Small mammals from the lasting fragments of Araucaria Forest in southern Brazil: a study about richness and diversity

ABSTRACT

Rodents and marsupials together, form the most rich group of mammals in Brazil, they are distributed in all biomes, including Atlantic Forest, and can be used to analyze environmental quality. The Araucaria Forest is a threatened formation of the Atlantic forest with few areas remaining intact and a huge lack of knowledge about the potential of its secondary forest fragments to act as habitat refuges to native fauna. This study evaluated the species richness and diversity of non-volant small mammals among five vegetation types within a protected area in an Araucaria Forest area from southern Brazil. The sampling was made in six bimonthly campaigns during a year, by pitfall and live traps. This effort resulted in 875 captures of 625 individuals from 16 species. The most common species in Pine Plantation was Oligoryzomys nigripes, in Natural Regeneration forest was Thaptomys nigrita and Akodon montensis was most often captured in the other vegetation. Although differences in species composition were found among the different vegetation types, there was no significant difference in species richness. Nevertheless, true diversity values were significantly lower in the Pine Plantation. The results demonstrated that the substitution of native for exotic vegetation generated a negative impact on the group diversity. More studies, in other Araucaria Forest areas are necessary to allow better understanding of the processes driving this loss of diversity in this biome threatened by antropic action.

KEYWORDS
Didelphimorphia; Mixed Rain Forest; Sigmodontinae; species composition

The Atlantic Forest in considered a world’s hotspot for biodiversity (Myers et al., 2000). Originally, the Brazilian Atlantic Forest covered 1227600 km² but after years of urbanization, industrialization, and agricultural expansion the biome was reduced to 28% of its original area (Myers et al., 2000; Rezende et al., 2018).

Ombrophilous Mixed Forest, or Araucaria Forest, is an Atlantic Forest formation, characterized by the predominance of Brazilian pine (Araucaria angustifolia) in the upper stratum. It occurs mainly in the Brazilian Southern Plateau, above 500-600 meters of altitude, in Paraná, Santa Catarina and Rio Grande do Sul states (MMA, 2010). Originally, this sub-region covered 253793 km² and, in 2009, it was narrowed to 32021 km² (12.6%) of fragmented patches and only 3.1% of that are located within protected areas (Ribeiro et al., 2009), current this number can be even lower. Because of its management history few areas remain intact and little is known about the potential of the secondary forest fragments to act as habitat refuges to native fauna.

As the most rich group of mammals in Brazil (Paglia et al., 2012), non-volant small mammals has been investigated for responding to different forms of environmental impacts as agricultural and mining activities, fragmentation and loss of habitat complexity (Martin et al., 2012; Ardente et al.; 2016; Paise et al., 2020; Hannibal et al., 2020), therefore they can be used to analyze environmental quality. This group is formed by Sigmodontinae rodents and Didelphimorphia marsupials because they weigh less than 2 kg and are captured and studied by similar methods (Voss & Emmons, 1996; Eisenberg & Redford, 1999).

In the present study we used non-volant small mammals to compare assemblages from five secondary vegetation physiognomies in Piraí do Sul National Forest, a forest mosaic inserted in a matrix of forestry and livestock, located in the Araucaria Forest domain. Recently two rodent species, Juliomys ossitenuis and Bibimys labiosus, were recorded for the first time in this locality expanding their knowing home ranges (Grazzini et al., 2015a,b) and suggesting Piraí do Sul National Forest to be an interesting refuge not studied enough. This National Forest has areas in different conservation contexts such as Araucaria angustifolia reforestation, Pinus elliottii plantation, and native Araucaria Forest in different successional stages which allowed us to assess how much diversity each vegetation retained after its unique management history.

Based on the fact that in a semi-deciduous mosaic area of ​​the Atlantic Forest, the low diversity of small mammals in the Eucalyptus plantation indicates that these homogeneous plantations have low aptitude for endemic species (Umetsu & Pardini, 2007). Our hypothesis is that (1) the planting of exotic trees (here Pinus elliotti) will be the least suitable area for the native fauna of the Araucaria Forest and will present the least wealth and diversity among the sampled areas and (2) due to its homogeneous characteristic, reforestation with Araucaria angustifolia will be less diverse than natural regeneration.

