05_Zuniga_05_21.indd


UDC 599(83)
SEASONAL VARIATION IN A SMALL-MAMMAL ASSEMBLAGE 
IN A PRIORITY SITE FOR CONSERVATION IN SOUTH-CENTRAL 
CHILE

A. H. Zúñiga1,2*, A. Muñoz-Pedreros3, V. Quintana4

1Departamento de Ciencias Agronómicas y Recursos Naturales, 
Universidad de La Frontera, Temuco, Chile
2Laboratorio de Ecología, Universidad de Los Lagos, Osorno, Chile
3Departamento de Ciencias Ambientales, Universidad Católica de Temuco, 
Núcleo de Estudios Ambientales NEA, Temuco, Chile
4Centro de Estudios Agrarios y Ambientales, Valdivia, Chile
*Corresponding author 
E-mail: alfredo.zuniga@ufrontera.cl

Seasonal Variation in a Small-Mammal Assemblage in a Priority Site for Conservation in South-
Central Chile. Zúñiga, A. H., Andrés Muñoz-Pedreros, A., Quintana, V. — Diversity of rodents were 
compared in a priority site of conservation in southern-central Chile through two seasons (winter and 
spring). Th rough the use of Sherman traps, the richness and abundance of species present in both the 
priority site (native forest) and its adjacent habitat (commercial plantation of Eucalyptus globulus) was 
assessed. Th ere were signifi cant diff erences in terms of diversity between both habitats, the composition 
was signifi cant only for the case of the native forest; however, the seasonal eff ect was only signifi cant in 
this same habitat. Th e ecological aspects linked in this pattern are discussed, which involved both the 
particularities of the recorded species and microhabitat features in both habitats. 
K e y  w o r d s : Forest, seasonality, trophic guild, plantation, vegetation cover.

Introduction

Th e change in land use, and consequently the loss of habitat, is one of the main causes of the loss of bio-
logical diversity (Vitousek et al., 1997). In Chile, replacement of the original forest cover by agroecosystems, 
and especially by forest plantations with exotic species (e. g., Pinus radiata and Eucalyptus spp.), has generated a 
great fragmentation of these ecosystems (Echeverría et al., 2006, Echeverría et al., 2008), aff ecting biological di-
versity, partially documented in some native fauna taxa (for insects, Sáiz & Salazar, 1981, Fierro et al., 2017; for 
small mammals, Muñoz-Pedreros & Murúa, 1989; Kelt 2001; for birds,  Estades & Temple, 1999). In this way, 
fragmentation is the transformation of a continuous area of habitat (i. e., forests) in an anthropized landscape, 
which maintains “islands of original habitat” (Saunders et al., 1991; Bustamante et al., 2003), and in southern 
Chile, forestry expansion has been the main cause of the loss of native forests in recent decades (Echeverría et 
al., 2007; Aguayo et al., 2009; Lara et al., 2012).

To analyze the eff ect of land use change on the rodent assemblage, two aspects must be considered: (a) 
partitioning of resources, and (b) seasonal availability of food. Partitioning of resources implies the existence of 
mechanisms that prevent interspecifi c competition among sympatric species (Grant, 1972), for example the dif-
ferentiation in the use of food and space (Price, 1978). Space plays an important role in this coexistence, where 
the diversity of strata in forest ecosystems allows the diversifi cation of niches (August, 1983). For example, 

Zoodiversity, 55(5):395–404, 2021
DOI 10.15407/zoo2021.05.395



396 A. H. Zúñiga, A. Muñoz-Pedreros, V. Quintana

sympatry between cursorial, scansorial and arboreal species has been documented in the Northern Hemisphere 
by various authors (e. g., M’Closkey, 1978, Jones et al., 2001). Food supply would be modulated by seasonal 
environmental variations, which aff ect the availability of plants (Rathcke & Placey, 1985) and animals (Borror 
et al., 1989). Th erefore, a change in the niche relationships between species is expected, a situation that would 
be diff erent in native forests versus forest plantations.

