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Diet of the thin-spined porcupine (Chaetomys subspinosus), an Atlantic forest endemic threatened with extinction in southeastern Brazil
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ORIGINAL INVESTIGATION
Diet of the thin-spined porcupine (Chaetomys subspinosus), an Atlantic forest endemic threatened with extinction in southeastern Brazil Rodrigo B. de Souto Lima, Pedro A. Oliveira, Adriano G. Chiarello Programa de Po´s-graduac- a˜o em Zoologia de Vertebrados, Pontifı´cia Universidade Cato´lica de Minas Gerais (PUC-Minas), Avenida Dom Jose´ Gaspar 500, Pre´dio 41, Belo Horizonte 30535-610, Minas Gerais, Brazil Received 13 July 2009; accepted 11 September 2009
Abstract Chaetomys is a poorly known, monotypic genus of tree porcupine threatened with extinction due to deforestation and habitat fragmentation. Its nocturnal habit, relatively restricted distribution and low level of activity have conspired for decades against detailed field studies. Here the diet of the species in restinga forests is described for the first time. Restinga is a subtype of lowland Atlantic forest occurring on sandy soils close to the Atlantic littoral in Brazil. Three radio-collared females were monitored for 12 months between March 2005 and February 2006. Leaves were the most heavily consumed dietary item, varying from 71.9% to 75.4% of the diet of each individual, followed by flowers (7.7% - 15.7%) and fruits (0 - 1.4%). Animals fed on 57 trees from 14 species, with a higher concentration on Pera glabrata (49.8%) and Tapiriria guianensis (22.7%). Pera glabrata is locally abundant and widely distributed in the Atlantic forest. Each individual consumed a smaller subset of plant species (4-10 species/individual) and shared only the two most important tree species (P. glabrata and T. guianensis). Results corroborate previous studies indicating that Chaetomys is a folivore, perhaps the most folivorous amongst the Erethizontidae. Since the most consumed plant species are relatively common and widespread, Chaetomys might thrive in a broader range of habitats than previously suspected, including secondary forests. & 2008 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. Keywords: Erethizontidae; Feeding habits; Folivore; Atlantic forest
Introduction Chaetomys subspinosus is an arboreal rodent endemic ´ vilato the Atlantic forest of Brazil (Moojen 1952; A Pires 1967; Coimbra-Filho 1972). Its taxonomic position has been controversial in the past, with some authorities including it in the spiny rat family (Echimyidae) (Patterson and Wood 1982; Woods 1993), others putting it among the Neotropical porcupines (Erethizontidae) (Moojen 1952; Cabrera 1961; Nowak and Paradiso Corresponding author. Tel./fax: +51 31 3319 4967.
E-mail address: [email protected] (A.G. Chiarello).
1983; Martin 1994; Carvalho 2000; Wilson and Reeder 2005). A recent and comprehensive molecular study confirms that Chaetomys is a basal but true member of the Erethizontidae (Vilela et al. 2009). Chaetomys subspinosus is one of the most distinct and poorly known species of the Atlantic forest (Oliver and Santos 1991). It is threatened with extinction due to habitat destruction, forest fragmentation and subsistence hunting (Chiarello et al. 2008; IUCN 2009). The Atlantic forest is an ecosystem extremely impacted by human disturbance, occupying today about 11.3% of its original extent (Ribeiro et al. 2009). Due to its high species richness, degree of endemisms and area reduction the
1616-5047/$ - see front matter & 2008 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2009.09.002 Mamm. biol. 75 (2010) 538–546
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Atlantic forest is considered a top biological hotspot (Myers et al. 2000; Laurance 2009). The observation of C. subspinosus in nature is difficult due to a combination of factors: small body size, cryptic coloration, low level of activity and slow and silent movement in the dense forest canopy. Even trained observers with adequate equipment (binoculars and powerful lights) might find it difficult to record accurate data on feeding and behavior. As a consequence, there are few ecological studies on the species. In a pioneering study Chiarello et al. (1997) managed to observe a translocated radio-collared individual for three nights. More recently Kuniy et al. (2005) reported the stomach contents of two individuals captured in northern Bahia. The only comprehensive studies on the ecology of free ranging individuals were carried out recently in Espı´rito Santo (Oliveira 2006), from which the present contribution derives, and in southern Bahia (Gine´ 2009). Available dietary data on diet indicates that Chaetomys is strongly folivorous (Chiarello et al. 1997; Gine´ 2009). Arboreal mammals with folivorous diets have low levels of metabolism and activity (McNab 1978). This is because leaves are poor in readily available energy such as sugars and starch and are difficult to digest (McNab 1978; Cork and Foley 1991; Milton 1998). Apart from poor digestibility, leaves are protected by chemical substances like alkaloids and tannins that inhibit their digestion both by vertebrates and invertebrates (Freeland 1991). Notwithstanding the feeding inhibitors, folivory is common among Erethizontids. Sphiggurus villosus, which is sympatric with Chaetomys, seems to be strictly folivorous (Passamani in press) and Coendou prehensilis, which is a wider ranging member of the family, is considered folivorous-frugivorous (Emmons and Feer 1997; Eisenberg and Redford 1999), although Santos-Ju´nior (1998) reports a higher ingestion of fruits than leaves in translocated individuals of this species. Erethizon dorsatum, the North American porcupine feeds on leaves of trees and shrubs, fruits, nuts, tree bark, aquatic plants, grasses and even cacti (Roze and Ilse 2003). Here we used radio telemetry and direct observation to investigate the feeding habits of three free-ranging Chaetomys in a forest reserve located in Espı´rito Santo state, southeastern Brazil. The study area was restinga, a subtype of lowland Atlantic forest that occurs close to the littoral on sandy soils. This vegetation formation is mostly gone since it occurs in areas highly impacted by city sprawl, tourism development and road construction. As a result, less than 0.5% of the Atlantic forest is represented today by restingas (Fundac- a˜o SOS Mata Atlantica and Instituto de Pesquisas Espaciais 2008; Ribeiro et al. 2009). Nevertheless, recent studies indicate that Chaetomys occurs predominantly in restingas rather than in forest formations located further inland (Chiarello et al. 2008). Thus results reported here apart from adding to the natural history of a poorly known
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Erethizontid, might help define the niche characteristics of the species, which is needed for a proper planning of its conservation management.
Material and methods Study area The study area is within the limits of a state park (Parque Estadual Paulo Ce´sar Vinha-PEPCV), located in the littoral of Espı´rito Santo state in southeastern Brazil (201330 -201380 S and 401230 -401260 W). The area is a sandy plain only a few meters above the sea level. Annual average temperature is 23.3 1C and annual average precipitation is 1307 mm (Fabris and Ce´sar 1996). Vegetation is a mosaic of restinga forest, open shrub vegetation and seasonally flooded areas. The restinga forest, the only vegetation formation used by Chaetomys (Oliveira 2006) contains 172 plant species distributed in 54 families (Assis et al. 2004a). Its higher strata are on average 8 m tall and some emergent trees reach 20 m. The most common families are Myrtaceae, Sapotaceae, Annonaceae, Bombacaceae and Meliaceae (Assis et al. 2004b). Epiphytes and lianas are abundant.
Data collection Study animals were located in their diurnal resting sites after intensive searches helped by a local inhabitant. After sedation with a mixture of ketamine (5 mg/kg of body weight) and xylazine (2 mg/kg of body weight), a VHF transmitter attached to a ball and chain collar was fitted to the neck region of each animal. The collars weighed 60 g (Telonics Inc., model 205), which represents less than 3% of the body weight. After a few nights the animals seemed to ignore the presence of the collars. Highly reflective tapes of the type used in road transport were attached to the transmitters, greatly increasing the chances of finding and monitoring a radio-collared animal even in dense vegetation. After recovering from the anesthesia the animals were released in the tree of capture. Three individuals, all adult females, were radio-collared. We tried hard to find males in the area but failed. The observations began 20 days after the capture date (Table 1). The observations were carried out monthly between March 2005 and February 2006. One individual (Ch970) was monitored for 10 months until it was found dead in the 11th month. The cause of death was unknown. The second (Ch160) could not be monitored in one month because the area it inhabited was temporarily flooded and therefore it was observed for 11 months, and the third (Ch274) was monitored for 12 months. Each animal was observed one night per month during the first five hours after
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Table 1. Animal
Ch-970 Ch-274 Ch-160 Total
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Monitoring period and sampling effort of the three radio-collared C. subspinosus. Weight (g)
2700 2200 2100
Capture date
04/03/2005 04/03/2005 05/03/2005
Monitoring
Number of scans
Period
Nights
25/03 to 13/11/2005 25/03/2005 to 21/02/2006 27/03/2005 to 22/02/2006
10 12 11 33
darkness, generally between 18:00 and 23:00 h [darkness began one hour earlier in the peak of winter (JuneAugust) and one hour later in the peak of summer (December-February)]. Previous studies indicate that a greater part of activity and feeding takes place in this period (Chiarello et al. 1997; Gine´ 2009). The animals were radio located in the afternoon in their diurnal resting sites using a receptor and a three-element Yagi antenna (Titley Electronicss, model Regal 2000). Once the study animal was located we waited for the animal to begin activity, which in general started only after the sunset. Binoculars (8 40), handheld torches (rechargeable Maglites with 12 watt halogen bulb) and head lamps (3 watt Petzl Duos) were used in the observations, which were always conducted by two observers. In the beginning of the study we realized that if the central focus of the Maglites was directed to the animal it tended to react stopping activity. So in order to avoid disturbing the normal rhythm of activity we directed the focus of the Maglites to the side of the animal, insuring that sufficient light was available for accurate observation without disturbing the animal. At the end of the study the animals were recaptured, had their collars removed, and were released in the forest. The consumption of tree species was quantified recording the duration of feedings bouts using a digital chronometer. A feeding bout was defined as beginning the moment when the animal was in the canopy of a tree, bringing food to the mouth or chewing plant parts. The feeding bout ended when the animal stopped chewing or manipulating plant parts. Feeding bouts of any duration were recorded. The consumed trees were marked with a colored tape, numbered for later collection of reproductive parts and identification by a botanist with a strong experience in local flora (Dr. Oberdan J. Pereira, Universidade Federal do Espı´rito Santo). The importance of each plant species in the diet was calculated by dividing the time spent feeding in each tree species by the total time spent feeding in all tree species and expressing the result as a percentage. Due to difficulties of observation, the quantification of tree part consumption (leaves, fruit, flower, other) was done differently. We used scan sampling (Altmann 1974) at every 10 minutes to record five mutually exclusive
hh:mm 47:20 52:20 51:10 150:50
356 347 337 1040
categories: resting, moving, feeding, other and indeterminate. Here we considered only the scans relative to feeding. The number of scans of each consumed item was tallied and the importance of each item was expressed as percentage of the total number of feeding scans.