MATERIALS AND METHODS

Study area. The study took place in the Piraí do Sul National Forest (“Floresta Nacional de Piraí do Sul”, hereafter SPNF) (24°38ʼ01ˮS, 49°53ʼ25ˮW) (Fig. 1). SPNF is a conservation unit for sustainable use in the state of Paraná, southern Brazil, located in areas of Forest with Araucaria and covers an area of ​​approximately 153 ha.

Fig. 1.
Location and vegetation types where small mammals were sampled between November 2012 and September 2013, at Piraí do Sul National Forest, Paraná state, Brazil (A, Pine Plantation; B, Riparian Forest; C, Araucaria Plantation; D, Natural Regeneration forest; E, High Altitude forest). Original distribution of Atlantic Forest biome (light gray) and Araucaria forest (dark gray).

Sampling of non-volant small mammals took place in five sites representative of the vegetation classes within SPNF. These vegetation classes were defined as: (1) Pinus elliotti reforestation (Pine Plantation or PP), (2) natural regenerating Riparian Forest (RF), (3) Araucaria angustifolia reforestation (Araucaria Plantation or AP), (4) naturally regenerating secondary Ombrophilous Forest (Natural Regenerationor NR) and (5) Early-stage high altitude forest (HA) (Fig. 1).

The Pine Plantation comprised trees planted 30 to 40 years ago and has never been managed. It has a semi-structured understory with practically nonexistent herbaceous extract and soil covered by the needles of the species.

The Riparian Forest is anearly- to mid-successional secondary forest bordering a river (approximately 2 m wide). The IBGE (2012) classifies this as Mixed Flooded Ombrophilous Forest (“Floresta Ombrófila Mista Aluvial”). The species composition can vary greatly according to geographic location and elevation. At higher elevations Podocarpus lambertii and Drimys brasiliensis are found, and as the altitude decreases, Araucaria angustifolia is associated with several Angiosperm ecotypes dominated by the Lauraceae family, with a prominence of Ocotea, Cryptocarya and Nectandra. In southern Brazil this formation is dominated by Araucaria angustifolia, Luehea divaricata, Blepharocalyx salicifolius and Sebastiania commersoniana (IBGE, 2012).

The Araucaria Plantation also contains 30 to 40 year old trees and is characterized as a medium successional stage. The richest families (with almost 40% of the species) are Flacourtiaceae, Lauraceae, Rubiaceae and Aquifoliaceae. The families with most individuals (excluding Araucariaceae) are Flacourtiaceae, Aquifoliaceae, Rubiaceae and Lauraceae, with nearly half the sampled angiosperms. The most representative species in the forest structure, after Araucaria angustifolia are Casearia sylvestris, Ilex paraguariensis and Rudgea jasminoides (Moro et al., 2009).

The Natural Regeneration forest is at a mid successional stage. The families with higher species richness (accounting for almost half of the species found) are Lauraceae, Myrtaceae, Sapindaceae, Rubiaceae and Flacourtiaceae. In terms of number of individuals, the most abundant families are Rubiaceae, Lauraceae, Sapindaceae, Myrtaceae and Flacourtiaceae, and those with highest importance value in the plant community are Lauraceae, Rubiaceae, Araucariaceae and Sapindaceae (Moro et al., 2009).

The High Altitude forest is approximately 1250 meters above sea level and is in an initial successional stage. It is a low (average height of 2 m) closed shrub, size, and herbaceous extract consisting of several species of Poaceae, terrestrial bromeliads, epiphytes, and mosses and lichens, pteridophytes and several scandent species of Asclepiadaceae, Malpiguiaceae and Sapindaceae, together with species of terrestrial Orchidaceae. The families with the greatest number of species and individuals are Myrtaceae, Asteraceae, Melastomataceae and Myrsinaceae (Moro et al., 2009).

Data collection. Data were collected between September 2012 and September 2013, in six bimonthly campaigns. During each campaign, traps were open for five nights, with exception of the first campaign when they remained open six nights. Traps were checked every early morning.