For the assemblage of rodents in southern Chile, the replacement of the native forest by forest plantations 
and agroecosystems has resulted in a structural modifi cation of the habitat, with a compressed vegetation foli-
age profi le and a diversity of strata concentrated in the shrub (Muñoz-Pedreros & Murúa, 1989), also altering 
the food supply (Muñoz-Pedreros et al., 1990; Muñoz-Pedreros, 1992). However, the aforementioned studies 
compare degraded native vegetation (not forests) with plantations, therefore there are very few studies in Chile 
that compare the diversity of rodents between native forests and plantations, contrasting it with habitat vari-
ables such as the vegetation structure (Moreira-Arce et al., 2015).  Th e objective of this study is to determine 
seasonal variations (diversity and abundance) of the assemblage of rodents in native forest versus forest planta-
tion, relating them to the diversity of strata.

Material and methods

Th is study was carried out in two sites: (a) Predio Rucamanque (38o 39´ S, 72o 36´ W), a patch of native 
forest, located northwest of the city of Temuco, in south-central Chile (fi g. 1). It has a size of 438 ha, and it is 
located in the Huimpil-Ñielol mountain range. Its vegetation is characterized by being of the evergreen hu-
mid forest type, which includes associations of olivillo (Lapagerio-Aextoxiconetum punctatii) and roble-laurel-
lingue (Nothofago-Perseetum) (Ramírez et al., 1989), also fi nding various alien species. (b) A forestal plantation 
of Eucalyptus globulus, with seven years old and located contiguously and south of the Rucamanque forest.

During the months of June to December 2017 (winter and spring of the southern southern hemisphere), 
80 collapsible medium Sherman traps baited with crushed oats were installed in both study areas, which were 
checked every morning. In each site (forest and Eucalyptus plantations), two transects of 20 traps each sepa-
rated by 500 meters were arranged, which allowed the independence of records considering the home range 
of these target species (< 3.700 m2; Muñoz-Pedreros, 1992), and that they acted as replicas. Th e spatial ar-
rangement of the traps in the form of lines allows a high perimeter / area ratio, facilitating catches (Pearson & 
Ruggiero, 2003). 

Th e catch rate index was calculated (Calhoum, 1959), which considers the number of catches per species 
as a function of the sampling eff ort (number of traps/night). Th is index is an indicator of the abundance of 
the components of the small mammal assemblage. Th e structure of this assemblage, in each environment and 
season, was characterized by α (intra-environment) diversity, measured as species richness (S), and Shannon-
Wiener index (Shannon, 1948), which quantifi es the total diversity of a sample infl uenced by two basic com-
ponents, species richness and evenness. Th e formula for this function is H´= - Σ (pi × log2pi), where pi is the 
proportion of the total number of individuals in the sample corresponding to the species. Th e values fl uctuate 
between zero, when there was only one species, and the maximum (Hmax) corresponding to log2 S. Pielou 

Fig. 1. Study area.



397Seasonal variation in a small-mammal assemblage in a priority site for conservation in south-central Chile

index (J´) was calculated according to the equation J = H´/H. Th is index describes the evenness of a com-
munity, through the proportion of the diversity observed (H´) in relation to the maximum expected diversity 
(Hmax). Th is value fl uctuates between zero (minimum heterogeneity), and one (maximum heterogeneity, 
where species are equally abundant (Morin, 2011). To test the null hypothesis that the H´diversity in the two 
environments in the two seasons of the year are equal, the Hutcheson procedure was performed (Hutchen-
son, 1970) described in Zar (Zar, 1996), consisting of a t test calculating the weighted diversity index Hp = 
(NlogN)–(Σfi  log fi )/N), including the calculation of its variance for each environment according to SH´ 2 = 
[Σ fi  log2 fi –(Σfi  log fi )2/N]/N2. Th e distribution pattern of the species in each habitat and seasom was ob-
tained by comparing the capture frequencies through a goodness-of-fi t test (Ojeda, 1989; Sokal & Rohlf, 1995). 
To determine the existence of diff erences at the microhabitat level between the forest and the Eucalyptus plan-
tation, canopy cover, herbaceous vegetation, shrub vegetation, litter and dead wood were compared, selecting 
40 random points in the two habitats with a radius of 100 m2, and estimating them as a percentage (Quinn 
& Keough, 2002). Th ese values were compared with the frequency of rodent records obtained in winter and 
spring through correlation analysis (Quinn & Keough, 2002), in order to determine the variables of greatest 
association with the occurrence of these species.