Data analysis To determine whether leaves are the most important food item both annually and seasonally (dry versus wet season) we first calculated the daily number of scans recorded for each consumed item. Dry season was defined as the period between April and September and wet season between October and March. Then we calculated the percentage of scans recording leaves and recording all other items put together (flower+fruit+ other). We contrasted the percentage of scans of leaves x other items using the Wilcoxon signed rank test. A similar procedure was used to compare young x mature leaf consumption. The only difference is that here we excluded data from the first three months [March, April and May (one wet season month and two dry season months)] because in the beginning of the study it was difficult to discern if the study animals were feeding on young or mature leaves. We used the Spearman rank correlation (rs) to compare the percentage of consumed species between seasons. All tests were performed with the software SPSS version 17.
Results Chaetomys subspinosus has a stereotypical behaviour when eating. Study animals usually climbed to the highest part of the tree crown and reached for the branch tips. When they arrived at this part, they sat on their hind limbs and anchored their tails around firm branches, leaving their fore limbs free to grab thinner, flexible twigs and bring them to the front of their heads. Then the leaves or other item on these twigs were apparently smelled, and if selected they were brought to the mouth, chewed and swallowed. In many occasions only the leaf blades were eaten, leaving the petioles intact. Animals always fed in trees: in all thirty-three observation nights none of the three study animals ever came down to feed
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on the ground. Leaves were the most abundant item in the diets of all three C. subspinosus (Fig. 1), with small variation between individuals (74.16% - 79.71%). Flowers were the second most consumed item (7.69% 15.73%), while fruits were consumed only rarely (0 1.45%). The identification of the consumed item was not possible in 11.66% of feeding scans. None of the animals ever fed on lianas or epiphytes, despite their great abundance in the study area.
Fig. 1. Diet composition of three radio-collared Chaetomys subspinosus. Proportion of items recorded in ‘‘feeding’’ scans.
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Leaves were eaten significantly more often than all other items put together in both dry and wet season (Table 2). Although the consumption of items other than leaves increased during the rainy season, this increase was only marginally significant (MannWhitney, p=0.075). The utilization of flowers, fruits and shoots usually occurred in an opportunistic manner, when those items were available among the leaves that were eaten in higher amount. On an annual basis the consumption of mature leaves was higher than that of young leaves, but the difference was not significant. Analyzing the seasons separately, young leaves were consumed significantly more often than mature leaves in the rainy season, while the opposite was observed in dry season (Table 3). The three study animals consumed plant parts from 57 individual trees belonging to 14 species and 9 families. Seven trees used by the animals for feeding couldn’t be collected and therefore were not identified. Over 80% of the total feeding time was allocated to Euphorbiaceae and Anacardiaceae. The genus Pera (Euphorbiaceae) alone represented 58.09% of the diet. Pera glabrata was the most important species for all three animals, representing on average 49.85% of their diet. The only other tree species consumed by all three study animals was Tapirira guianensis, but its relative importance varied (Table 4). These top two plant species accounted for 88.36% of the diet of Ch 970, 73.56% for Ch 160, and 65.71% for Ch 274. The total number of tree species consumed by each study animal varied from 4 to 10 species (Table 4). The Fig. 2 shows a slight
Table 2. Annual and seasonal variation in the diet of three females C. subspinosus, expressed as percentage of feeding scans recorded within and between season comparisons (Wilcoxon and Mann-Whitney tests, respectively). (p): test significance. Season
Rainy Dry Mann-Whitney (p) Annual
n
13 18 31
Leaves
Other items
Wilcoxon
Average
s.d.
Average
s.d.
71.64 82.75 0.075 78.09
19.55 29.14
28.36 17.25 0.075 21.91
19.55 29.14
0.006 0.002
25.79
o0.001
25.79
p
Table 3. Annual and seasonal variation in the consumption of young and mature leaves by three females C. subspinosus, expressed as percentage of feeding scans recorded for the item ‘‘leaf’’. Within and between season comparisons measured by Wilcoxon and Mann-Whitney tests, respectively. (p): test significance. Season
Rainy Dry Mann-Whitney (p) Annual
n
12 12 24
Young leaves
Mature leaves
Wilcoxon
Average
s.d.
Average
s.d.
p
69.44 1.28 0.0008 35.36
35.58 4.44
30.56 98.71 0.0008 64.64
30.58 4.44
0.058 0.001
40.85
0.106
40.85
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Table 4.
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Time spent feeding (in minutes and percentages) on each tree species by the three females C. subspinosus.
Species/Family
Pera glabrata/Euphorbiaceae Tapirira guianensis/Anarcadiaceae Pera leandri/Euphorbiaceae Matayba guianensis/Sapindaceae Inga fagifolia/Fabaceae Humiria balsamifera/Humiriaceae Zollernia glabra/Fabaceae Myrtaceae sp 1./ Myrtaceae Inga laurina/Fabaceae Manilkara subsericea/Sapotaceae Moraceae sp 1/Moraceae Eugenia punicifolia/Myrtaceae Coccoloba alnifolia/Polygonaceae Psidium macahense/Myrtaceae TOTAL
Ch 970
Ch 274
Ch 160
Total
Min.
%
Min.
%
Min.
%
Min.
308 292 53
45.36 43.00 7.81
236 71 86
48.16 14.49 17.55
297 20
57.34 3.86
35 55
7.14 11.22
84 40
16.22 7.72
43
8.30
18 8
3.47 1.54
5 2 1 518
0.97 0.39 0.19 100
841 383 139 84 75 55 43 26 18 8 7 5 2 1 1687
26
3.83
7
679
100
490
1.43
100
% 49.85 22.70 8.24 4.98 4.45 3.26 2.55 1.54 1.07 0.47 0.41 0.30 0.12 0.06 100
P. glabrata and T. guianensis individuals were never eaten although they were traversed by the study animals.
Discussion
Fig. 2. Accumulated number of plant species consumed by the three radio-collared animals along the monitoring period. The upper line shows the combined diet of all three animals.
tendency to curve stabilization for each animal considered separately, but when data from the three animals are combined the curve was still ascending by the end of the study period. There was no significant correlation in tree species importance (% in diet) between the dry and wet seasons (Spearman rank correlation coefficient, rs=0.367, N=14, p=0.197). Nevertheless, the two most important tree species (P. glabrata and T. guianensis) remained the same in both seasons (Table 5). A smaller number of species (n=7) was used as source of food in the wet season than in dry season (n=12) (Table 5). Besides selecting certain tree species as food sources, Chaetomys subspinosus also seems to select individual trees. Some individual trees were fed upon repeatedly in distinct observation nights, while others from the same species were ignored, despite their close proximity. Some
Results show important individual variations both in terms of species consumed and their relative importance in the diet. These differences are partly due to distinct characteristics of the home range of each individual, which did not overlap and were widely separated from one another. The forest fragments in which the study animals lived were separated by marshlands or sandy areas with shrubby vegetation, and apparently each home range has a distinct floristic composition. The home ranges of Ch970 and Ch274 were far closer to each other than to the Ch160 and, in fact three of the four species consumed by Ch970 were also consumed by Ch274. The forest fragment where Ch160 lived was larger than that of the other two. Perhaps due to this higher diversity Ch160 included a higher number of tree species in its diet than did the other two animals. On the other hand, Ch160 was the only female not observed suckling an infant during the study. Females during lactation have higher energy demand than non-lactating females (Robbins 1993). Thus the low diversity diet of both Ch970 and Ch274 might result, alternatively, from a more conservative foraging strategy of these lactating females. Leaves were the most commonly consumed item throughout the year. Similarly, Gine´ (2009) did not notice significant differences between seasons in the main items consumed by Chaetomys observed in southern Bahia, although he did record significant seasonal
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Table 5.
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Time spent feeding on each tree species according to season.
