The influence of edge on small mammals: evidence from Brazilian Atlantic forest fragments

The influence of edge on small mammals: evidence from Brazilian Atlantic forest fragments

BIOLOGICAL CONSERVATION ELSEVIER Biological Conservation 85 (1998) 1-8 The influence of edge on small mammals: evidence from Brazilian Atlantic for...

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BIOLOGICAL CONSERVATION

ELSEVIER

Biological Conservation 85 (1998) 1-8

The influence of edge on small mammals: evidence from Brazilian Atlantic forest fragments S.M. Stevens, T.P. Husband * Department of Natural Resources Science, University of Rhode Island, Kingston. R.L 02881, USA Received 21 July 1995; received in revised form 27 November 1997; accepted 27 November 1997

Abstract

Small mammal diversity was examined in relation to distance from the forest/farmland edge in two fragments of Brazilian Atlantic forest in Sergipe, Brazil. Tolerance to and use of the edge and surrounding matrix of agricultural land by nine species of small mammals, as well as microclimatic conditions and vegetation structure were measured along 12 transects placed both inside the forest and in the surrounding matrix. As distance from edge increased into the forest, both the number of species and species diversity significantly increased, air temperature significantly decreased and relative humidity significantly increased. During the study, no small mammals were captured outside of the forest in the surrounding farmland. Of the 671 total captures, only 43 occurred along the edge, and 39 of the 43 were captures of only two species. This influence that edge may have on some small mammals may be a key to discerning a species' probability of survival in small fragments with hard edges. © 1998 Published by Elsevier Science Ltd. All rights reserved Keywords: Forest edge; Edge effect; Forest fragmentation; Tropical rain forest; Microclimate; Small mammals; Tropical mammals

1. Introduction In a fragmented landscape of forest patches, farm fields, and cropland, transitions are often very abrupt. Deforestation creates edge and exposes forest to the conditions found within the surrounding matrix. The outermost portions of a forest adjacent to the edge become part of the zone of transition or ecotone and may undergo changes in microclimate, composition of species, and vegetation structure (Hansen et al., 1992; Harris, 1988; Saunders et al., 1991). As a result, mammal species dependent upon conditions only found in the interior forest lose their habitat as the effects of edge expand into the forest interior (Merriam and Wegner, 1992). Small patches may no longer have interior forest conditions, and as a result may undergo dramatic changes in the natural composition of mammalian species that existed within what was once continuous forest (Yahner, 1988; Fonseca and Robinson, 1990). In areas that contain a great number of rare and endemic species, such as the Atlantic Forest along * Corresponding author. Tel.: 001 401 874 2912; fax: 001 401 874 4561; e-mail: [email protected]

Brazil's coastline, effects of fragmentation are of immediate concern (Stamps et al., 1987; Yahner, 1988; Bennett, 1990; Laurance and Yensen, 1991; Mares, 1992; Primack, 1993; Terborgh, 1992). The Atlantic Forest is one of the world's most biologically diverse systems, supporting c. 7% of the world's species (Quintela, 1990). It has been estimated that this forest supports at least 130 species of mammals of which 51 are endemic (Oliver and Santos, 1991). The Atlantic forest has undergone and currently is undergoing extensive, irreversible fragmentation as forest is converted to crops and pasture for cattle. Unfortunately, because only 2-5% of the original forest remains, and because the remnants are often small, isolated patches, the future of many of its species is tenuous (Terborgh, 1992). Our study examines the effects of edge on small mammal communities within two remnants of Brazilian Atlantic forest. We measured changes in the mean number of small mammal species and diversity in relation to distance from the forest/farmland edge, both in the forest and the surrounding matrix. Microclimatic changes and trends also were measured to examine differences between the forest and the matrix, and to help

0006-3207/98/$19.00 © 1998 Published by Elsevier Science Ltd. All rights reserved PII: S0006-3207(98)00003-2

S.M. Stevens, T.P. Husband/Biological Conservation 85 (1998) 1-8

determine how far into the forest these climatic elements were affected by edge.