Results

With a total sampling eff ort of 1600 traps / night, 62 specimens were captured (3.9 % 
of trapping success), with fi ve species: three of the Cricetidae family: long-tailed mouse 
Oligoryzomys longicaudatus (Bennett, 1832), long-haired mouse Abrothrix longipilis 
(Waterhouse, 1837), olive mouse Abrothrix olivaceus (Waterhouse, 1837), plus two exotic 
and invasive species of the family Muridae, black rat Rattus rattus (Linne, 1758), and brown 
rat Rattus norvegicus (Berkenhout, 1769). 

In winter, with a sampling eff ort of 800 traps / night, 37 specimens were recorded, the 
fi ve species (4.6 % of capture success), of which 31 specimens were captured in native forest 
and six in forest plantation (two species). In spring, with the same sampling eff ort, 25 speci-
mens were recorded (3.1 % of capture success), of fi ve species, of which 20 were captured 
in native forest and fi ve in forest plantations (table 1).

 Oligoryzomys longicaudatus was the only native rodent in commercial planta-
tions, where this species had a lower capture frequency in relation to the native forest. 
O. longicaudatus presented the highest representation of captures in relation to the rest 
of the native species in both seasons (fi g. 2). R. rattus presented the second highest repre-
sentation than in the rest of the species in winter in both habitats. In spring, this situation 
changed, being the frequency of captures of native species in the forest higher than the exot-
ic rodents (fi g. 2). Th e distribution pattern of the species presented a non-random character 
in the forest (χ2 = 21.74, p = 0.0002; χ2 = 12.50, p = 0.0140 for winter and forest, respectively; 
g.l.= 4 in both cases), while in the plantation the opposite pattern was obtained (χ2 = 1.50, 
p = 0.2207, g.l. = 1; χ2 = 0.40, p = 0.8187, g.l.=2 for winter and spring, respectively).

Regarding diversity, forest presented signifi cant diff erences in relation to the planta-
tion both in winter (T = 6.78; t0.05(2)9 = 1.83; p < 0.0001) and spring (T = 6.81; t0.05(2)214 = 1.76; 
p < 0.0001), situation that was also appreciated when comparing the forest in both seasons 
 (T = 2.66; t0.05(2)45 = 1.76; p = 0.0108). However, the plantation did not show diff erences be-
tween seasons (T = 0.09; t0.05(2)4 = 2.13; p = 0.9281).

When comparing the frequency of capture of species based on habitat, only O. longi-
caudatus presented a statistical signifi cance, while the rest of the species did not present 
the same pattern. Th is fact was observed both in winter (Mann-Whitney test, U = 78.50, 
p < 0.0001; U = 49.50, p = 0.145; U = 54 p = 0.066; U = 51, p = 0.290 for O. longicaudatus, 
A. olivaceus, A. longipilis, and R. rattus respectivamente; R. norvegicus only had a capture in 
the plantation), both in spring (U = 64.50, p = 0.015; U = 54, p = 0.065; U = 49.50, p = 0.145; 
U = 36, p = 0.539; U = 40, p = 1 for O. longicaudatus, A. olivaceus, A. longipilis, R. rattus and 
R. norvegicus, respectively). On the other hand, it was observed that no species exhibited 
signifi cant diff erences (in the sampling seasons, winter and spring) when comparing their 
frequency of records in both habitats independently.



398 A. H. Zúñiga, A. Muñoz-Pedreros, V. Quintana

Regarding the structure 
of the existing microhabitat 
both in forest and plantations, 
signifi cant diff erences were 
only observed in the canopy, 
herbaceous vegetation and 
litter. (Mann-Whitney test, 
p < 0,0001 in all cases; table 2). 
When these covers were as-
sociated with the frequency of 
rodent records, low correlation 
values were observed in gen-
eral terms (table 3), highlight-
ing the statistical signifi cance 
in winter of O. longicaudatus 
for canopy (p = 0.012), herb 
(p = 0.002), litter (p = 0.004) 
and dead wood (p  =  0.019), 
and A. olivaceus for canopy 
(p = 0.007). For spring, this dif-
ferentiation was only observed 
in A. longipilis for canopy  (p  = 
0.038), and A  olivaceus for 
shrub cover and litter (p = 0.038 
and p = 0.008, respectively).