In each site three lines of pitfall traps were installed, with four 60 L buckets connected in each line by black plastic (approximately 80 cm heigh), 10 m distant from each other and approximately 30 m a row from another. Each line was approximately 40 m long. Additionally, in each site three lines containing six live traps each were installed approximately 5 m distant from each other, and baited with a paste made with bananas, sardines, bacon, oatmeal, peanut butter and corn flour. The live traps models included: Sherman (small: 250 x 90 x 90 mm; large: 310 x 95 x 95 mm) and Tomahawk (small: 350 x 145 x 180 mm; large: 450 x 145 x 180 mm). Each line was approximately 25 m long and lines were separated by approximately 30 m. This provided a total of 30 traps (12 pitfalls and 18 live traps) installed per campaign in each site. The live traps were placed preferentially on the ground.

All captured individuals received either a field number or a numbered tag, and had their specific identification, sex, reproductive condition, capture location, trap type and position recorded. To provide precise taxonomic identification at least one male and one female per species were collected for cytogenetic procedures and morphological analysis based on external and skull morphology, the results of these procedures are better described in Grazzini et al. (2015c). The classification of Sigmodontinae species followed Carleton & Musser (2005), with the exception of species of the Tribe Oryzomyini, which were identified based on Weksler & Percequillo (2011). Didelphimorphia were identified following Gardner (2005).

All captures were made according to the Brazilian federal environment agency license no. 35534-1SISBIO.

Data analysis. To compare the species richness per site rarefaction curves were calculated based on individuals using a Poisson model in EstimateS 9.1.0 (Colwell et al., 2012).

To measure diversity we adopted the concept of true diversity (Jost, 2006), measured by the effective number of species. Thus, true diversities (TD) were calculated of order q = 0 (counts species equally without regard to their relative abundances) and q = 1 (counts individuals equally and thus weighs species in proportion to their abundances) using maximum likelihood estimators (MLE) for vegetation types (α diversity), and the SPNF (γ diversity) (Jost, 2006; Chao et al., 2012), through software SPADE (Chao & Shen, 2010). Additive and multiplicative diversity components were calculated from the obtained result. The β+ (additive partition approach) component was calculated from the equation: β+ = γ - α; and β* (multiplicative partition approach) using the equation: β* = γ / α (Chao et al., 2012).

The β+ component of q = 0 order partition was divided by (N - 1), where N is the number of communities, to quantify the number of unique species per vegetation type (Chao et al., 2012). Relative species turnover per vegetation type (i.e. effective number of species not contained in the typical local community) was calculated from the use of β* from q = 0 in the equation (β -1) / N - 1 (Chao et al., 2012). This measure of differentiation is 0 when there is no difference between the turnover units, and is equal to 1 when each unit is completely distinct from all other units (Jost, 2007). The result was used to indicate the effect of vegetation type on the regional diversity of the group.

The TD of order q = 1 was used to compare the diversity among vegetation types by overlapping of 95% confidence intervals. In addition, the relative number of individuals of the species was obtained by dividing the total number of sampled individuals of each species by the total number of individuals recorded in the vegetation types (Magurran, 2011).

Finally a cluster analysis was performed using a matrix of Bray-Curtis similarity index values, as tested and recommended by Clarke and Warnick (cited in Magurran, 2011), using the UPGMA algorithm with 200 bootstrap repetitions in PAST 3 (Hammer et al., 2001).

RESULTS

A total of 875 captures (19.4% capture success) were obtained from a sampling effort of 4500 trap.nights (900 per vegetation type). This included 625 individuals belonging to 16 species (Tab. I). Pine plantation and Araucaria plantation presented the lowest richness with eight species each while other vegetation types registered 10 species each. However, interval of confidence in rarefaction curves indicated no significant difference in species richness between the vegetation types (Fig. 2).