Species/Family
Pera glabrata/Euphorbiaceae Tapirira guianensis/Anarcadiaceae Pera leandri/Euphorbiaceae Matayba guianensis/Sapindaceae Inga fagifolia/Fabaceae Humiria balsamifera/Humiriaceae Zollernia glabra/Fabaceae Myrtaceae sp 1/Myrtaceae Inga laurina/Fabaceae Manilkara subsericea/Sapotaceae Moraceae sp 1/ Moraceae Eugenia punicifolia/Myrtaceae Coccoloba alnifolia/Polygonaceae Psidium macahense/Myrtaceae TOTAL
Dry season
Rainy season
Minutes
%
Minutes
%
348 237 139 31
41.23 28.08 16.47 3.67
493 146
58.48 17.32
20 20 26
2.37 2.37 3.08
53 75 35 23
6.29 8.90 4.15 2.73
18
2.14
8 7 5 2 1 844
0.95 0.83 0.59 0.24 0.12 100
variation in food availability in the forest. In PEPCV young leaves were consumed more often than mature leaves during the wet season, a period of the year when new leaves are more available, at least in the forests of the region (Jackson 1978). Although the phenology of the study area was not monitored, this area has a pattern of precipitation and temperature similar to that of Santa Teresa, where the study of Jackson (1978) was carried out. Thus the phenological pattern might be similar between these two areas. In another restinga forest in Ubatuba, state of Sa˜o Paulo, Talora and Morelato (2000) also recorded higher availability of new leaves during wet season. Among the members of Erethizontidae whose diet is known, Chaetomys is probably one of the most folivorous (Roze 1989; Santos Ju´nior 1998; Eisenberg and Redford 1999; Gine´ 2009; Passamani in press). The frugivory speculated by Kuniy et al. (2005) should be viewed with care since it was based on the contents of just two stomachs. Chaetomys subspinosus is apparently a caecal fermenter since its caecum is enlarged and differentiated (Martinez et al. 2005, Gine´ 2009). Caecal fermentation with some specialization for retention and separation of particulates is essential for small-bodied mammals with a high degree of folivory such as Chaetomys, because it allows a higher passage rate and a lower loss of nitrogen in feces, increasing the efficiency of the digestive process (Cork 1996). The lethargic behavior observed in this species (Chiarello et al. 1997; Oliveira 2006; Gine´ 2009) is also an adaptation to a strongly folivorous diet. Arboreal folivores have activity and metabolic rates lower than expected due to the low caloric value of leaves, presence of feeding deterrents (secondary compounds) in leaves, and also due to relatively small body masses (McNab 1978; Cork and Foley 1991).
843
100
Freeland (1991) states that smaller mammals detoxify and eliminate secondary compounds more rapidly than larger mammals, allowing the first to specialize on a lower number of plant species than the latter. Chaetomys concentrates its feeding on a few plant species. From a pool of at least 92 tree species known to exist in PEPCV (Assis et al. 2004b) only 14 were consumed by the three study animals, each of which consumed an even smaller subset of species. Further, only three species made up more than 80% of the diet. Gine´ (2009) also found a small number of plant species (n=17) consumed by the four individuals observed by him in southern Bahia, where dense rain forest (ombrophilous) predominates. Since this type of forest is probably richer in plant species than the restinga forest of PEPCV, the degree of diet specialization might be even higher in Bahia. Roze (1984) reports similar results for the North American pocupine Erethizon dorsatum in winter. This population consumed 10 tree species in total but each individual concentrated on one or two species and the top three species made up 80% of the population0 s diet (Roze 1984). Similarly, the translocated Coendou prehensilis observed by Santos Ju´nior (1998) fed on a total of 14 species, with a strong concentration on three species. It seems therefore that Chaetomys follows the same feeding pattern observed by other Erethizontids and some sympatric arboreal folivores such as the maned sloth Bradypus torquatus (Chiarello 1998). Analyzing the two lists of consumed species available thus far (present study and Gine´ 2009) we observe that three genera (Pera, Tapirira and Inga) were common to the two diets, that is, only 14% of the 21 genera were shared by the species. If we compare tree species, the percentage of overlap decreases to 7% (2 species out of
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27 taxa identified to the species level). This finding suggest that Chaetomys might be considered a generalist at the population level but a specialist at the individual level, similar to what has been observed for Bradypus sloths (Chiarello 1998). One may speculate that the strong concentration on Pera is due to two main aspects: availability in the forest and nutrient composition. Availability has been observed to be an important selection criterion in the diet of E. dorsatum (Roze 1984). Botanic studies in restingas (Assumpc- a˜o and Nascimento 2000; Assis et al. 2004b) indicate that P. glabrata is relatively common in these environments. Since P. glabrata has a wide geographic distribution (Assis et al. 2004b), it is possible that this species is important in the diet of Chaetomys in other Atlantic forest physiognomies as well. In fact, Pera glabrata was the third most heavily consumed species in Bahia representing more than one third of the Chaetomys diet there (Gine´ 2009). However, in southern Bahia Pera glabrata is not a highly abundant species (Gine´ 2009). This suggests that abundance may play a role but it is not the only criterion in the selection process. Gine´ (2009) measured the amount of dry matter, protein, fiber, among other dietary components of the seven plants most consumed by Chaetomys and concluded that the preferred ones were particularly rich in proteins and fiber. However, Pera glabrata ranked lowest in amount of protein and the highest in amount of fiber among the top seven consumed species. It is therefore likely that other nutrients or the amount and toxicity of secondary compounds might be more relevant for the selection of this plant genus by Chaetomys. The fact that some individuals of P. glabrata within the home range of the study animals were visited and consumed regularly while others were ignored or were less visited lends support to this hypothesis. The same was observed for Tapiriria guianensis, the second most consumed plant in PEPCV. Several studies show that herbivore mammals select among individuals of a given plant species for feeding. Australian marsupials (Phascolarctos cinereus and Pseudocheirus peregrinus) for example, select among individual Eucalyptus according to the amount of DFP, a phenolic compound (Lawler et al. 1998). For North American porcupines feeding on Populus tremuloides, some genets are preferred over others, based on the levels of two phenolic glycosides in the food trees (Diner et al. 2009). As there are few similarities between the diet studies available thus far, it seems that Chaetomys is not highly specialized in terms of habitat requirements. The most important tree species consumed are pioneers, have a relatively wide geographic distribution and may even be tolerant of forest disturbances. This is the case of Pera glabrata and Tapiriria guianensis in the present study (Pereira Junior et al. 2007; Silva et al. 2003; Sztutman and Rodrigues 2002). In southern Bahia six out of the
seven most important species are typical of the early stages of succession (Gine´ 2009). This spells good news for the conservation of the species since within its geographic distribution Chaetomys might be present in more habitat types than previously expected. Further, the rarity of records of this species might be more related to its cryptic behavior and nocturnal habit than to restrict feeding preferences.
Acknowledgements This study was financed by Ministerio do Meio Ambiente through a PROBIO grant and by PUC Minas through Fundo de Incentivo a Pesquisa grant. Museu de Biologia Prof. Melo Leita˜o and PEPCV offered valuable logistic support. We worked together with Instituto Drı´ades in this project and are particularly indebted to Deborah Faria and Gaston Gine´ for their help and feedback. The Brazilian environmental Agency (IBAMA) provided authorization for capturing the animals. We would like to thank Dr. Oberdan J. Pereira for plant identification, Mister Toninho for finding and capturing the porcupines, and Ne´lson Curi for veterinary support. Dr. Uldis Roze kindly reviewed an early version of this manuscript. The Brazilian Science Council (CNPq) and the Fundac- a˜o de Amparo a Pesquisa de Minas Gerais (FAPEMIG) provided research grants to AGC during data analysis.
References Altmann, J., 1974. Observational study of behavior: sampling methods. Behavior 49, 227–267. Assis, A.M., Thomaz, L.D., Pereira, O.J., 2004a. Florı´stica de uma Floresta de Restinga no Municı´pio de Guaraparı´, Espı´rito Santo, Brasil. Acta Bot. Bras. 18, 191–201. Assis, A.M., Pereira, O.J., Tomaz, L.D., 2004b. Fitossociologia de uma floresta de Restinga no Parque Estadual Paulo Ce´sar Vinha, Setiba, municı´pio de Guarapari (ES). Rev. Bras. Bot. 27, 349–361. Assumpc- a˜o, J., Nascimento, M.T., 2000. Estrutura e composica˜o de quatro formac- o˜es vegetais de restinga no complexo lagunar Grussaı´/Iquipari, Sa˜o Joa˜o da Barra, RJ, Brasil. Acta Bot. Bras. 14, 301–315. ´ vila-Pires, F.D., 1967. The type-locality of ‘‘Chaetomys A subspinosus’’ (Olfers, 1818) (Rodentia, Caviomorpha). Museu Nacional, Rio de Janeiro. Rev. Bras. Biol. 27, 177–179. Cabrera, A., 1961. Cata´logo de los mamı´feros de Ame´rica del Sur, vol. 2. Rev. Mus. Argent. Cienc. Nat. Bernardino Rivadavia 4, 309–732. Carvalho, G., 2000. Substitution of the deciduous premolar in Chaetomys subspinosus (Olfers, 1818) (Hystricognathi, Rodentia) and its taxonomic implications. Z. Saugetierkd. 65, 187–190.