2. Methods 2.1. Study sites

Sergipe, the smallest state in Brazil, is located along Brazil's Atlantic coastline. Few tracts of Atlantic forest still exist in Sergipe, and those are scattered widely throughout the state. Most of the remnants, including our two study sites, are located south of the city of Estancia (11°15'S, 37°25'W). One of the study sites (Study site 1), is c. 145 ha and was once continuous with what is now perhaps the largest remaining tract of forest in Sergipe, but has been separated for many years by public road and farmland. This last large remnant is c. 547 ha and was chosen as the second study site (Study site 2). Both forests are now surrounded by a mosaic of cattle pastures and coconut palm groves. Sergipe's Atlantic forest is drier than Atlantic forest farther south along the coast. Rainfall in Sergipe averages 1250-1400 mm/yr with a wet season occurring January through April (Universidade Federal de Sergipe, 1979). The average temperature is 24-25°C. The Sergipe forest has a continuous overstory, but the substory is patchy, which may be the result of firewood collection by local people who continue to rely on wood for cooking. Selective logging in the past has removed most of the very large old trees. The undergrowth is made up mostly of herbaceous plants, with very few shrubs. Epiphytes and lianas are common. Six transects, 300m long were placed 50m apart at both sites. The transects extended 200 m into the forest and 100 m into the surrounding agricultural land, which at site 1 was coconut palm groves with cattle pasture beneath, and at site 2, open cattle pasture. We initially placed the transects on aerial photographs to make sure that a > 300-m buffer of forest existed on the other three sides. This was to ensure that each trapping station would be placed at a known distance from the farmland/forest edge, and to lessen the possible influence from other edges. First we established six stations along each forest edge, 50 m apart. From each edge station, 10 more trap stations, 20 m apart, were extended into the forest and five stations, also 20 m apart, were placed extending out into the agricultural land (a total of 96 stations at each site). The edge was abrupt and distinct at each site. We used a combination of attributes from both the farmland and forest, 50% canopy cover of woody vegetation, and 75% herbaceous cover of grass monocultures from the surrounding pasture land, to make sure that the trap station on the edge would be placed in an area representative of both field and forest.

2.2. M a m m a l census

From August to December 1993, we censused small mammals (< 1.5kg) at both sites. Each trap station consisted of two Sherman live-traps, one placed on the ground and the second placed 0.5-3 m above the ground on fallen logs, blowdowns, vines or live branches (Malcolm, 1991). Every other trap station, including the edge station, had a Tomahawk live-trap placed either on or 0.1 m above the ground. All traps were baited with a mixture of crimped oats, cracked corn, raisins, and dry dog food. For four consecutive nights each month, three of the six transects were censused at each site. Censusing of all six transects was completed in two consecutive weeks before rotation between sites took place. Traps were checked each morning beginning at 0600 h. Each captured animal was ear tagged as well as injected subcutaneously with a passive integrated transponder (PIT) (Destron IDI, Boulder, CO). A portable reader (Model HS5600L, Destron IDI, Boulder, CO), which supplies an electromagnetic current was used to read the animal's number upon recapture. Because this method of tagging has not been used much on small mammals other than domestic cats (Fagerstone and Johns, 1987; Thomas et al., 1987; Barnard, 1989; Prentice et al., 1990; Rao and Edmondson, 1990; Schooley et al., 1993), and has never been tested in moist, tropical environments, we used ear tags along with the PIT tags as a backup. 2.3. Abiotic measurements

Abiotic measurements were taken each day at active trap stations. Air temperature (resolution I°C) and relative humidity (accuracy 2%, resolution 1%) were recorded using a hand held Protimeter digital hygrometer. Soil temperature was measured using a Taylor digital thermometer (accuracy ± 0.6°C) placed 2.5 cm into the ground surface. Rain gauges were set along the same transect at the edge, the 100-m station outside of the forest, and at the 120-m station inside the forest. 2.4. Habitat analysis

Vegetation measurements were taken around each trap station in order to describe its associated habitat (Table 1). We measured percentage canopy cover using a spherical crown densiometer and canopy height using a Haga altimeter. Other measurements were recorded on a qualitative sliding scale (August, 1983; Fonseca, 1988; Fonseca and Robinson, 1990). Both herbaceous and shrub cover were estimated in a 3.5-m-radius circle around each trap station and placed each in a percentage class. Vines were classified from counts within a 3.5-m-radius circle around each station.

