasminha River and dirt roads within and around the park.We installed 20 sand plots, 10 in the Fantasminha Module and 10 in the Perobas Module.Each sand plot represented a sample point and was placed approximately 100 m from adjacent plots.All plots were standardized at 60 cm × 60 cm with sand fill 20 cm deep.To prepare the plots, the sand was loosened and moistened with a spray of water.Plots were baited with banana, orange, pineapple and bacon.Sand plots were inspected daily in the morning.Total sample effort was 840 sand plot-nights (20 plots, 6 days/month for 7 months).
Samples on sand banks of the Fantasminha River and on dirt roads were carried out simultaneously with the sand plots (Rudran et al. 1996;Araújo et al. 2012).We looked for footprints on the river sand banks and the roads during two days each month, totaling 14 days over seven months of sampling.
The tracks were measured with a ruler and photographed.Tracks were identified using field guides (Becker and Dalponte 1991;Oliveira and Cassaro 2006;Borges and Tomás 2008;Carvalho Jr. and Luz 2008;Moro-Rios et al. 2008).Plaster molds of tracks in good condition were prepared for further analysis (Borges and Tomás 2008).Plaster molds were cataloged and deposited in the collection of the Laboratory of Biology, Study Group in Mammalian Ecology and Environmental Education (GEEMA) from the State University of Maringá, Campus Goioerê.

Camera traps and visual methods
Three Bushnell ® camera traps were positioned 300 m apart from each other and 30 cm above ground installed on tree trunks.The equipment was placed only in the Perobas module for security reasons.We baited the camera trapping points (bacon, banana, pineapple and oranges) to lure the animals (Cullen Jr. et al. 2006).
Traps were positioned at strategic points, such as near burrows, possible tracks and waterways.Over the study we accumulated 126 camera-days (3 traps × 6 days × 7 months).
The species recorded by the camera traps were easily recognized, however doubts were clarified with the aid of Reis et al. (2011a) and Patrocínio (2009).The photos were also cataloged and deposited in the collection at the Laboratory of Biology, Universidade Paranaense, Campus Cianorte.

Data analysis
Species richness was estimated using program EstimateS version 8.2 (Colwell 2006).Analyses were conducted in classic mode using sampled-based incidence data and the Chao 2 and ICE indices were used for estimation of species richness.We based richness estimates on eight sampling periods: recently collected specimens followed by the seven additional field sampling periods.Data on frequency of observations by species and sampling method were analyzed using descriptive statistics and represented in percentages.Conservation status was determined globally (IUCN 2015), for Brazil (Chiarello et al. 2008), and for Paraná (Mikich and Bérnils 2004).

RESULTS
We gathered a total of 198 records of 19 species of large and medium-sized native or exotic terrestrial mammals from seven orders and 14 families (Table 1).Three species were collected in the three years prior to our survey and deposited in the collection at the Laboratory of Biology, Universidade Paranaense, Campus Cianorte (Appendix, Figure A1): Procyon cancrivorous (2007), Leopardus guttulus (2007), andCoendou spinosus (2008).All were killed on roads in or adjacent to the park.Only C. spinosus was not recorded during the sampling period.Four other specimens were collected during the study (Appendix, Figure A1): Eira barbara (7 November 2010), Tamandua tetradactyla (14 December 2010),  (Chiarello et al., 2008), Paraná status (Mikich and Bérnils, 2004).Site: Fantasminha (F), Perobas (P).(10 May 2011).We considered all collected specimens as valid records for the richness estimation.We excluded feral domestic dogs from the richness estimates and from the final species tally.The richest orders were Carnivora (six species, 31.6%) and Rodentia (five species, 26.3%), followed by Cingulata, Lagomorpha, and Didelphimorphia (two species, 10.5% each).Pilosa and Primates were represented by only one species each (5.3%).Richness estimates generated by the Chao 2 method (n = 26.17)and the ICE method (n = 25.56) were somewhat higher than the observed richness curve for the study area (Figure 3).The observed richness tracked the lower confidence interval closely.

