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Ecological Factors Influencing Small Rodents in a Tree Thinned Japanese Larch Larix kaempferi Plantation

PJZ_51_6_2153-2160

 

 

Ecological Factors Influencing Small Rodents in a Tree Thinned Japanese Larch Larix kaempferi Plantation

Jae-Kang Lee, Hyun-Su Hwang, Tae-Kyung Eom and Shin-Jae Rhim*

School of Bioresource and Bioscience, Chung-Ang University, Ansung 17546, South Korea

ABSTRACT

We used a capture-recapture method to investigate the ecological factor influencing small rodents in a tree thinned Japanese larch Larix kaempferi plantation in Mt. Maehwa, Hongcheon, South Korea. The mid-story, understory and ground vegetation coverage, the number of standing and downed trees ha-1 and the volume of downed trees ha-1 were significantly different between the pre- and post-thinning sessions. Mean density of Apodemus agrarius, A. peninsulae, and Myodes regulus were significantly different between sessions. Monthly captured adults and juveniles of A. agrarius and A. peninsulae were significantly higher in the post- than in the pre-thinning session. Population sizes were dramatically increased in the post-thinning session. Ground and understory vegetation coverage and number of downed trees ha-1 positively influenced the density. The overstory vegetation coverage negatively influenced the density. Tree thinning resulted in well-developed ground and understory vegetation and increasing downed trees might be an important method for forest management and biodiversity conservation.


Article Information

Received 14 August 2018

Revised 12 May 2019

Accepted 09 July 2019

Available online 16 August 2019

Authors’ Contribution

JKL and SJR designed the study and wrote the manuscript. HSH and TKE performed field work and analyzed the data.

Key words

Downed tree, Ground vegetation, Population size, Small rodents, Understory vegetation

DOI: http://dx.doi.org/10.17582/journal.pjz/2019.51.6.2153.2160

* Corresponding author: sjrhim@cau.ac.kr

0030-9923/2019/0006-2153 $ 9.00/0

Copyright 2019 Zoological Society of Pakistan



INTRODUCTION

Many forests are managed for human usage worldwide (Carry and Johnson, 1995). Management can ultimately affect the habitat resources of species in forest ecosystems (Moses and Boutin, 2001; Etcheverry et al., 2005; Rebbah et al., 2019). In many cases, habitats are damaged by removing the standing trees and understory vegetation according to forest practices (Franklin et al., 2002). There are a variety of silvicultural forest practices ranging from clear-cutting to single tree selection (Sullivan and Sullivan, 2001). The well-known responses of crop trees to thinning include an increase in the stem diameter, crown size, and volume of trees, and a decrease in the mortality of trees (Homyack et al., 2004). However, the effect of these tree thinning patterns on small rodents is not clear.

Small rodents represent a huge amount of the faunal biomass in forest ecosystems (Moreira-Arce et al., 2015). Moreover, they play important roles as consumers, prey and dispersers of fungi and plants. Rodents prey on the seeds of trees, and can limit natural generation (Levey et al., 2002; Lee, 2012). They have been considered indicator species in their habitat (Ausden, 2007), and might be influenced by the habitat elements contributing to habitat complexity, such as standing trees, snags, understory cover and downed trees (Fontúrbel, 2012; Moreira-Arce et al., 2015).

Small rodents comprise an essential component of managed coniferous forests (Zabel and Anthony, 2003; Sollmann et al., 2015). Moreover, forest management practices could be an influencing factor for mammals in coniferous plantations (Sullivan and Sullivan, 2001; Korea Forest Service, 2012). For example, the post-management changes that occur in habitat variables might affect the on-ground cover, used for nesting and shelter from predators (Homyack et al., 2004; Kang et al., 2013a).

Silviculture of plantations of Japanese larch Larix kaempferi has been performed on a national scale in South Korea since the 1960s. Tree thinning of overstocked Japanese larch plantation has been practiced increasingly to increase the growth rate of trees and reduce competition among them. However, changes in habitat characteristics with thinning of coniferous plantations are poorly understood. Moreover, forest managers have an interest in biological conservation as the basis for sustainable forest management (Homyack et al., 2004; Korea Forest Service, 2012).

There is a lack of information on the response of small rodents to tree thinning in the silvicultured Japanese larch plantations in South Korea. This information is essential for the conservation and management of biodiversity and habitat in these plantations. We hypothesized that habitat variables, such as vegetation coverage, standing trees, and downed trees, might be affected by tree thinning, and an increase in the densities and population of small rodents might be observed because they are influenced by these habitat changes. Here, we used the capture-recapture method to investigate small rodent populations close to habitat features that have been changed by tree thinning in a Japanese larch plantation.