Tab. I.
Capture indexes of small mammals sampled at five vegetation types of Piraí do Sul National Forest, Paraná state, Brazil. Number of individuals, number of captures, relative capture success (%), true diversity order q = 0 (i.e. species richness), additive partition approach (β+), multiplicative partition approach (β*), unique species per vegetation (β+/N-1), species not contained in the typical local community or turnover (β* -1/N-1), true diversity in order q = 1.

Vegetation	Individuals	Captures	Capture success (%)	q = 0					q = 1
				TD	β+	β*	β+/N-1	β* -1/N-1	TD
Pine Plantation	103	118	13.1	8	8.0	2.00	2.0	0.25	3.75
Araucaria Plantation	120	183	20,3	8	8.0	2.00	2.0	0.25	4.54
Riparian Forest	102	154	17.1	10	6.0	1.60	1.5	0.15	4.26
High Altitude forest	125	180	20.0	10	6.0	1.60	1.5	0.15	4.58
Natural Regeneration forest	175	240	26.7	10	6.0	1.60	1.5	0.15	5.34
Piraí do Sul National Forest (Total)	625	875	19.4	16	6.8	1.74	1.7	0.18	5.33

Fig. 2.
Rarefaction curves of small mammals sampled at five vegetation types of Piraí do Sul National Forest, Paraná state, Brazil, with a 95% confidence interval (A, Pine Plantation; B, Riparian Forest; C, Araucaria Plantation; D, Natural Regeneration forest; E, High Altitude forest).

The species richness average between the sampled sites in SPNF was 9.2, resulting in β+ = 6.8 and β* = 1.74. The number of unique species per vegetation type was 1.7 and the turnover (or species not contained in the typical local community) was 0.18 (Tab. I). Looking at the calculated turnover of each vegetation type PP and AP had higher indexes than NR, HA and RF indicating those two vegetation types had more distinct compositions. The TD (q = 1) was higher in NR, intermediate in RF, AP and HA, and significantly lower in PP compared to NR (Fig. 3).

Fig. 3.
True diversity values (TD), order q = 1, of small mammals sampled at five vegetation types of Piraí do Sul National Forest, Paraná state, Brazil. Equal letters indicate overlap of the 95% confidence intervals (PP, Pine Plantation; RF, Riparian Forest; AP, Araucaria Plantation; NR, Natural Regeneration forest; HA, High Altitude forest).

The rodent Akodon montensis was the most abundant (i.e. the species with most individuals captured) in three of the five vegetation type. The exceptions were PP and NR where Oligoryzomys nigripes and Thaptomys nigrita were more abundant respectively. Bibimys labiosus and Didelphis albiventris were captured exclusively in PP; Oxymycterus nasutus exclusively in NR; and Cryptonanus sp. and Monodelphis scalops exclusively in HA (Tab. II).

Tab. II.
Individuals (Nº) and relative number of individuals (%) of small mammals sampled at five vegetation types of Piraí do Sul National Forest (PSNF), Paraná state, Brazil (PP, Pine Plantation; RF, Riparian Forest; AP, Araucaria Plantation; NR, Natural Regeneration forest; HA, High Altitude forest).

Species	PP		RF		AP		NR		HA		PSNF (Total)
	Nº	%	Nº	%	Nº	%	Nº	%	Nº	%	Nº	%
DIDELPHIMORPHIA
Cryptonanus sp.	0	0	0	0	0	0	0	0	2	2	2	<1
Didelphis albiventris Lund, 1940	2	2	0	0	0	0	0	0	0	0	2	<1
Didelphis aurita Wied-Neuwied, 1826	2	2	6	6	5	4	2	1	3	2	18	2.8
Gracilinanus microtarsus (Wagner, 1842)	0	0	1	1	1	1	1	<1	0	0	3	<1
Monodelphis americana (Muller, 1776)	0	0	0	0	2	2	0	0	1	<1	3	<1
Monodelphis scalops (Wagner 1847)	0	0	0	0	0	0	0	0	1	<1	1	<1
RODENTIA
Akodon montensis Thomas, 1913	19	19	52	51	56	47	51	29	61	50	239	38.2
Bibimys labiosus Winge, 1887	1	1	0	0	0	0	0	0	0	0	1	<1
Brucepattersonius iheringi (Thomas, 1896)	6	6	6	6	9	8	7	4	5	4	33	5.3
Juliomys ossitenuis Costa, Pavan, Leite & Fagundes, 2007	0	0	1	1	0	0	2	1	0	0	3	<1
Nectomys squamipes (Brants, 1827)	0	0	2	2	0	0	7	4	0	0	9	1.4
Oligoryzomys nigripes (Olfers, 1818)	59	57	27	26	28	23	25	14	25	20	164	26.2
Oxymycterus judex (Thomas, 1909)	0	0	1	1	0	0	0	0	2	2	3	<1
Oxymycterus nasutus (Waterhouse, 1897)	0	0	0	0	0	0	1	<1	0	0	1	<1
Sooretamys angouya (Fisher, 1814)	2	2	3	3	5	4	21	12	5	4	36	5.8
Thaptomys nigrita (Lichtenstein, 1829)	12	12	3	3	14	12	58	33	20	16	107	17.1
TOTAL	103		102		120		175		125		625