Discussion
Th e pattern of diversity 

observed in the forest is lower 
than that reported in other 
sites in the region (Muñoz-
Pedreros et al., 1990; Kelt, 
2000). However, there is a 
contrast with Eucalyptus plan-
tation, where exotic species 
predominated. Th is fact sug-
gests a limitation on the part 
of Eucalyptus plantations to  
sustain the requirements of 

T a b l e  1 .  Number of catches per species, Diversity (H´), Maximum diversity (Hmax) and evenness (J), 
for the habitats examined in the study area in two seasons

Habitat Forest Plantation
Season Winter Spring Winter Spring

Oligoryzmoys longicaudatus
Abrothrix longipilis
Abrothrix olivaceus
Rattus rattus
Rattus norvegicus
Number of specimens
Richness of species
H´
Hmax
J´

16
5
3
6
1

31
5

1.86
2.32
0.80

10
4
3
2
1

20
5

1.92
2.32
0.91

1
0
0
5
0
6
2

0.65
1.00
0.65

2
0
0
2
1
5
3

1.52
1.58
0.96

Fig. 2. Rodent capture rate (plus standard deviations) in the study 
area in a) winter, and b) spring: O. long. — Oligoryzmoys longicau-
datus; A. long. — Abrothrix longipilis; A. oliv. — Abrothrix olivaceus; 
R.  rat  — Rattus rattus; R. nor. — Rattus norvegicus.



399Seasonal variation in a small-mammal assemblage in a priority site for conservation in south-central Chile

rodents, due to the low diversity of plant species that the plantations harbored (Wang et 
al., 2011), thus resulting in a limited food supply for rodents. Th is situation also applies 
to insects, where there is information about the decrease in their diversity in Eucalyp-
tus plantations (Fierro et al., 2017), which would reinforce the hypothesis of resource 
limitation in homogeneous environments for the case of these species. It is noteworthy 
the absence of in the study area the climbing mouse Irenomys tarsalis, and the marsu-
pial Dromiciops gliroides, which has been previously detected as prey by local carnivores 
(Zúñiga et al., 2005; Zúñiga et al., 2008). Th is fact would be explained by their spatial hab-
its, which are mainly arboreal (Kelt, 1993; Fontúrbel et al., 2010), limiting the chance of 
successful capture (Rau et al., 1995), because the Sherman traps, being located at ground 
level, would be limited in terms of the delectability of species in the other strata. How-
ever, considering that this cricetid has also been detected in other studies with this same 
technique (Zúñiga et al., 2021), it is necessary to consider its situation in the study area 
with caution, where its absence of records could be due to small population sizes.

Th e dominance of the assemblage in the forest by O. longicaudatus can be explained 
by its fl exibility to use diff erent microhabitats, mainly in the vertical layer of this habitat 
(Murúa, 1982), situation that is favored by the extensive tree cover present (Salas, 2001). 
Likewise, the herbivorous habits of this species are favored by the high richness of available 
plant species (Meserve et al., 1988; Ramírez et al., 1989; González et al. 1989), thus contrib-
uting to the selection of this habitat. On the other hand, the incursion into the plantations 
by this cricetid is due to sporadic forays in search of food (Murúa et al., 1986), those that 
would not obey some pattern of selectivity for resources. In contrast, the two recorded spe-
cies of Abrothrix (A. longipilis and A. olivaceus), had a lower frequency of recordings in the 
two seasons, which is explained by their preference for open environments (Glantz, 1984), 
which would be mainly associated with the clearings present in the forest. Th e trophic gen-
eralism of these species would allow them to diff erentiate from O. longicaudatus, which 
food habits is based mainly on arthropods (Meserve et al., 1988; Silva, 2005), a group that is 
available in the forest (Fierro et al., 2011). Its absence in the Eucalyptus plantation contrasts 
with what was previously observed in Pinus radiata plantations (Muñoz & Murúa, 1989), 
where they could take advantage of the plant resources available mainly through scrubs. In 
this sense, the opportunistic condition that Abrothrix olivaceus establishes when feeding 
on fungi linked to Pinus radiata plantations is remarkable (Bozinovic & Muñoz-Pedreros, 
1995). However, this situation has not been detected in the studied plantations. In this way, 