 

MATERIALS AND METHODS

This study was carried out from May to November in 2014 and 2015 in a Japanese larch Larix kaempferi plantation (37°40′03″–37°40′17″ N, 127°52′07″–127° 52′13″ E) in Mt. Maehwa, Hongcheon, South Korea. The annual mean temperature was 10.8°C (range 35.7 to –19.6°C) and annual precipitation was 828 mm. The altitude of the study area ranged from 170 – 260 m above sea level. The dominant tree species was Japanese larch, which were planted in 1960. We selected four 90 × 90 m study plots, each of which were divided into a grid pattern, consisting of a 15 × 15 m array for trapping and habitat surveying. Each study plot was spatially separated from the other plots by a distance of 500 m, based on the estimated home range of small rodents (range 1743 to 14692 m2) in South Korea (Lee and Rhim 2016). There was no small rodent caught on neighboring plots in this study. We divided the study period into pre-thinning (May to November 2014) and post-thinning (May to November 2015) sessions. The trees were thinned in January 2015 in this area.

Habitat variables were measured at each trap station within circles of radius 5.64 m. In each circle, we recorded the species and number of standing trees and the number and volume of downed trees. Within the 5.64–m radius circles, we classified a vertical layer into ground (0–1 m), understory (1–2 m), mid-story (2–8 m), sub-overstory (8–20 m), and overstory (20–30 m) regions. Based on the percentage of cover in each vertical layer, the vegetation coverage was classified into the following four categories: 0 (percent coverage = 0%), 1 (1–33%), 2(34–66%) and 3 (67–100%) (Lee et al., 2012; Rhim et al., 2012).

We trapped small mammals in each study plot on three consecutive nights per month from May to November in 2014 and 2015. Each study plot (100 × 100 m) had 49 (7 × 7 array) trap stations at 15 m intervals. A Sherman live trap (7.62 × 8.89 × 22.86 cm, LFA trap) was installed at each station. The traps were baited with peanuts and checked each morning (Kang et al., 2013a). During the trapping sessions, we recorded the trap location, rodent species, if the individual was new or recaptured, individual identity, and age class. Rodent species were identified by morphometric and fur parameters. Age class was distinguished by tooth wear, sexual organs, pregnancy, and lactation. All captured small rodents were toe-clipped for individual identification and immediately released at the captured trap station (Lee et al., 2008; Kang et al., 2013b).

For habitat variable and small rodent population analysis, a Mann-Whitney U test (Zar, 2010) was carried out to compare the vegetation coverage (ground, understory, mid-story, sub-overstory and overstory), number of standing trees ha-1, number of downed trees ha-1, volume of downed trees ha-1, and monthly captured adult and juvenile small rodents between the pre- and post-thinning sessions. Density (number of individuals ha-1) estimates in each plot were obtained by analyzing the mark-recapture data for each small rodent species using POPAN analysis of the Jolly-Seber stochastic model (Seber, 1982; Lee et al., 2012). Means of the parameter estimates were computed across all models occupied by a given variable, along with the 95% confidence interval (Burnham and Anderson, 2002; Kang et al., 2013b). Population density estimations were conducted using the MARK 8.0 program. Estimated monthly mean densities of small rodent species were compared using the Kruskal-Wallis test.

We assessed which habitat variables might be sharing small rodent densities by using a generalized linear mixed model (GLMM; Zuur et al., 2009) to account for the spatially and temporally nested data (four densities estimated per site × two seasons). First, we ran a normality test (Zar, 2010) on all candidate independent variables. Then, we evaluated the multicollinearity of the parameters by calculating the Spearman correlation coefficient (r) and, for each highly correlated pair (correlation ≥ 0.7; Fowler et al., 1998). The parameters with r > 0.7 were excluded from further analysis. We performed a GLMM analysis (R packages: lme4; Density = habitat variable 1 + habitat variable 2 + · · · + [1|plot] + [1|year]) using the trap ID as a random factor, and all possible combinations of the independent variables (Bates et al., 2014). The trap ID was used as a random factor because all small rodent individuals can be independently captured in all traps. For every mode, MARK processed the Akaike information criterion (AIC) corrected for a small sample size (Burnham and Anderson, 2002; Kang et al., 2013a) that included habitat variables. AIC model weights (ω) were determined for each of the variables that were present in at least one selected model resulting from the GLMM. Values were considered statistically significant at P < 0.05.