R.B. de Souto Lima et al. / Mamm. biol. 75 (2010) 538–546
Chiarello, A.G., Passamani, M., Zorte´a, M., 1997. Field observations on the thin-spined porcupine, Chaetomys subspinosus (Rodentia; Echimyidae). Mammalia 61, 29–36. Chiarello, A.G., 1998. Diet of the Atlantic Forest maned sloth Bradypus torquatus (Xenarthra: Bradypodidae). J. Zool. London 246, 11–19. Chiarello, A.G., Aguiar, L.M.S., Cerqueira, R., Melo, F.R., Rodrigues, F.H.G., Silva, V.M.F., 2008. Mamı´feros Ameacados de Extinc- a˜o no Brasil. In: Machado, A.B.M., Drummond, G.M., Paglia, A.P. (Eds.), Livro Vermelho da Fauna Brasileira Ameac- ada de Extinc- a˜o. MMA and Fundaca˜o Biodiversitas, Brası´lia and Belo Horizonte, pp. 680–874. Coimbra-Filho, A.F., 1972. Mamı´feros ameac- ados de extinc- a˜o no Brasil. In: Espe´cies da Fauna Brasileira Ameac- adas de Extinc- a˜o. Academia Brasileira de Cieˆncias, Rio de Janeiro, pp. 13–98. Cork, S.J., 1996. Optimal digestive strategies for arboreal herbivorous mammals in contrasting forest types: why Koalas and Colobines are different. Aust. J. Ecol. 21, 10–20. Cork, S.J., Foley, W.J., 1991. Digestive and metabolic strategies of arboreal mammalian folivores in relation to chemical defenses in temperate and tropical forests. In: Palo, R.T., Robbins, C.T. (Eds.), Plant Defenses Against Mammalian Herbivory. CRC Press, Boca Raton, pp. 133–166. Diner, B., Berteaux, D., Fyles, J., Lindroth, R.L., 2009. Behavioral archives link the chemistry and clonal structure of trembling aspen to the food choice of North American porcupine. Oecologia 160, 687–695. Eisenberg, J.F., Redford, K.H., 1999. Mammals of the Neotropics. The Central Neotropics, vol. 3, Ecuador, Peru, Bolivia, Brazil. The University of Chicago Press, Chicago. Emmons, L.H., Feer, F., 1997. Neotropical Rainforest Mammals: A Field Guide, second ed University of Chicago Press, Chicago. Fabris, L.C., Ce´sar, O., 1996. Estudos florı´sticos em uma mata litoraˆnea no sul do estado do Espı´rito Santo, Brasil. Boletim do Museu de Biologia Mello Leita˜o 5, 15–46 (ISSN: 0103-9121). Freeland, W.J., 1991. Plant secondary metabolites: biochemical coevolution with herbivores. In: Palo, R.T., Robbins, C.T. (Eds.), Plant Defenses Against Mammalian Herbivory. CRC Press, Boca Raton, pp. 61–81. Fundac- a˜o SOS Mata Atlaˆntica, Instituto de Pesquisas Espaciais, 2008. Atlas dos Remanescentes Florestais da Mata Atlaˆntica: Perı´odo 2000 a 2005. Fundac- a˜o SOS Mata Atlaˆntica and Instituto de Pesquisas Espaciais, Sa˜o Paulo. Gine´, G.A.F., 2009. Ecologia e comportamento do ouric- opreto (Chaetomys subspinosus, Olfers 1818) em fragmentos de Mata Atlaˆntica do municı´pio de Ilhe´us, sul da Bahia. Tese de Doutorado, Universidade de Sa˜o Paulo, Piracicaba. IUCN, 2009. IUCN red list of threatened species. Version 2009.1. /www.iucnredlist.orgS. Downloaded on 09 July 2009. Jackson, J.F., 1978. Seasonality of flowering and leaf-fall in a Brazilian subtropical lower montane moist forest. Biotropica 10, 38–42. Kuniy, A.A., Rossi, L., Gomes, E.P.C., 2005. Ana´lise do conteu´do estomacal e intestinal de dois espe´cimes de ourico-preto (Chaetomys subspinosus Olfers, 1818). Acta Biol. Leopoldensia 27, 187–189.
545
Laurance, W.F., 2009. Conserving the hottest of the hotspots. Biol. Conserv. 142, 1137. Lawler, I.R., Foley, W.J., Eschler, B.M., Pass, D.M., Handasyde, K., 1998. Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116, 160–169. Martin, T., 1994. On the systematic position of Chaetomys subspinosus (Rodentia: Caviomorpha) based on evidence from the incisor enamel microstructure. J. Mamm. Evol. 2, 117–131. Martinez, R.A., Gine´, G., Le-Pendu, Y., Alvarez, M., Faria, D., 2005. Algumas considerac- o˜es sobre a anatomia interna e externa do ouric- o-preto Chaetomys subspinosus Olfers 1818 (Rodentia: Erethizontidae). In: UFES/Sociedade Brasileira de Mastozoologia, Livro de Resumos do III Congresso Brasileiro de Mastozoologia. UFES, Vito´ria, pp. 105. McNab, B.K., 1978. Energetics of arboreal folivores: physiological problems and ecological consequences of feeding on an ubiquitous food supply. In: Montgomery, G.G. (Ed.), The Ecology of Arboreal Folivores. Smithsonian Institution Press, Washington, DC, pp. 153–162. Milton, K., 1998. Physiological ecology of howlers (Alouatta): energetic and digestive considerations and comparison with the Colobinae. Int. J. Primatol. 19, 513–548. Moojen, J., 1952. Os roedores do Brasil, vol. 1. Instituto Nacional do Livro, Rio de Janeiro. Myers, N., Mittermeier, R.A., Fonseca, G.A.B., Kent, J., 2000. Biodiversity hotspots for conservation priorities. Nature 403, 853–858. Nowak, R.M., Paradiso, J.L., 1983. Walker’s Mammals of the World. The Johns Hopkins University Press, Baltimore, London. Oliveira, P.A., 2006. Ecologia do ouric- o-preto Chaetomys subspinosus (Olfers 1818) (Rodentia: Erethizontidae) no Parque Estadual Paulo Ce´sar Vinha, Guarapari, Espı´rito Santo. Dissertac- a˜o de Mestrado, Pontifı´cia Universidade Cato´lica/Minas Gerais. Oliver, W.L.R., Santos, I.B., 1991. Threatened endemic mammals of the Atlantic forest region of south-eastern Brazil. Wildl. Preserv. Trust Spec. Sci. Rep. 4, 1–126. Passamani, M. Use of space and activity pattern of Sphiggurus villosus (F. Cuvier, 1823) from Brazil (Rodentia: Erethizontidae). Mamm. Biol. (2009), in press doi:10.1016/j. mambio.2009.04.005. Patterson, B., Wood, A.E., 1982. Rodents from the Deseadan Oligocene of Bolivia and the relationships of the Caviomorpha. Bull. Mus. Comp. Zool. 149, 371–573. Pereira Junior, J., Moreira, A.C.C., Hottz, D., Paula, R.R., Somner, G.V., Menezes, L.F.T., 2007. Ana´lise Estrutural de uma Formac- a˜o Vegetal Arbustiva Aberta na Restinga da Marambaia-RJ. Rev. Bras. Biocieˆnc. 5, 366–368. Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J., Hirota, M.M., 2009. The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 142, 1141–1153. Robbins, C.T., 1993. Wildlife Feeding and Nutrition, second ed Academic Press, San Diego. Roze, U., 1984. Winter foraging by individual porcupines. Can. J. Zool. 12, 2425–2428.
546
R.B. de Souto Lima et al. / Mamm. biol. 75 (2010) 538–546
Roze, U., 1989. The North American Porcupine. Smithsonian Institution Press, Washington, DC, pp. 87–105. Roze, U., Ilse, L.M., 2003. Porcupine. In: Feldhamer, G.A., Thompson, B.C., Chapman, J.A. (Eds.), Wild Mammals of North America second ed Johns Hopkins University Press, Baltimore, London, pp. 371–380. Santos Junior, T.S., 1998. Monitoramento de Coendou prehensilis (Rodentia: Erethizontidae) resgatados no reservato´rio da Usina Hidrele´trica de Miranda (MG) e translocados para a Reserva de Jacob, Nova Ponte, MG. Dissertac- a˜o de Mestrado, Universidade Federal de Brası´lia, Brası´lia. Silva, A.F., Oliveira, R.V., Santos, N.R.L., Paula, A., 2003. Composic- a˜o florı´stica e grupos ecolo´gicos das espe´cies de um trecho de floresta semidecı´dua submontana da ´ rvore 27, Fazenda Sa˜o Geraldo, Vic- osa-MG. Rev. A 311–319. Sztutman, M., Rodrigues, R.R., 2002. O mosaico vegetacional numa a´rea de floresta contı´nua da planı´cie litoraˆnea, Parque
Estadual da Campina do Encantado, Pariquera-Ac- u, SP. Rev. Bras. Bot. 25, 161–176. Talora, D.C., Morellato, P.C., 2000. Fenologia de espe´cies arbo´reas em florestas de planı´cie litoraˆnea do sudeste do Brasil. Rev. Bras. Bot. 23, 13–26. Vilela, R.V., Machado, T., Ventura, K., Fagundes, V., Silva, M.J.J., Yonenaga-Yassuda, Y., 2009. The taxonomic status of the endangered thin-spined porcupine, Chaetomys subspinosus (Olfers, 1818), based on molecular and karyologic data. BMC Evol. Biol. 9, 29. Wilson, D.E., Reeder, D.M., 2005. Mammal Species of the World: A Taxonomic and Geographic Reference, third ed The Johns Hopkins University Press, Baltimore. Woods, C.A., 1993. Suborder Hystricognathi. In: Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species of the World: A Taxonomic and Geographic Reference second ed Smithsonian Inst. Press, Washington, DC, pp. 771–806.