S.M. Stevens, T.P. Husband/Biological Conservation 85 (1998) 1-8 Table 1 Vegetation variables measured at each trap station Vegetation variable

Description

Canopy cover (CC)

Canopy cover directly above trap station

Canopy height (CH)

Canopy height directly above trap station

Herbaceous cover (HC)

Percentage of herbaceous cover, 3.5-m radius around trap station: 0 = no cover, 1 = 1 < 5%, 2 = 5 < 20%, 3 = 2 0 < 50%, 4 = 5 0 < 7 5 % , 5 = 7 5 < 100%

Shrub cover (SC)

Shrub cover, 3.5-m radius around trap station: scoring same as H C above

Vine density (V)

N u m b e r of vines, 3.5-m radius around trap station: 0 = no vines, 1 = 1-5 vines, 2 = 6 - 1 0 vines, 3 = 11-20 vines, 4 = > 20 vines

ANOVA was used to test if distance from edge was equal for the five classes for the number of species, species diversity, soil temperature, air temperature, and relative humidity. Differences between all observed values were considered to be statistically significant at p < 0.05. The ANOVA model included a nested variable of repetition by site by distance by time to block out variability that may be attributed to differences between sites, transects, and month-to-month climatic differences. Fisher's Least Significant Difference (LSD) test was used to detect differences among distance classes. To find potential predictors of both mean number of species and diversity, all of the abiotic and vegetation variables, as well as distance from edge, were used in stepwise multiple regression analysis. Stepwise multiple regression analysis was also performed on the residuals of all the variables named above after the effects of distance from edge had been removed. All tests were conducted on SAS (SAS Institute Inc., 1993).

2.5. Data analysis 3. Results Because Tomahawk traps were located at every other station along each transect, we pooled the data collected for every two consecutive trap stations in the forest to form five distance classes. For analysis purposes, we considered the six transects at each site as repetitions and the four consecutive trap nights a month for each station as the smallest basic unit of measurement. The number of species and a species diversity index were calculated for the distance classes along each transect. The number of species (S) is the average number of species captured for each distance class. Species diversity was calculated using the Shannon index, H' (Shannon, 1948).

3.1. Edge effects on species diversity Over a period of 4 months, nine species (Emmons, 1990), representing three families of small mammals were captured (Table 2). Akodon sp. was only found at site 1. For both sites a sampling effort of 6144 total trap nights yielded 671 captures of 163 individuals, for a trapping success of about 11%. We did not capture any small mammals in the farmland at either site, in the 2304 trap nights recorded there. LSD comparisons of the mean number of species, S, and small mammal diversity, H', observed in the five

Table 2 Small m a m m a l capture data from two Atlantic forest remnants, Sergipe, Brazil, August-December, 1993 Site 1 Family (species)

Total captures

Total individs

Male

Site 2 Female

Sex unknown

Total captures

Total individs

Male

Female

Sex unknown

Didelphidae

Didelphis marsupialis Gracilinanus sp. Marmosops sp. Metachirus nudicaudatus Micoureus cinereus

31

3

1

l

1

25 63 10 113

5 16 3 23

1 10 2 13

4 6 1 10

0 0 0 0

16 6 14 7 145

5 3 5 3 17

4 1 4 2 12

1 2 1 1 5

0 0 0 0 0

44

24

12

6

6

94

25

14

8

3

49 23 28

10 8 10

7 6 6

3 2 4

0 0 0

0 1 2

0 1 2

0 1 2

0 0 0

0 0 0

386

102

285

61

Echimyidae

Proechymys trinomys Muridae

Akodon sp. Oxymycterus sp. Rhipidomys sp. Total

4

S.M. Stevens, T.P. Husband/Biological Conservation 85 (1998) 1-8

Table 3 Mean number of small mammal species (S) and diversity (H'), air temperature (°C), relative humidity (%), and soil temperature (°C) from two fragments of Atlantic forest, Sergipe, Brazil, August-December, 1993. Overall means + 1SD from combined sampling points at 20-m intervals from the forest edge to 180m (see text)a Distance class

Distance from edge (m)

n

Mean no. of species (S)

n

Species diversity (H')

n

Air Temp.

n

Rel. Humidity

n

Soil Temp.