The result of the cluster analysis of species similarity among vegetation types indicated next to the 90% similarity between HA and AP followed by RF (approximately 85%) and NR (approximately 70%). The species composition in PP was the most dissimilar to that of the other vegetation types with approximately 55% (Fig. 4).

Fig. 4.
Dendrogram from the cluster analysis of the similarity of small mammals sampled at five vegetation types of Piraí do Sul National Forest, Paraná state, Brazil (PP, Pine Plantation; RF, Riparian Forest; AP, Araucaria Plantation; NR, Natural Regeneration forest; HA, High Altitude forest).

DISCUSSION

The number of individuals and capture success obtained in the study were high when compared to other efforts conducted in the Atlantic Forest biome (e.g. Pires et al., 2002; Dalmagro & Vieira, 2005; Astúa et al., 2006; Pardini & Umetsu, 2006; Pessôa et al., 2009; Lima et al., 2010; Pedó et al., 2010; Gatto-Almeida et al., 2016). For the species, the fact that Akodon montensis and Oligoryzomys nigripes were the most abundant (i.e. more individuals captured) was expected and Quintela et al. (2012) even state that these are the most abundant non-volant small mammals in most studies in forest formations from Southern Brazil. The third ranked species in terms of number of individuals captured was Thaptomys nigrita, which was also common in a study in Mixed Rain Forest close to SPNF (Oliveira et al., 2005), which reinforces the suggestion that this species is associated with this vegetation type in Paraná. The rarest species were Bibimys labiosus, Monodelphis scalops and Oxymycterus nasutus, which had not been registered in many of the previous studies in the Araucaria Forest (Cademartori et al., 2002, 2004, 2008a,b; Oliveira et al., 2005; Pedó et al., 2010; Marques et al., 2011).

We expected PP to present lower richness as reported Umetsu & Pardini (2007), Fonseca et al. (2009), Pardini et al. (2009), Rosa & Vieira (2010) in their study sites. However, we only found slightly higher richness in natural regenerating vegetation types i.e. RF, NR and HA sites, which might not be real if confidence of interval in rarefaction curves is considered. The same pattern was observed for AP.

In the specific case of the present study, it may be important to note that the reforestation areas (i.e. PP and AP) are surrounded by native vegetation types at a good level of conservation, the areas are not managed for 40 years and there are other native species growing within them. The results of Stallings (1991) and Rosa & Vieira (2010) emphasize the importance of this aspect: the first of which found a richer and more abundant assemblage of non-volant small mammals in a Eucalyptus plantation with an understory composed of native species compared to areas where there was only exotic species, and the second recorded only four species in a pine reforestation area without understory in the state of Rio Grande do Sul, Brazil. Either way, richness measure does not seem to be appropriate to assess the differences between areas sampled in SPNF.