DISCUSSION
There are few studies on faunal surveys in northwestern Paraná.Rocha-Mendes et al. (2005) recorded 39 species in three fragments totaling 703 ha in the city of Fênix based only on interviews with local residents.Another survey, using 248 sand plots and yielding 10 species, was conducted during four days in a forest fragment of approximately 382 ha, near the city of Umuarama (Oliveira et al. 2012).According There were 92 records in all the sand plots representing 46.5% of the total records obtained (Appendix, Figure A2).Of the species identified, the species most frequently recorded were Didelphis sp. with 22 occurrences.We recorded tracks of Leopardus guttulus, listed as globally vulnerable as L. tigrinus (Trigo et al. 2013;IUCN 2015), for which the presence was confirmed by a specimen deposited at the Laboratory of Zoology, Universidade Paranaense, Campus Cianorte, that was collected as roadkill in 2007.Tracks on river sand banks and on the dirt roads accounted for 32.8% of the total records.Hydrochoerus hydrochaeris and Procyon cancri vorus tracks were observed both along the river and on dirt roads in both modules.Puma yagouaroundi was recorded on tracks and on dirt road but only in the Fantasminha module (Table 2).
We made 16 visual observations representing 8.1% of the total records.Taxa observed most frequently were Sapajus nigritus and Nasua nasua, observed on both modules and along the river.Two other species sighted were Sylvilagus brasiliensis in both modules and Euphractus sexcinctus in the Perobas module.The camera to Rocha-Mendes et al. (2005), the number of species recorded was satisfactory, based upon the sampling effort employed; however, the fragment was in a rural area, much less disturbed than our site.Cinturão Verde Park is located in and around the city of Cianorte, under intense anthropogenic impacts marked by landfills, erosion, sewage, invasive plant species, the presence of domestic animals, and significant edge effects.The more irregular and smaller the fragment, the greater the area of contact with the surrounding matrix of development and associated microclimatic changes (Laurance and Bierregaard 1997), reducing or eliminating sensitive populations of forest species (Hero and Ridgway, 2006).
This makes it all the more surprising that we recorded as many species as we did in our surveys and the richness estimator indicated that the park may support approximately 26 species.The results suggest that the inventory for the park attained 73% of the estimated richness for the area.The 19 species represent 7.6% of total recorded for the Atlantic Forest and 47.5% of the 40 species of large and medium-sized mammals anticipated for the northwestern region of Paraná  (Mikich and Oliveira 2003;Instituto Pró-Carnívoros 2011;Reis et al. 2011a).Our study recorded species that had not yet been identified for the area, including one globally threatened species and two threatened at the state level (Table 1).
The Perobas module plots obtained more records than those installed in the Fantasminha module.Perobas is larger and less disturbed; other studies also reveal higher richness in larger and less disturbed Atlantic Forest fragments (Fonseca 1989).There are also several dirt roads that surround and cut through Perobas, but they also connect this fragment with several others and perhaps serve as an "ecological stepping stone" for animals to move between fragments (Reis and Tres 2006).Most species recorded in the Fantasminha module were generalists, indicating that this fragment has a higher degree of degradation.We observed a constant presence of domestic waste and signs of human activity on the trails and in the river, as well as the presence of invasive plant species.

Most commonly recorded species: disturbance-tolerant and invasive species
According to Rossi et al. (2006), two species of opossum, Didelphis albiventris and D. aurita, occur in the state of Paraná.These species can be distinguished easily by ear pigmentation (Silva 1994) but not by footprints.Therefore, in this study, only the genus is documented and not species..The high number of records was expected because marsupials are quite tolerant of human habitation and their tracks and signs can be found in residential areas (Becker and Dalponte 1991).A second abundant species, the diurnal N. nasua, was detected by nearly all methods.Dasypus novemcinctus also was common, with 12 records in sand traps and 20 additional records via other methods.Although this armadillo is hunted, it remains common and widely distributed in Brazil (Aguiar 2004).
Of note is the high number of records of Canis familiaris (domestic dog) found in sand plots and camera traps, which were often full of their images.This species can be very destructive by consuming the prey of wild carnivores, transmitting diseases, and hunting and killing many species of wildlife (Negrão and Valladares-Padua 2006).

Most uncommonly recorded species
There were six records of Eira barbara prints in the sand traps.There were no previous records of this species in the park.Hydrochoeris hydrochaeris is the largest living rodent (Reis et al. 2011a) and its tracks were only observed outside the sand plots, as were P. cancrivorus and P. yagouaroundi.Of tracks identified outside of the sand plots, most were along the river; this watercourse is the only one within the park, so animals likely use it as a water source.The tracks of small felines are very similar and difficult to identify; however, the record of P. yagouaroundi was possible to confirm because the smaller felids occurring in the state of Paraná (excluding L. pardalis) are L.wiedii, L. guttulus and P. yagouaroundi).Of these three species P. yagouaroudi is most distinctive because the palmar pad has a somewhat triangular ovate shape with three ripples in the heel and the impression of the four fingers is rounded in the form of a semicircle in front of the pad (Moro-Rios et al. 2008).