1 2 3 4 5

0and20 40 and 60 80 and 100 120 and 140 160 and 180

48 48 48 48 48

0-8+0-7A 1-0±0.8 A 1,4±0.8 B 1,5~1.2B 1.8± 1-0 C

48 48 48 48 48

0.05±0.1A 0.09±0.2 AB 0.12±0.2 CB 0.16±0.2C 0.24:t:0.2 D

355 357 356 355 354

26.8±2.2A 26.7i2.1 B 25.8+ 1.8 C 25.7±1-7C 25.7:t: 1.8 C

333 330 322 326 322

48.4±18.1A 50.5± 17-2 B 52.7~16.5 CB 54.4±16.2C 55-2± 16.3 C

350 351 350 349 348

24-7±1.3A 24.2±1.0 B 24.3±0.9 B 24-2~0.9B 24.3±0.9 B

a Means followed by the same letter are not significantly different at p < 0.05 (Fisher's least significant difference test).

distance classes showed significant differences between some classes (Table 3). The results of ANOVA indicated that distance from edge was significant in explaining both the number of species and diversity ( F = 11.05, d.f.=4, p < 0.0001 and F = 11.13, d.f.=4, p < 0.0001, respectively).

3.2. Edge tolerance Although all species ranged widely within the forest, of the 671 total captures, only 43 occurred along the edge. Thirty-nine of these 43 captures were of two species, Proechymys trinomys and Micoureus cinereus (Fig. 1). Marmosops and Rhipidomys were only captured on the edge one and two times, respectively. Oxymycterus ranged widely but was only captured < 40 m from the edge twice. Metachirus, was never captured < 80/m from the edge, Gracilinanus, with two exceptions, was only captured >80m from the edge, and Didelphis and Akodon were found >40 m into the forest.

3.3. Distance effects on abiotic parameters Distance from the forest edge explained the significant variation in soil temperature ( F = 10.32, d.f.=4, p < 0.0001), air temperature ( F = 20-12, d.f.=4, p < 0.0001), and relative humidity ( F = 3.84,

d.f. = 4, p < 0.0052). Dramatic differences occurred for all three parameters between the farmland and the forest (Fig. 2). Air temperature was significantly higher at the edge and < 60m into the forest where it decreased and remained stable (Table 3). Soil temperature followed a similar pattern, but decreased and remained stable after 20 m from the edge, while relative humidity increased steadily from edge, stabilizing after 80 m (Fig. 2). The mean daily rainfall 100m from the forest edge into the farmland (12.6± 18.3mm) did not differ significantly from the mean throughfall at the edge (7.2 ± 10.6 mm), and 100 m into the forest (8.6± 13.8 mm).

3.4. Predictors of small mammal species diversity Distance contributed the most to the variability in both the number of species (S) and diversity (H') (Table 4). Canopy height was the only other variable entered in the regression model, but it only contributed significantly to the variability in S, not in H'. In a second analysis involving relative humidity, soil and air temperature, we found that distance was the only significant contributor to the variability in both S and H'. In the analysis of residuals, no variable was entered into the regression at the p < 0.05 level.

Table 4 Distance from edge into the forest, and vegetation and abiotic variables as significant predictors of the mean number of small mammals (S) and diversity (H'), using stepwise regression analysis Community parameter Vegetation variables included S H'

Abiotic variables included S H'

Significant predictors

Slope

r2(%)

F

p

Distance Canopy Ht. Distance Canopy Ht.

+ + + +

34.5

49.56 5-22 45.35 3.62

< 0.0001 0.02 < 0.0001 0.06

Distance Distance

+

12.5

34.15

< 0.0001

+

12.5

33.95

<0.0001

29.7

S.M. Stevens, T.P. Husband/Biological Conservation 85 (1998) 1-8

Proechymys trinomys

Micoureus cinereus

50

5O

40

40

Gracillnanus

5

sp. No.

Individuals

No.

Captllres

6

!

5

I 4 30

30

20

20

i0

i0

1

2

3

4

Distance

1

5

class

Marmosops

2

3

4

1 2 3 4 Distance class

5

D i s t a n c e class

Rhip1domys

sp.

sp.

Akodon

5

sp.

20

15

12

4 15 3

21 M

o

0 1

2 3 Distance

4 5 class

Oxymycterus

1

0 2

3

Distance

sp.

4

1

5

class

Metachirus nudlcaudatus

2

3

Distance

4

5

class

Dideiphis marsupialis

I0 15 8

i0 6,

4

o 1

2

3

Distance

4

class

5

1

2 3 Distance

4 5 class

1

2

3

Distance

4

r

class

Fig. 1. Small mammal captures in relation to distance from edge in two remnants of Atlantic forest, Sergipe, Brazil, August-December, 1993. Distance class 1 =0 and 20m from the edge, class 2=40 and 60m, class 3 =80 and 100m, class 4 = 120 and 140m, and class 5 = 160 and 180m from the forest/farmland edge.