Regarding species composition, some studies showed distinctions in the composition of assemblages of reforested environments (Umetsu & Pardini, 2007; Fonseca et al., 2009; Pardini et al., 2009; Rosa & Vieira, 2010) which led us to expect that PP and AP would present different species composition. This hypothesis was only partially met once no exclusive species were registered for AP area, while Bibimys labiosus and Didelphis albiventris were recorded only in PP. On the other hand, AP area register Gracilinanus microtarsus and Monodelphis americana two species captured in others areas of SPNF and not in PP. There is not much information about Bibimys labiosus or Monodelphis americana sensibility to environmental quality but Didelphis albiventris (actually the genus Didelphis) is considered ecologically generalist and frequently is found in disturbed environments (Olifiers et al., 2005; Cantor et al., 2010; Beatty et al., 2014) while Graciliananus microtarsus has been showed to not be sensible to a variety of atrophic disturbs (e.g. Pardini et al., 2005; Püttker et al., 2008).

The turnover indexes (q = 0) that measured the effective number of species not contained in the typical local community showed higher values of differentiation (0.25) for both reforestation areas (i.e. PP and AP) while the natural regenerating areas showed similar and lower indexes (0.15) meaning these last are more similar in composition to the general community of PSNF. This result helps to corroborate our initial hypothesis that the reforested environments would have different species composition.

Furthermore, TD (q = 1) analysis found higher values in RF, AP, NR and HA, and significant difference between the PP and NR confirming our initial hypothesis that native environments have greater diversity of non-volant small mammals. In a comparison made between pine reforestation and native area of coastal forest (“restinga”), Rosa & Vieira (2010) found no significant difference in diversity. However, the analysis was based on the Shannon-Wiener index, which may have masked the true diversity of the assemblages, besides the fact that the coastal forest is very different from a forest environment. When compared to the AP, the values found in RF and HA were very similar, suggesting that they are structurally similar assemblages. Although not statistically significant, the diversity of NR was somewhat larger, a result similar to that found by Umetsu & Pardini (2007) using as a basis the richness, abundance and species composition of the analyzed assemblages, suggesting that among the different management histories evaluated in PSNF, the natural regenerating area holds the higher diversity.

The cluster analysis showed similar results to those of TD (q = 1), in that the most distinctive assemblage (in terms of structure) is the PP, a result that is in line with its lower TD and the large number of Oligoryzomys nigripes captured. The second most distinct assemblage was found in NR, which was also expected due to its higher TD and the large number of Thaptomys nigrita. The assemblages of RF, AP and HA were much more similar to each other, a result also reflected in the TD values.

Together, the results of the TD (q=1) and cluster analysis showed that there were differences in the structure of the assemblages among the physiognomies that are all secondary and with a history of 40 years of regeneration, but different in their floral composition. Furthermore, our results confirm that the replacement of native by exotic vegetation negatively influenced some components of the local diversity. The importance of the result is not restricted to the SPNF, but the groupʼs conservation in the Araucaria Forest. This is a phytophysiognomy of the Atlantic Forest biome that retains only 12.6% of its original forest, with only 3.1% of these protected by Integral Protection Conservation Units (Ribeiro et al., 2009). Most of these unprotected forests are small forest fragments inserted into matrices of various human activities. The results demonstrated the potential of these secondary forest fragments to act as true habitat refuges for the group, provided they retain a certain degree of conservation of native vegetation and structure.

Acknowledgements.

We are grateful to the ICMBio environmental analysts that work at Piraí do Sul National Forest Gustavo Nabrzecki and Karina Ferreira de Barros, the unit employees Arnoldo Félix da Silva, Cássio Marcelo Mochi-Junior, Heloisa de Oliveira and Jaqueline dos Santos Pontes for help in field work; to Iris Hass and Ives José Sbalqueiro for their support in laboratory work; to Renata Pardini (USP), Juliana Quadros (UFPR) and Darren Norris (UNESP) for contributions to the text and English translation; to CNPq for the partial financial support via the Protax Edict (process 562357/2010-6); and to the Postgraduate Program in Zoology at the Universidade Federal do Paraná (UFPR) for the masters scholarship to the first author.

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Publication Dates

• Publication in this collection
  23 Aug 2021
• Date of issue
  2021

History

• Received
  09 Aug 2020
• Accepted
  06 May 2021