 

RESULTS

Coverage of mid-story, understory, and ground vegetation were significantly different between the pre- and post-thinning sessions. Coverage of vegetation in the vertical foliage layers, except for the coverage of ground vegetation, was decreased by tree thinning. However, the coverage of ground vegetation was dramatically increased in the post-thinning session. The number of standing trees ha-1, number of downed trees ha-1 and volume of downed trees ha-1 were significantly different between the pre- and post-thinning sessions in the Japanese larch plantation. The number of standing trees ha-1 was decreased by tree thinning. However, the number and volume of downed trees ha-1 were higher in the post- than in pre-thinning session (Table I).

During this study, we captured 306 small rodents belonging to three species (438 captures in total): 218 Apodemus agrarius, 60 A. peninsulae, and 28 Myodes regulus individuals. Apodemus agrarius was the dominant species in the study area. During the pre-thinning session, only two small rodent species (A. agrarius and A. peninsulae) were captured in the study area. However, during the post-thinning session, study species (A. agrarius, A. peninsulae, and Myodes regulus) were captured.

The number of monthly captured adults of A. agrarius and A. peninsulae were significantly higher in the post-thinning than in the pre-thinning session. Moreover, the number of monthly captured juveniles of A. agrarius and A. peninsulae were significantly different between the pre- and post-thinning sessions (Table II).


 

Table I.- Differences in habitat variables between pre-thinning and post-thinning sessions in a Japanese larch Larix kaempferi plantation resulted with a Mann-Whitney U test. Values are means±SE.

Variable

Session

Z

p

Pre-thinning

Post-thinning

Coverage of overstory vegetation (20–30 m)

0.54±0.08

0.37±0.06

–1.37

0.170

Coverage of sub-overstory vegetation (8–20 m)

1.28±0.07

1.13±0.06

–1.02

0.308

Coverage of mid-story vegetation (2–8 m)

2.41±0.07

1.39±0.09

–7.53

<0.001

Coverage of understory vegetation (1–2 m)

1.45±0.08

0.99±0.05

–4.42

<0.001

Coverage of ground vegetation (0–1 m)

1.67±0.08

2.21±0.08

–4.47

<0.001

No. of standing trees ha-1

869.39±37.55

459.73±32.50

–7.24

<0.001

No. of downed trees ha-1

275.84±28.68

1339.33±87.83

–9.75

<0.001

Volume of downed trees ha-1 (m3)

12.33±1.97

18.22±1.86

–4.71

<0.001

 

Table II.- Differences in the number of monthly captured adults and juveniles of small rodents between the pre-thinning and post-thinning sessions in a Japanese larch Larix kaempferi plantation resulted with a Mann-Whitney U test. Values are means±SE, represented in ind ha-1.

Age

Species

Session

Z

P

Pre-thinning

Post-thinning

Adult

Apodemus agrarius

1.07±0.21

5.64±0.98

–3.72

0.001

Apodemus peninsulae

0.64±0.13

2.14±0.51

–2.15

0.039

Myodes regulus

-

0.71±0.30

2.41

0.114

Juvenile

Apodemus agrarius

0.21±0.07

4.14±0.22

–3.20

0.002

Apodemus peninsulae

-

0.64±0.15

–2.69

0.050

Myodes regulus

-

0.43±0.13

2.12

0.210

 

The estimated mean density of the three species studied were significantly different during the study period in the Japanese larch plantation (Kruskal-Wallis test, χ2 = 12.45, p = 0.002) (Fig. 1). The density of captured A. agrarius (Mann-Whitney U test, Z = –4.10, p < 0.001) and A. peninsulae (Z = –2.60, p = 0.011) individuals were significantly different, but higher in the post-thinning session. However, we found no significant difference in the density of M. regulus individuals between the pre- and post-thinning sessions. The overall density for study species significantly increased from 1.93 ind ha-1 in the pre-thinning session to 13.71 ind ha-1 in the post-thinning session (Mann-Whitney U test, Z = –4.17, p < 0.001).

The estimated densities of A. agrarius and A. peninsulae in the pre-thinning session were 9.00 and 4.00 ind ha-1 respectively. In the post-thinning session, the estimated densities of these species were over 3-6 times greater than those in the pre-thinning session. Moreover, the estimated density of M. regulus dramatically increased from 0 ind ha-1 in the pre-thinning session to 7.00 ind ha-1

 

Table III.- Estimation of the densities (no. ha-1) of small rodent species between the pre-thinning and post-thinning sessions in a Japanese larch Larix kaempferi plantation resulted with POPAN analysis of the Jolly-Seber stochastic model. Values are means±SE, represented in ind ha-1. 95% CI: 95% confidence interval.