6

S.M. Stevens, T.P. Husband/Biological Conservation 85 (1998) 1-8 60

~>~ J

55

.~

E r~

50

>

~

4s

40

35 i00 80

60

40

100 80

60

40

20 0 20 40 60 80 i00 120 140 160 180 200 Distance from edge (m]

28.5

X

.~

24. s

<

22.5 20

0

20

Distance

40

60

gO 1 0 0 120 140 1 6 0 1 8 0 2 0 0

from edge

(m)

30.0

o

27.5 p

I

[~ []

G~

ite 1 Site

2

25.0 .,.-t 0

22.5

i00 80

60

40

20

0

20

Distance

40

60

80 i00 120 140 160 180 200

from edge

(m)

Fig. 2. Relative humidity, air temperature and soil temperature in relation to distance from edge, in two fragments of Atlantic forest, Sergipe, Brazil. Measurements were taken each day at working trap stations, August-December, 1993. Ten trap stations 20m apart were placed inside the forest and five in the surrounding matrix, 0 m represents the edge station. Bars represent one standard error.

S.M. Stevens, T.P. Husband/Biological Conservation 85 (1998) 1-8

4. Discussion The conservation of mammalian communities in any habitat type subject to fragmentation, is dependent upon knowledge of both the biological and physical effects of fragmentation (Yahner, 1988; Bierregaard et al., 1992). Although we were able to show that small mammal diversity increased with distance from edge, we were unable to answer why this effect occurs. Our microclimatic results coincide closely with other studies on variation associated with edges. In the North American forests of Pennsylvania and northern Delaware, significant edge effects were found to extend < 50 m into the forest (Matlack, 1993). In the Brazilian Amazon, forest air temperature increased and humidity decreased with distance from edge _<40m, and depletion of soil moisture was found within <20m of the forest edge (Kapos, 1989). Our results indicate that for the two remnants of Atlantic forest, air temperature decreased and relative humidity increased <60m from the edge before stabilizing, which may therefore be considered the transition here for microclimatic conditions between the farmland and forest interior. We found it more difficult to determine a precise distance at which small mammal diversity and the mean number of species were affected by the influence of edge. Both continued to increase as far from the edge as 120-160m, but in addition to microclimatic conditions, other variables, such as changes in vegetation structure, evaporation, wind and light (Lovejoy et al., 1986), or increased predation (Andren and Angelstam, 1988) may have an effect. The absence of any small mammal records outside of the forest in the farmland suggests strict avoidance of the edge and farmland during this 4-month sampling period. However, this may not mean that there is never movement by small mammals across the edge into the farmland at other times during the year. In tropical Australian rain forest, mammals that exploited the forest edge and surrounding matrix were found to remain stable and even increase in forest fragments, but those that avoided the matrix declined or disappeared (Laurance, 1990, 1991a, b, 1994). Because extinctions within small forest patches may be common for some small mammals, the survival of their population is dependent upon recolonization. This is only possible if dispersing individuals are able to move about in the landscape (Fahrig and Merriam, 1994). In these two patches of Atlantic forest, dispersal of small mammals may be impeded by the effects of edge and surrounding agricultural land. Because our study documents the avoidance of farmland matrix by small mammals, and shows that mammalian diversity and abundance increases with distance from edge, a number of questions should be considered when targeting forest remnants for conservation. What

type of matrix surrounds the remnant, and is it hospitable to most dispersers? What is the distance from a remnant to other forest patches, and is dispersal and recolonization possible for small mammals? And finally, is there sufficient interior forest to support small mammal species dependent upon interior conditions?

Acknowledgements The authors thank the Federal Universidade de Sergipe for their hospitality in allowing us full use of their research station in Crasto, and a vehicle for the entire 5 months. We also thank Partners of America for funding the project, Susan Lewis for her assistance in the field, and Clovis Franco for his dedication. Most importantly we thank the landowners for allowing us full access to their properties. This paper is contribution no. 3150 of the Agricultural Experiment Station, University of Rhode Island, Kingston, RI 02881.

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