ORIGINAL INVESTIGATION
Diet of the thin-spined porcupine (Chaetomys subspinosus), an Atlantic forest endemic threatened with extinction in southeastern Brazil Rodrigo B. de Souto Lima, Pedro A. Oliveira, Adriano G. Chiarello Programa de Po´s-graduac- a˜o em Zoologia de Vertebrados, Pontifı´cia Universidade Cato´lica de Minas Gerais (PUC-Minas), Avenida Dom Jose´ Gaspar 500, Pre´dio 41, Belo Horizonte 30535-610, Minas Gerais, Brazil Received 13 July 2009; accepted 11 September 2009
Abstract Chaetomys is a poorly known, monotypic genus of tree porcupine threatened with extinction due to deforestation and habitat fragmentation. Its nocturnal habit, relatively restricted distribution and low level of activity have conspired for decades against detailed field studies. Here the diet of the species in restinga forests is described for the first time. Restinga is a subtype of lowland Atlantic forest occurring on sandy soils close to the Atlantic littoral in Brazil. Three radio-collared females were monitored for 12 months between March 2005 and February 2006. Leaves were the most heavily consumed dietary item, varying from 71.9% to 75.4% of the diet of each individual, followed by flowers (7.7% - 15.7%) and fruits (0 - 1.4%). Animals fed on 57 trees from 14 species, with a higher concentration on Pera glabrata (49.8%) and Tapiriria guianensis (22.7%). Pera glabrata is locally abundant and widely distributed in the Atlantic forest. Each individual consumed a smaller subset of plant species (4-10 species/individual) and shared only the two most important tree species (P. glabrata and T. guianensis). Results corroborate previous studies indicating that Chaetomys is a folivore, perhaps the most folivorous amongst the Erethizontidae. Since the most consumed plant species are relatively common and widespread, Chaetomys might thrive in a broader range of habitats than previously suspected, including secondary forests. & 2008 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. Keywords: Erethizontidae; Feeding habits; Folivore; Atlantic forest
Introduction Chaetomys subspinosus is an arboreal rodent endemic ´ vilato the Atlantic forest of Brazil (Moojen 1952; A Pires 1967; Coimbra-Filho 1972). Its taxonomic position has been controversial in the past, with some authorities including it in the spiny rat family (Echimyidae) (Patterson and Wood 1982; Woods 1993), others putting it among the Neotropical porcupines (Erethizontidae) (Moojen 1952; Cabrera 1961; Nowak and Paradiso Corresponding author. Tel./fax: +51 31 3319 4967.
E-mail address: [email protected] (A.G. Chiarello).
1983; Martin 1994; Carvalho 2000; Wilson and Reeder 2005). A recent and comprehensive molecular study confirms that Chaetomys is a basal but true member of the Erethizontidae (Vilela et al. 2009). Chaetomys subspinosus is one of the most distinct and poorly known species of the Atlantic forest (Oliver and Santos 1991). It is threatened with extinction due to habitat destruction, forest fragmentation and subsistence hunting (Chiarello et al. 2008; IUCN 2009). The Atlantic forest is an ecosystem extremely impacted by human disturbance, occupying today about 11.3% of its original extent (Ribeiro et al. 2009). Due to its high species richness, degree of endemisms and area reduction the
1616-5047/$ - see front matter & 2008 Deutsche Gesellschaft fu¨r Sa¨ugetierkunde. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2009.09.002 Mamm. biol. 75 (2010) 538–546
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Atlantic forest is considered a top biological hotspot (Myers et al. 2000; Laurance 2009). The observation of C. subspinosus in nature is difficult due to a combination of factors: small body size, cryptic coloration, low level of activity and slow and silent movement in the dense forest canopy. Even trained observers with adequate equipment (binoculars and powerful lights) might find it difficult to record accurate data on feeding and behavior. As a consequence, there are few ecological studies on the species. In a pioneering study Chiarello et al. (1997) managed to observe a translocated radio-collared individual for three nights. More recently Kuniy et al. (2005) reported the stomach contents of two individuals captured in northern Bahia. The only comprehensive studies on the ecology of free ranging individuals were carried out recently in Espı´rito Santo (Oliveira 2006), from which the present contribution derives, and in southern Bahia (Gine´ 2009). Available dietary data on diet indicates that Chaetomys is strongly folivorous (Chiarello et al. 1997; Gine´ 2009). Arboreal mammals with folivorous diets have low levels of metabolism and activity (McNab 1978). This is because leaves are poor in readily available energy such as sugars and starch and are difficult to digest (McNab 1978; Cork and Foley 1991; Milton 1998). Apart from poor digestibility, leaves are protected by chemical substances like alkaloids and tannins that inhibit their digestion both by vertebrates and invertebrates (Freeland 1991). Notwithstanding the feeding inhibitors, folivory is common among Erethizontids. Sphiggurus villosus, which is sympatric with Chaetomys, seems to be strictly folivorous (Passamani in press) and Coendou prehensilis, which is a wider ranging member of the family, is considered folivorous-frugivorous (Emmons and Feer 1997; Eisenberg and Redford 1999), although Santos-Ju´nior (1998) reports a higher ingestion of fruits than leaves in translocated individuals of this species. Erethizon dorsatum, the North American porcupine feeds on leaves of trees and shrubs, fruits, nuts, tree bark, aquatic plants, grasses and even cacti (Roze and Ilse 2003). Here we used radio telemetry and direct observation to investigate the feeding habits of three free-ranging Chaetomys in a forest reserve located in Espı´rito Santo state, southeastern Brazil. The study area was restinga, a subtype of lowland Atlantic forest that occurs close to the littoral on sandy soils. This vegetation formation is mostly gone since it occurs in areas highly impacted by city sprawl, tourism development and road construction. As a result, less than 0.5% of the Atlantic forest is represented today by restingas (Fundac- a˜o SOS Mata Atlantica and Instituto de Pesquisas Espaciais 2008; Ribeiro et al. 2009). Nevertheless, recent studies indicate that Chaetomys occurs predominantly in restingas rather than in forest formations located further inland (Chiarello et al. 2008). Thus results reported here apart from adding to the natural history of a poorly known
539
Erethizontid, might help define the niche characteristics of the species, which is needed for a proper planning of its conservation management.
Material and methods Study area The study area is within the limits of a state park (Parque Estadual Paulo Ce´sar Vinha-PEPCV), located in the littoral of Espı´rito Santo state in southeastern Brazil (201330 -201380 S and 401230 -401260 W). The area is a sandy plain only a few meters above the sea level. Annual average temperature is 23.3 1C and annual average precipitation is 1307 mm (Fabris and Ce´sar 1996). Vegetation is a mosaic of restinga forest, open shrub vegetation and seasonally flooded areas. The restinga forest, the only vegetation formation used by Chaetomys (Oliveira 2006) contains 172 plant species distributed in 54 families (Assis et al. 2004a). Its higher strata are on average 8 m tall and some emergent trees reach 20 m. The most common families are Myrtaceae, Sapotaceae, Annonaceae, Bombacaceae and Meliaceae (Assis et al. 2004b). Epiphytes and lianas are abundant.
Data collection Study animals were located in their diurnal resting sites after intensive searches helped by a local inhabitant. After sedation with a mixture of ketamine (5 mg/kg of body weight) and xylazine (2 mg/kg of body weight), a VHF transmitter attached to a ball and chain collar was fitted to the neck region of each animal. The collars weighed 60 g (Telonics Inc., model 205), which represents less than 3% of the body weight. After a few nights the animals seemed to ignore the presence of the collars. Highly reflective tapes of the type used in road transport were attached to the transmitters, greatly increasing the chances of finding and monitoring a radio-collared animal even in dense vegetation. After recovering from the anesthesia the animals were released in the tree of capture. Three individuals, all adult females, were radio-collared. We tried hard to find males in the area but failed. The observations began 20 days after the capture date (Table 1). The observations were carried out monthly between March 2005 and February 2006. One individual (Ch970) was monitored for 10 months until it was found dead in the 11th month. The cause of death was unknown. The second (Ch160) could not be monitored in one month because the area it inhabited was temporarily flooded and therefore it was observed for 11 months, and the third (Ch274) was monitored for 12 months. Each animal was observed one night per month during the first five hours after
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Table 1. Animal
Ch-970 Ch-274 Ch-160 Total
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Monitoring period and sampling effort of the three radio-collared C. subspinosus. Weight (g)
2700 2200 2100
Capture date
04/03/2005 04/03/2005 05/03/2005
Monitoring
Number of scans
Period
Nights
25/03 to 13/11/2005 25/03/2005 to 21/02/2006 27/03/2005 to 22/02/2006
10 12 11 33
darkness, generally between 18:00 and 23:00 h [darkness began one hour earlier in the peak of winter (JuneAugust) and one hour later in the peak of summer (December-February)]. Previous studies indicate that a greater part of activity and feeding takes place in this period (Chiarello et al. 1997; Gine´ 2009). The animals were radio located in the afternoon in their diurnal resting sites using a receptor and a three-element Yagi antenna (Titley Electronicss, model Regal 2000). Once the study animal was located we waited for the animal to begin activity, which in general started only after the sunset. Binoculars (8 40), handheld torches (rechargeable Maglites with 12 watt halogen bulb) and head lamps (3 watt Petzl Duos) were used in the observations, which were always conducted by two observers. In the beginning of the study we realized that if the central focus of the Maglites was directed to the animal it tended to react stopping activity. So in order to avoid disturbing the normal rhythm of activity we directed the focus of the Maglites to the side of the animal, insuring that sufficient light was available for accurate observation without disturbing the animal. At the end of the study the animals were recaptured, had their collars removed, and were released in the forest. The consumption of tree species was quantified recording the duration of feedings bouts using a digital chronometer. A feeding bout was defined as beginning the moment when the animal was in the canopy of a tree, bringing food to the mouth or chewing plant parts. The feeding bout ended when the animal stopped chewing or manipulating plant parts. Feeding bouts of any duration were recorded. The consumed trees were marked with a colored tape, numbered for later collection of reproductive parts and identification by a botanist with a strong experience in local flora (Dr. Oberdan J. Pereira, Universidade Federal do Espı´rito Santo). The importance of each plant species in the diet was calculated by dividing the time spent feeding in each tree species by the total time spent feeding in all tree species and expressing the result as a percentage. Due to difficulties of observation, the quantification of tree part consumption (leaves, fruit, flower, other) was done differently. We used scan sampling (Altmann 1974) at every 10 minutes to record five mutually exclusive
hh:mm 47:20 52:20 51:10 150:50
356 347 337 1040
categories: resting, moving, feeding, other and indeterminate. Here we considered only the scans relative to feeding. The number of scans of each consumed item was tallied and the importance of each item was expressed as percentage of the total number of feeding scans.