T a b l e  2 . Mean (% + standard deviation) of the covers of the vegetation strata in the habitats sampled in 
the study area

Variable Forest Plantation
Canopy

Herb
Shrub 
Litter

Dead wood

52.57 (17.25)
3.67 (9.49)

12.47 (5.08)
52.25 (10.73)

7.35 (2.65)

12 (3.80)
39.60 (8.89)
13.02 (2.99)
30.62 (8.38)
6.55 (2.35)

T a b l e  3 . Spearman correlations (ρ) obtained for the species in the area in the study, in relation to the 
vegetation cover  

Vegetation 
cover

O. long.* A. long.** A. oliv.*** R. rat.**** R. nor.*****
W S W S W S W S W S

Canopy
Herbs
Shrub
Litter
Dead wood

0.291
–0.359
0.032
0.327
0.272

0.083
–0.131
0.039
0.032

–0.041

0.177
–0.226
0.131
0.209
0.055

0.330
–0.116
–0.242
0.139
0.001

0.309
–0.117
–0.185
0.114

–0.205

0.204
–0,214
0.010
0.306
0.170

0,281
–0,188
–0,083
0,201

–0,026

–0.158
–0.044
0.102

–0.214
–0.106

0.033
–0.150
–0.022
0.168
0.097

–0.176
0.037

–0.004
–0.087
0.046

N o t e . Signifi cate correlations are highlighted in bold characters.
*O. long.— Oligoryzomys longicaudatus; **A. long. — Abrothrix longipilis; ***A. oliv. — Abrothrix olivaceus; 
****R. rat. — Rattus rattus; *****R. nor. — Rattus norvegicus. W — Winter; S — Spring. 



400 A. H. Zúñiga, A. Muñoz-Pedreros, V. Quintana

the homogeneous disposition of these resources in the case of Eucalyptus plantations means 
that their records may be of very low frequency, despite the vagility of rodents (Muñoz & 
Murúa, 1989).

Th e dominance in Eucalyptus plantations of Rattus rattus, one of the registered exotic 
species, would be explained by its ecological versatility, since it can be found in high popu-
lation sizes in diff erent habitats (King et al., 1996). Although this rodent can use environ-
ments with low tree cover, it could eventually make use of sites with wide vegetation cover, 
such as the forest, to minimize the risk of predation (King et al., 1996). Similarly, R. nor-
vegicus is found both in the forest and on plantations, although in a lower proportion than 
R. rattus. Th is fact supposes a lower suitability to use this habitat, which refers to its greater 
affi  nity with anthropized environments (Fernández & Simonetti, 2013). Notwithstanding 
the above, its proximity to watercourse sites suggests that this would be a key resource for 
its persistence in certain habitats, so its presence in the study area would be more restricted. 
In general terms, it has been observed that exotic species have a high potential for invasive-
ness of novel environments in Chile, where native species have little affi  nity given their 
coverage requirements (Simonetti, 1989), which in contrast, has allowed exotic species to 
dominate these habitats progressively (Jaksic et al., 2002). 

Although the species of the assemblage present relatively diff erent food habits (Meserve 
et al., 1988), there may be a degree of ecological fl exibility depending on the availability of 
the food, which suggests a greater trophic overlap in a context of scarcity. Th is scenario 
assumes that the diff erentiation in the use of the micro-habitats, where the morphological 
particularities of the species are essential for their coexistence (Vásquez, 1996). In this way, 
it is assumed that species such as O. longicaudatus partially use the tree canopy in their 
movements (Murúa et al., 1986), contrasting with the rest of the species observed, which 
are essentially cursorials. Despite this, the lack of correlation between their abundance and 
canopy cover could be explained by the low frequency of recordings in the Eucalyptus plan-
tations. By other hand, both species of Abrothrix tend to occupy sites with diff erent levels of 
vegetation cover, which would favor a low likelihood of interaction among them (Glantz, 
1984).