Species of conservation concern
Leopardus guttulus is the smallest cat species in Brazil, having body proportions similar to the domestic cat (Oliveira and Cassaro 2006).This cat is considered a flagship species that can be used in public relations to rally protection for areas and other animals (Chiarello et al. 2008).L. guttulus is also considered an umbrella species (Schonewald-Cox et al. 1991;Roberge and Angelstam 2004) whose conservation can provide protection to a large number of species that naturally occur in the same area (Indrusiak and Eizirik 2003).There might be some question as to the identification of this species; however, there was no other possible match to the tracks other than domestic cats.We discarded the possibility of domestic cats since none were ever seen during the study, either inside or adjacent to the park and never captured in any camera trap images (where many feral domestic dogs were observed).We are also confident in what we felt was a very careful analysis of the characteristics of the tracks we observed.There is also a 2007 record of a roadkill from the park.This species is threatened due to hunting for their fur, animal trafficking and the loss of habitat (Mikich and Bérnils 2004).Sylvilagus brasiliensis and Cuniculus paca, are listed as vulnerable and endangered, respectively, for the state of Paraná (MMA 2008).The large increase in populations of L. europaeus, an introduced species (Reis et al. 2011b), is a major reason for inclusion of S. brasiliensis in the vulnerable category.Cuniculus paca is threatened and declining due to hunting as a game species and a decrease in the quality and extent of its habitat (Mikich and Bérnils 2004).The only primate observed was (Sapajus nigritus), but it was recorded in high numbers with all methods.This species is diurnal (Becker and Dalponte 1991) and has a large population in the park.This primate is listed as globally Near Threatened by the IUCN (2015).

Historical data
We also consulted the collection of specimens de pos ited at the Laboratory of Zoology, Universidade Paranaense, Campus Cianorte for historical records.Of the 19 taxa identified in this study, of them (L.europaeus, T. tetradactyla and C. spinosus) were included in the list of species with records in the teaching collection.These animals were roadkilled on the streets and highways surrounding the study area in the three years prior to the study and were collected and archived at the university.Besides these specimens cited, there is a specimen of Lontra longicaudis in this collection, but despite many reports of the occurrence of this animal fishing near the Cinturão Verde Park, the record was not considered valid due to an unconfirmed collection locality.It is likely that this species, as well as Pteronura brasiliensis, occasionally use nearby locations due to the large populations of fish and ease of hunting in dammed areas of the watershed.Within the conservation area there is only a narrow and shallow waterway so that L. longicaudis and P. brasiliensis likely rarely traverse the park.The high levels of disturbance and regular human activity also likely explain the absence of Puma concolor, Leopardus pardalis, Chrysocyon brachyurus and other less common larger mammals, which might be found in this region.
These results contribute to the knowledge of the biology of mammals in the northwestern region of Paraná state.The information obtained suggests the need for implementation of improved conservation strategies focusing on the importance of minimizing impacts in the area and eliminating invasive species.Previous research on faunal collapse in forest fragments has shown that a failure to maintain predator populations can result in large population increases of herbivores, resulting in significant plant community impacts (Terborgh et al. 2001;Estes et al. 2011).Recent research has highlighted the equally severe consequences of the depletion of large and medium-sized herbivores (Ripple et al. 2015).The remaining relatively high species richness of large and medium-sized mammals in the region can likely be conserved with improved management of this urban wildlife corridor, which will in turn maintain the ecological processes associated with these forest fragments.

Figure 1 .
Figure 1.Location of the city of Cianorte in the state of Paraná, with and a satellite image (Googe Earth™) of the city of Cianorte, Paraná, Brazil showing the distribution of the units of the Parque Cinturão Verde surrounding the city.

Figure 2 .
Figure 2. Schematic locations of the collection points, sand traps, and camera traps in the Fantasminha module and along the Rio Fantasminha (1),

Figure 3 .
Figure 3. Observed and estimated richness of the large and medium size mammals of the Cinturão Verde Park.Graph presents observed richness against two estimates, ICE and Chao 2. Only the 95% confidence intervals for Chao 2 are shown to minimize clutter.

Table 1 .
Medium and large size terrestrial mammals from the Cinturão Verde Park in Cianorte, state of Paraná, southeast of Brazil.Legend -IUCN status: IUCN (2015), Brazil status Martins et al. | Paraná urban meso-mammals

Table 2 .
Number of observations by method of data collection for all species of large and medium-sized mammals recorded in the Cinturão Verde Park in Cianorte, state of Paraná, southeast of Brazil, from September to December 2010 and March to May 2011.Domestic dogs were very abundant everywhere, but their numbers are not included, nor was the roadkill of Myocastor.Legendfor observations: sand tracks (ST), river tracks (RT), dirt road tracks (DT), camera trap (CT), visual observation (VO), and specimens from collections (MS).
* The presence of two species was confirmed by visual observation, however they can only be identified to genus by tracks, thus observations are merged.Martins et al. | Paraná urban meso-mammals