Data analysis To determine whether leaves are the most important food item both annually and seasonally (dry versus wet season) we first calculated the daily number of scans recorded for each consumed item. Dry season was defined as the period between April and September and wet season between October and March. Then we calculated the percentage of scans recording leaves and recording all other items put together (flower+fruit+ other). We contrasted the percentage of scans of leaves x other items using the Wilcoxon signed rank test. A similar procedure was used to compare young x mature leaf consumption. The only difference is that here we excluded data from the first three months [March, April and May (one wet season month and two dry season months)] because in the beginning of the study it was difficult to discern if the study animals were feeding on young or mature leaves. We used the Spearman rank correlation (rs) to compare the percentage of consumed species between seasons. All tests were performed with the software SPSS version 17.
Results Chaetomys subspinosus has a stereotypical behaviour when eating. Study animals usually climbed to the highest part of the tree crown and reached for the branch tips. When they arrived at this part, they sat on their hind limbs and anchored their tails around firm branches, leaving their fore limbs free to grab thinner, flexible twigs and bring them to the front of their heads. Then the leaves or other item on these twigs were apparently smelled, and if selected they were brought to the mouth, chewed and swallowed. In many occasions only the leaf blades were eaten, leaving the petioles intact. Animals always fed in trees: in all thirty-three observation nights none of the three study animals ever came down to feed
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on the ground. Leaves were the most abundant item in the diets of all three C. subspinosus (Fig. 1), with small variation between individuals (74.16% - 79.71%). Flowers were the second most consumed item (7.69% 15.73%), while fruits were consumed only rarely (0 1.45%). The identification of the consumed item was not possible in 11.66% of feeding scans. None of the animals ever fed on lianas or epiphytes, despite their great abundance in the study area.
Fig. 1. Diet composition of three radio-collared Chaetomys subspinosus. Proportion of items recorded in ‘‘feeding’’ scans.
541
Leaves were eaten significantly more often than all other items put together in both dry and wet season (Table 2). Although the consumption of items other than leaves increased during the rainy season, this increase was only marginally significant (MannWhitney, p=0.075). The utilization of flowers, fruits and shoots usually occurred in an opportunistic manner, when those items were available among the leaves that were eaten in higher amount. On an annual basis the consumption of mature leaves was higher than that of young leaves, but the difference was not significant. Analyzing the seasons separately, young leaves were consumed significantly more often than mature leaves in the rainy season, while the opposite was observed in dry season (Table 3). The three study animals consumed plant parts from 57 individual trees belonging to 14 species and 9 families. Seven trees used by the animals for feeding couldn’t be collected and therefore were not identified. Over 80% of the total feeding time was allocated to Euphorbiaceae and Anacardiaceae. The genus Pera (Euphorbiaceae) alone represented 58.09% of the diet. Pera glabrata was the most important species for all three animals, representing on average 49.85% of their diet. The only other tree species consumed by all three study animals was Tapirira guianensis, but its relative importance varied (Table 4). These top two plant species accounted for 88.36% of the diet of Ch 970, 73.56% for Ch 160, and 65.71% for Ch 274. The total number of tree species consumed by each study animal varied from 4 to 10 species (Table 4). The Fig. 2 shows a slight
Table 2. Annual and seasonal variation in the diet of three females C. subspinosus, expressed as percentage of feeding scans recorded within and between season comparisons (Wilcoxon and Mann-Whitney tests, respectively). (p): test significance. Season
Rainy Dry Mann-Whitney (p) Annual
n
13 18 31
Leaves
Other items
Wilcoxon
Average
s.d.
Average
s.d.
71.64 82.75 0.075 78.09
19.55 29.14
28.36 17.25 0.075 21.91
19.55 29.14
0.006 0.002
25.79
o0.001
25.79
p
Table 3. Annual and seasonal variation in the consumption of young and mature leaves by three females C. subspinosus, expressed as percentage of feeding scans recorded for the item ‘‘leaf’’. Within and between season comparisons measured by Wilcoxon and Mann-Whitney tests, respectively. (p): test significance. Season
Rainy Dry Mann-Whitney (p) Annual
n
12 12 24
Young leaves
Mature leaves
Wilcoxon
Average
s.d.
Average
s.d.
p
69.44 1.28 0.0008 35.36
35.58 4.44
30.56 98.71 0.0008 64.64
30.58 4.44
0.058 0.001
40.85
0.106
40.85
542
Table 4.
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Time spent feeding (in minutes and percentages) on each tree species by the three females C. subspinosus.
Species/Family
Pera glabrata/Euphorbiaceae Tapirira guianensis/Anarcadiaceae Pera leandri/Euphorbiaceae Matayba guianensis/Sapindaceae Inga fagifolia/Fabaceae Humiria balsamifera/Humiriaceae Zollernia glabra/Fabaceae Myrtaceae sp 1./ Myrtaceae Inga laurina/Fabaceae Manilkara subsericea/Sapotaceae Moraceae sp 1/Moraceae Eugenia punicifolia/Myrtaceae Coccoloba alnifolia/Polygonaceae Psidium macahense/Myrtaceae TOTAL
Ch 970
Ch 274
Ch 160
Total
Min.
%
Min.
%
Min.
%
Min.
308 292 53
45.36 43.00 7.81
236 71 86
48.16 14.49 17.55
297 20
57.34 3.86
35 55
7.14 11.22
84 40
16.22 7.72
43
8.30
18 8
3.47 1.54
5 2 1 518
0.97 0.39 0.19 100
841 383 139 84 75 55 43 26 18 8 7 5 2 1 1687
26
3.83
7
679
100
490
1.43
100
% 49.85 22.70 8.24 4.98 4.45 3.26 2.55 1.54 1.07 0.47 0.41 0.30 0.12 0.06 100
P. glabrata and T. guianensis individuals were never eaten although they were traversed by the study animals.
Discussion
Fig. 2. Accumulated number of plant species consumed by the three radio-collared animals along the monitoring period. The upper line shows the combined diet of all three animals.
tendency to curve stabilization for each animal considered separately, but when data from the three animals are combined the curve was still ascending by the end of the study period. There was no significant correlation in tree species importance (% in diet) between the dry and wet seasons (Spearman rank correlation coefficient, rs=0.367, N=14, p=0.197). Nevertheless, the two most important tree species (P. glabrata and T. guianensis) remained the same in both seasons (Table 5). A smaller number of species (n=7) was used as source of food in the wet season than in dry season (n=12) (Table 5). Besides selecting certain tree species as food sources, Chaetomys subspinosus also seems to select individual trees. Some individual trees were fed upon repeatedly in distinct observation nights, while others from the same species were ignored, despite their close proximity. Some
Results show important individual variations both in terms of species consumed and their relative importance in the diet. These differences are partly due to distinct characteristics of the home range of each individual, which did not overlap and were widely separated from one another. The forest fragments in which the study animals lived were separated by marshlands or sandy areas with shrubby vegetation, and apparently each home range has a distinct floristic composition. The home ranges of Ch970 and Ch274 were far closer to each other than to the Ch160 and, in fact three of the four species consumed by Ch970 were also consumed by Ch274. The forest fragment where Ch160 lived was larger than that of the other two. Perhaps due to this higher diversity Ch160 included a higher number of tree species in its diet than did the other two animals. On the other hand, Ch160 was the only female not observed suckling an infant during the study. Females during lactation have higher energy demand than non-lactating females (Robbins 1993). Thus the low diversity diet of both Ch970 and Ch274 might result, alternatively, from a more conservative foraging strategy of these lactating females. Leaves were the most commonly consumed item throughout the year. Similarly, Gine´ (2009) did not notice significant differences between seasons in the main items consumed by Chaetomys observed in southern Bahia, although he did record significant seasonal
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Table 5.
543
Time spent feeding on each tree species according to season.