In general terms, the low association of vegetation cover with the frequency of spe-
cies records would be explained by the interaction of these variables, which would aff ect 
their space requirements. However, the statistical signifi cance resulting from the com-
parison of three of the fi ve covers, allows to establish the structural diff erence between 
both habitats. One aspect to consider in the selection of native forest by rodents is the 
use of vegetation cover as a visual obstacle against predators (Simonetti, 1989), situation 
that acquires relevance in the face of evidence of predation in the study area (Zúñiga et 
al., 2005). Th is fact shows a constant threat from local carnivores, as well as a selective 
pressure that urges rodents to use anti-predation behaviors, which would lead to the use 
of sites with high vegetation cover. A similar pattern has been observed in the northern 
hemisphere, where there is a positive relationship between the cover of shrub vegetation 
and the abundance of individuals (Carrilho et al., 2017), which suggests its suitability 
to support rodent populations. Despite the absence of statistical signifi cance observed 
around the shrub cover between both habitats, the higher standard deviation of this vari-
able in forest suggests a condition of greater heterogeneity in this habitat, where larger 
patches would be those that would provide greater protection against predators. Th is fact 
has been observed in Pinus radiata plantations in Argentine Patagonia, where the rich-
ness of shrub vegetation partially explained the abundance of local rodents (Lantschner 
et al., 2011).  

Th e importance of litter as a predictor of the occupation of rodents in the forest could 
be explained by its use as a facilitator in the formation of nesting sites (Clark & Kaufman, 
1991), where signifi cant diff erences observed between both habitats would allow part of the 
selectivity of the species for the forest. However, the signifi cant association of this variable 



401Seasonal variation in a small-mammal assemblage in a priority site for conservation in south-central Chile

with two of the recorded species (O. longicaudatus and A. olivaceus) reports on the link 
between this species and the forest microhabitat, as well as its spatial habits associated with 
the horizontal profi le of the ground (Glantz, 1984).

Th ere are reports of the importance of dead wood as a resource facilitator for rodents 
due to its association with epigean fauna, with which it is positively associated (Loeb, 1999, 
Ulyshen, 2016). Th is fact contrasts with the absence of statistical signifi cance observed for 
both habitats, which would be attributable to chemical properties of dead wood from Euca-
lyptus plantations, limiting the degradation processes of organic matter (Graça et al., 2002). 
Th is situation has been reported for Pinus radiata plantations (Husk et al., 2001), which 
would partially explain its eff ect on plantations in the study area. However, this would 
constitute a hypothesis that should be tested. Being O. longicaudatus the only rodent with a 
signifi cant association of this variable (in winter), its trophic fl exibility could be considered 
to explain part of this pattern (Meserve et al., 1988). Th us, the changes in the availability of 
resources promoted by seasonality (spring) would allow a change in their interaction with 
the habitat, aff ecting their use of space.

Th e diff erences observed in the capture frequency of rodents between seasons would be 
explained mainly by the particularities of their reproductive dynamics (González & Murúa, 
1983), which present diff erences throughout the year. Th e higher frequency of captures 
obtained in winter would be due to a surplus of individuals from the previous season (fall), 
with a remaining population of adults. Th is fact acquires consistency with the record in the 
traps of juvenile A. longilipis individuals in spring (Zúñiga, personal observation). How-
ever, seasonal diff erences in the abundance of records observed in O. longicaudatus could 
be explained by interannual patterns of great variation recorded for this rodent (Murúa et 
al., 1986), wihere the availability of resources has a strong eff ect. In this way, and given the 
restricted time horizon of fi eld sampling, it is necessary to carry out long-term monitoring 
to determine the scope of these fl uctuations in the study area.

As a conclusion, it was obtained that forest harbored more diversity than the Eucalyp-
tus plantation throughout the two sampled seasons. Diff erences observed were manifested 
both in the number of native species (being greater in the case of the forest), and the type of 
dominance (by an exotic species in the plantation, however in less abundance in relation to 
the forest). Th e evaluation of its variation in a broader time frame, as well as its relationship 
with the availability of resources for each species is pending.

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Received 17 November 2020
Accepted 1 September 2021