Species/Family
Pera glabrata/Euphorbiaceae Tapirira guianensis/Anarcadiaceae Pera leandri/Euphorbiaceae Matayba guianensis/Sapindaceae Inga fagifolia/Fabaceae Humiria balsamifera/Humiriaceae Zollernia glabra/Fabaceae Myrtaceae sp 1/Myrtaceae Inga laurina/Fabaceae Manilkara subsericea/Sapotaceae Moraceae sp 1/ Moraceae Eugenia punicifolia/Myrtaceae Coccoloba alnifolia/Polygonaceae Psidium macahense/Myrtaceae TOTAL
Dry season
Rainy season
Minutes
%
Minutes
%
348 237 139 31
41.23 28.08 16.47 3.67
493 146
58.48 17.32
20 20 26
2.37 2.37 3.08
53 75 35 23
6.29 8.90 4.15 2.73
18
2.14
8 7 5 2 1 844
0.95 0.83 0.59 0.24 0.12 100
variation in food availability in the forest. In PEPCV young leaves were consumed more often than mature leaves during the wet season, a period of the year when new leaves are more available, at least in the forests of the region (Jackson 1978). Although the phenology of the study area was not monitored, this area has a pattern of precipitation and temperature similar to that of Santa Teresa, where the study of Jackson (1978) was carried out. Thus the phenological pattern might be similar between these two areas. In another restinga forest in Ubatuba, state of Sa˜o Paulo, Talora and Morelato (2000) also recorded higher availability of new leaves during wet season. Among the members of Erethizontidae whose diet is known, Chaetomys is probably one of the most folivorous (Roze 1989; Santos Ju´nior 1998; Eisenberg and Redford 1999; Gine´ 2009; Passamani in press). The frugivory speculated by Kuniy et al. (2005) should be viewed with care since it was based on the contents of just two stomachs. Chaetomys subspinosus is apparently a caecal fermenter since its caecum is enlarged and differentiated (Martinez et al. 2005, Gine´ 2009). Caecal fermentation with some specialization for retention and separation of particulates is essential for small-bodied mammals with a high degree of folivory such as Chaetomys, because it allows a higher passage rate and a lower loss of nitrogen in feces, increasing the efficiency of the digestive process (Cork 1996). The lethargic behavior observed in this species (Chiarello et al. 1997; Oliveira 2006; Gine´ 2009) is also an adaptation to a strongly folivorous diet. Arboreal folivores have activity and metabolic rates lower than expected due to the low caloric value of leaves, presence of feeding deterrents (secondary compounds) in leaves, and also due to relatively small body masses (McNab 1978; Cork and Foley 1991).
843
100
Freeland (1991) states that smaller mammals detoxify and eliminate secondary compounds more rapidly than larger mammals, allowing the first to specialize on a lower number of plant species than the latter. Chaetomys concentrates its feeding on a few plant species. From a pool of at least 92 tree species known to exist in PEPCV (Assis et al. 2004b) only 14 were consumed by the three study animals, each of which consumed an even smaller subset of species. Further, only three species made up more than 80% of the diet. Gine´ (2009) also found a small number of plant species (n=17) consumed by the four individuals observed by him in southern Bahia, where dense rain forest (ombrophilous) predominates. Since this type of forest is probably richer in plant species than the restinga forest of PEPCV, the degree of diet specialization might be even higher in Bahia. Roze (1984) reports similar results for the North American pocupine Erethizon dorsatum in winter. This population consumed 10 tree species in total but each individual concentrated on one or two species and the top three species made up 80% of the population0 s diet (Roze 1984). Similarly, the translocated Coendou prehensilis observed by Santos Ju´nior (1998) fed on a total of 14 species, with a strong concentration on three species. It seems therefore that Chaetomys follows the same feeding pattern observed by other Erethizontids and some sympatric arboreal folivores such as the maned sloth Bradypus torquatus (Chiarello 1998). Analyzing the two lists of consumed species available thus far (present study and Gine´ 2009) we observe that three genera (Pera, Tapirira and Inga) were common to the two diets, that is, only 14% of the 21 genera were shared by the species. If we compare tree species, the percentage of overlap decreases to 7% (2 species out of
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27 taxa identified to the species level). This finding suggest that Chaetomys might be considered a generalist at the population level but a specialist at the individual level, similar to what has been observed for Bradypus sloths (Chiarello 1998). One may speculate that the strong concentration on Pera is due to two main aspects: availability in the forest and nutrient composition. Availability has been observed to be an important selection criterion in the diet of E. dorsatum (Roze 1984). Botanic studies in restingas (Assumpc- a˜o and Nascimento 2000; Assis et al. 2004b) indicate that P. glabrata is relatively common in these environments. Since P. glabrata has a wide geographic distribution (Assis et al. 2004b), it is possible that this species is important in the diet of Chaetomys in other Atlantic forest physiognomies as well. In fact, Pera glabrata was the third most heavily consumed species in Bahia representing more than one third of the Chaetomys diet there (Gine´ 2009). However, in southern Bahia Pera glabrata is not a highly abundant species (Gine´ 2009). This suggests that abundance may play a role but it is not the only criterion in the selection process. Gine´ (2009) measured the amount of dry matter, protein, fiber, among other dietary components of the seven plants most consumed by Chaetomys and concluded that the preferred ones were particularly rich in proteins and fiber. However, Pera glabrata ranked lowest in amount of protein and the highest in amount of fiber among the top seven consumed species. It is therefore likely that other nutrients or the amount and toxicity of secondary compounds might be more relevant for the selection of this plant genus by Chaetomys. The fact that some individuals of P. glabrata within the home range of the study animals were visited and consumed regularly while others were ignored or were less visited lends support to this hypothesis. The same was observed for Tapiriria guianensis, the second most consumed plant in PEPCV. Several studies show that herbivore mammals select among individuals of a given plant species for feeding. Australian marsupials (Phascolarctos cinereus and Pseudocheirus peregrinus) for example, select among individual Eucalyptus according to the amount of DFP, a phenolic compound (Lawler et al. 1998). For North American porcupines feeding on Populus tremuloides, some genets are preferred over others, based on the levels of two phenolic glycosides in the food trees (Diner et al. 2009). As there are few similarities between the diet studies available thus far, it seems that Chaetomys is not highly specialized in terms of habitat requirements. The most important tree species consumed are pioneers, have a relatively wide geographic distribution and may even be tolerant of forest disturbances. This is the case of Pera glabrata and Tapiriria guianensis in the present study (Pereira Junior et al. 2007; Silva et al. 2003; Sztutman and Rodrigues 2002). In southern Bahia six out of the
seven most important species are typical of the early stages of succession (Gine´ 2009). This spells good news for the conservation of the species since within its geographic distribution Chaetomys might be present in more habitat types than previously expected. Further, the rarity of records of this species might be more related to its cryptic behavior and nocturnal habit than to restrict feeding preferences.
Acknowledgements This study was financed by Ministerio do Meio Ambiente through a PROBIO grant and by PUC Minas through Fundo de Incentivo a Pesquisa grant. Museu de Biologia Prof. Melo Leita˜o and PEPCV offered valuable logistic support. We worked together with Instituto Drı´ades in this project and are particularly indebted to Deborah Faria and Gaston Gine´ for their help and feedback. The Brazilian environmental Agency (IBAMA) provided authorization for capturing the animals. We would like to thank Dr. Oberdan J. Pereira for plant identification, Mister Toninho for finding and capturing the porcupines, and Ne´lson Curi for veterinary support. Dr. Uldis Roze kindly reviewed an early version of this manuscript. The Brazilian Science Council (CNPq) and the Fundac- a˜o de Amparo a Pesquisa de Minas Gerais (FAPEMIG) provided research grants to AGC during data analysis.
References Altmann, J., 1974. Observational study of behavior: sampling methods. Behavior 49, 227–267. Assis, A.M., Thomaz, L.D., Pereira, O.J., 2004a. Florı´stica de uma Floresta de Restinga no Municı´pio de Guaraparı´, Espı´rito Santo, Brasil. Acta Bot. Bras. 18, 191–201. Assis, A.M., Pereira, O.J., Tomaz, L.D., 2004b. Fitossociologia de uma floresta de Restinga no Parque Estadual Paulo Ce´sar Vinha, Setiba, municı´pio de Guarapari (ES). Rev. Bras. Bot. 27, 349–361. Assumpc- a˜o, J., Nascimento, M.T., 2000. Estrutura e composica˜o de quatro formac- o˜es vegetais de restinga no complexo lagunar Grussaı´/Iquipari, Sa˜o Joa˜o da Barra, RJ, Brasil. Acta Bot. Bras. 14, 301–315. ´ vila-Pires, F.D., 1967. The type-locality of ‘‘Chaetomys A subspinosus’’ (Olfers, 1818) (Rodentia, Caviomorpha). Museu Nacional, Rio de Janeiro. Rev. Bras. Biol. 27, 177–179. Cabrera, A., 1961. Cata´logo de los mamı´feros de Ame´rica del Sur, vol. 2. Rev. Mus. Argent. Cienc. Nat. Bernardino Rivadavia 4, 309–732. Carvalho, G., 2000. Substitution of the deciduous premolar in Chaetomys subspinosus (Olfers, 1818) (Hystricognathi, Rodentia) and its taxonomic implications. Z. Saugetierkd. 65, 187–190.
R.B. de Souto Lima et al. / Mamm. biol. 75 (2010) 538–546
Chiarello, A.G., Passamani, M., Zorte´a, M., 1997. Field observations on the thin-spined porcupine, Chaetomys subspinosus (Rodentia; Echimyidae). Mammalia 61, 29–36. Chiarello, A.G., 1998. Diet of the Atlantic Forest maned sloth Bradypus torquatus (Xenarthra: Bradypodidae). J. Zool. London 246, 11–19. Chiarello, A.G., Aguiar, L.M.S., Cerqueira, R., Melo, F.R., Rodrigues, F.H.G., Silva, V.M.F., 2008. Mamı´feros Ameacados de Extinc- a˜o no Brasil. In: Machado, A.B.M., Drummond, G.M., Paglia, A.P. (Eds.), Livro Vermelho da Fauna Brasileira Ameac- ada de Extinc- a˜o. MMA and Fundaca˜o Biodiversitas, Brası´lia and Belo Horizonte, pp. 680–874. Coimbra-Filho, A.F., 1972. Mamı´feros ameac- ados de extinc- a˜o no Brasil. In: Espe´cies da Fauna Brasileira Ameac- adas de Extinc- a˜o. Academia Brasileira de Cieˆncias, Rio de Janeiro, pp. 13–98. Cork, S.J., 1996. Optimal digestive strategies for arboreal herbivorous mammals in contrasting forest types: why Koalas and Colobines are different. Aust. J. Ecol. 21, 10–20. Cork, S.J., Foley, W.J., 1991. Digestive and metabolic strategies of arboreal mammalian folivores in relation to chemical defenses in temperate and tropical forests. In: Palo, R.T., Robbins, C.T. (Eds.), Plant Defenses Against Mammalian Herbivory. CRC Press, Boca Raton, pp. 133–166. Diner, B., Berteaux, D., Fyles, J., Lindroth, R.L., 2009. Behavioral archives link the chemistry and clonal structure of trembling aspen to the food choice of North American porcupine. Oecologia 160, 687–695. Eisenberg, J.F., Redford, K.H., 1999. Mammals of the Neotropics. The Central Neotropics, vol. 3, Ecuador, Peru, Bolivia, Brazil. The University of Chicago Press, Chicago. Emmons, L.H., Feer, F., 1997. Neotropical Rainforest Mammals: A Field Guide, second ed University of Chicago Press, Chicago. Fabris, L.C., Ce´sar, O., 1996. Estudos florı´sticos em uma mata litoraˆnea no sul do estado do Espı´rito Santo, Brasil. Boletim do Museu de Biologia Mello Leita˜o 5, 15–46 (ISSN: 0103-9121). Freeland, W.J., 1991. Plant secondary metabolites: biochemical coevolution with herbivores. In: Palo, R.T., Robbins, C.T. (Eds.), Plant Defenses Against Mammalian Herbivory. CRC Press, Boca Raton, pp. 61–81. Fundac- a˜o SOS Mata Atlaˆntica, Instituto de Pesquisas Espaciais, 2008. Atlas dos Remanescentes Florestais da Mata Atlaˆntica: Perı´odo 2000 a 2005. Fundac- a˜o SOS Mata Atlaˆntica and Instituto de Pesquisas Espaciais, Sa˜o Paulo. Gine´, G.A.F., 2009. Ecologia e comportamento do ouric- opreto (Chaetomys subspinosus, Olfers 1818) em fragmentos de Mata Atlaˆntica do municı´pio de Ilhe´us, sul da Bahia. Tese de Doutorado, Universidade de Sa˜o Paulo, Piracicaba. IUCN, 2009. IUCN red list of threatened species. Version 2009.1. /www.iucnredlist.orgS. Downloaded on 09 July 2009. Jackson, J.F., 1978. Seasonality of flowering and leaf-fall in a Brazilian subtropical lower montane moist forest. Biotropica 10, 38–42. Kuniy, A.A., Rossi, L., Gomes, E.P.C., 2005. Ana´lise do conteu´do estomacal e intestinal de dois espe´cimes de ourico-preto (Chaetomys subspinosus Olfers, 1818). Acta Biol. Leopoldensia 27, 187–189.
545
Laurance, W.F., 2009. Conserving the hottest of the hotspots. Biol. Conserv. 142, 1137. Lawler, I.R., Foley, W.J., Eschler, B.M., Pass, D.M., Handasyde, K., 1998. Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116, 160–169. Martin, T., 1994. On the systematic position of Chaetomys subspinosus (Rodentia: Caviomorpha) based on evidence from the incisor enamel microstructure. J. Mamm. Evol. 2, 117–131. Martinez, R.A., Gine´, G., Le-Pendu, Y., Alvarez, M., Faria, D., 2005. Algumas considerac- o˜es sobre a anatomia interna e externa do ouric- o-preto Chaetomys subspinosus Olfers 1818 (Rodentia: Erethizontidae). In: UFES/Sociedade Brasileira de Mastozoologia, Livro de Resumos do III Congresso Brasileiro de Mastozoologia. UFES, Vito´ria, pp. 105. McNab, B.K., 1978. Energetics of arboreal folivores: physiological problems and ecological consequences of feeding on an ubiquitous food supply. In: Montgomery, G.G. (Ed.), The Ecology of Arboreal Folivores. Smithsonian Institution Press, Washington, DC, pp. 153–162. Milton, K., 1998. Physiological ecology of howlers (Alouatta): energetic and digestive considerations and comparison with the Colobinae. Int. J. Primatol. 19, 513–548. Moojen, J., 1952. Os roedores do Brasil, vol. 1. Instituto Nacional do Livro, Rio de Janeiro. Myers, N., Mittermeier, R.A., Fonseca, G.A.B., Kent, J., 2000. Biodiversity hotspots for conservation priorities. Nature 403, 853–858. Nowak, R.M., Paradiso, J.L., 1983. Walker’s Mammals of the World. The Johns Hopkins University Press, Baltimore, London. Oliveira, P.A., 2006. Ecologia do ouric- o-preto Chaetomys subspinosus (Olfers 1818) (Rodentia: Erethizontidae) no Parque Estadual Paulo Ce´sar Vinha, Guarapari, Espı´rito Santo. Dissertac- a˜o de Mestrado, Pontifı´cia Universidade Cato´lica/Minas Gerais. Oliver, W.L.R., Santos, I.B., 1991. Threatened endemic mammals of the Atlantic forest region of south-eastern Brazil. Wildl. Preserv. Trust Spec. Sci. Rep. 4, 1–126. Passamani, M. Use of space and activity pattern of Sphiggurus villosus (F. Cuvier, 1823) from Brazil (Rodentia: Erethizontidae). Mamm. Biol. (2009), in press doi:10.1016/j. mambio.2009.04.005. Patterson, B., Wood, A.E., 1982. Rodents from the Deseadan Oligocene of Bolivia and the relationships of the Caviomorpha. Bull. Mus. Comp. Zool. 149, 371–573. Pereira Junior, J., Moreira, A.C.C., Hottz, D., Paula, R.R., Somner, G.V., Menezes, L.F.T., 2007. Ana´lise Estrutural de uma Formac- a˜o Vegetal Arbustiva Aberta na Restinga da Marambaia-RJ. Rev. Bras. Biocieˆnc. 5, 366–368. Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J., Hirota, M.M., 2009. The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 142, 1141–1153. Robbins, C.T., 1993. Wildlife Feeding and Nutrition, second ed Academic Press, San Diego. Roze, U., 1984. Winter foraging by individual porcupines. Can. J. Zool. 12, 2425–2428.
546
R.B. de Souto Lima et al. / Mamm. biol. 75 (2010) 538–546
Roze, U., 1989. The North American Porcupine. Smithsonian Institution Press, Washington, DC, pp. 87–105. Roze, U., Ilse, L.M., 2003. Porcupine. In: Feldhamer, G.A., Thompson, B.C., Chapman, J.A. (Eds.), Wild Mammals of North America second ed Johns Hopkins University Press, Baltimore, London, pp. 371–380. Santos Junior, T.S., 1998. Monitoramento de Coendou prehensilis (Rodentia: Erethizontidae) resgatados no reservato´rio da Usina Hidrele´trica de Miranda (MG) e translocados para a Reserva de Jacob, Nova Ponte, MG. Dissertac- a˜o de Mestrado, Universidade Federal de Brası´lia, Brası´lia. Silva, A.F., Oliveira, R.V., Santos, N.R.L., Paula, A., 2003. Composic- a˜o florı´stica e grupos ecolo´gicos das espe´cies de um trecho de floresta semidecı´dua submontana da ´ rvore 27, Fazenda Sa˜o Geraldo, Vic- osa-MG. Rev. A 311–319. Sztutman, M., Rodrigues, R.R., 2002. O mosaico vegetacional numa a´rea de floresta contı´nua da planı´cie litoraˆnea, Parque
Estadual da Campina do Encantado, Pariquera-Ac- u, SP. Rev. Bras. Bot. 25, 161–176. Talora, D.C., Morellato, P.C., 2000. Fenologia de espe´cies arbo´reas em florestas de planı´cie litoraˆnea do sudeste do Brasil. Rev. Bras. Bot. 23, 13–26. Vilela, R.V., Machado, T., Ventura, K., Fagundes, V., Silva, M.J.J., Yonenaga-Yassuda, Y., 2009. The taxonomic status of the endangered thin-spined porcupine, Chaetomys subspinosus (Olfers, 1818), based on molecular and karyologic data. BMC Evol. Biol. 9, 29. Wilson, D.E., Reeder, D.M., 2005. Mammal Species of the World: A Taxonomic and Geographic Reference, third ed The Johns Hopkins University Press, Baltimore. Woods, C.A., 1993. Suborder Hystricognathi. In: Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species of the World: A Taxonomic and Geographic Reference second ed Smithsonian Inst. Press, Washington, DC, pp. 771–806.