Species

Session

Pre-thinning

Post-thinning

Size

95% CI

Size

95% CI

Apodemus agrarius

9.00±0.00

9.00–9.00

61.22±7.14

53.46–85.86

Apodemus peninsulae

4.00±0.00

4.00–4.00

13.12±1.90

11.47–20.51

Myodes regulus

-

-

7.00±0.00

7.00±0.00

Total

13.00±0.00

13.00–13.00

83.84±7.93

74.25–108.56

 

Table IV.- Models based on the correlated Akaike information criterion (AICc) built to explain the density of the small rodent species ranked by the AICc value resulting from the generalized linear mixed model.

Species

Models

AICc

AICc

ωi

Apodemus agrarius

[intercept + coverage of ground + coverage of understory + coverage of overstory + No. of trees ha-1]

442.40

0.00

0.14

[intercept + coverage of ground + coverage of understory + No. of trees ha-1]

442.46

0.06

0.14

[intercept + coverage of ground + coverage of understory + coverage of mid-story + No. of trees ha-1]

443.32

0.92

0.09

[intercept + coverage of ground + coverage of understory + coverage of mid-story + coverage of overstory + No. of trees ha-1]

443.52

1.11

0.08

[intercept + coverage of ground + coverage of understory + coverage of sub-overstory + coverage of overstory + No. of trees ha-1]

444.17

1.76

0.06

[intercept + coverage of ground + coverage of understory + coverage of overstory + No. of trees ha-1 + volume of downed trees]

444.30

1.90

0.05

[intercept + coverage of ground + coverage of understory + coverage of sub-overstory + No. of trees ha-1]

444.38

1.98

0.05

Apodemus peninsulae

[intercept + No. of trees ha-1]

252.03

0.00

0.07

[intercept + coverage of mid-story + No. of trees ha-1]

252.16

0.13

0.07

[intercept + coverage of mid-story]

252.48

0.45

0.06

[intercept + coverage of understory + coverage of mid-story + No. of trees ha-1]

253.93

1.90

0.03

[intercept + coverage of understory + No. of trees ha-1]

253.97

1.94

0.03

[intercept + coverage of sub-overstory + No. of trees ha-1]

253.99

1.96

0.03

 

Table V.- Variables including the best models explaining the variability in relative abundance of each model’s categories.

Species

Variables

Coefficient

SE

Z

P

95% CI

Apodemus

Intercept

0.2763

0.4730

0.58

0.559

-0.6507–1.2033

agrarius

Coverage of ground vegetation

0.3447

0.1074

3.21

0.001

0.1343–0.5552

Coverage of understory vegetation

-0.3050

0.1264

2.41

0.116

-0.5527–-0.0573

Coverage of mid-story vegetation

-0.1051

0.0987

1.06

0.287

-0.2986–0.0885

Coverage of sub-overstory vegetation

-0.0681

0.1259

0.54

0.588

-0.1786–0.3149

Coverage of overstory vegetation

-0.2095

0.1462

1.43

0.152

-0.4960–0.0770

No. of standing trees ha-1

-0.0015

0.0003

4.98

<0.001

-0.0021–-0.0009

Volume of downed trees ha-1

0.0022

0.0044

0.50

0.620

-0.0107–0.0064

Apodemus

Intercept

-0.8668

0.5757

1.51

0.132

-1.9951–0.2616

peninsulae

Coverage of understory vegetation

0.0953

0.1989

0.48

0.632

-0.2945–0.4851

Coverage of mid-story vegetation

-0.2807

0.1744

1.61

0.108

-0.6225–0.0610

Coverage of sub-overstory vegetation

-0.0832

0.2348

0.35

0.723

-0.5433–0.3770

No. of standing trees ha-1

-0.0009

0.0005

1.84

0.066

-0.0018–0.0001

 

in the post-thinning session. The total estimated densities of small rodents were larger in the post-thinning session (Table III).

The best model of density of small rodent species in a Japanese larch plantation had an Akaike weight (ω) of 0.03–0.14. Seven models fulfilled the criteria defined as best models (AICc < 2) for A. agrarius. Moreover, six models were defined for A. peninsulae (Table IV). The ground and understory vegetation coverage were highly positive correlated, and the number of standing trees ha-1 were highly negative correlated with the density of A. agrarius (Table V).

 

DISCUSSION

In this study, study species shared the same forest ecosystem. The three captured species are the most common and dominant small rodent species in the forests of South Korea. These species exhibit low forest-type specificity, have a broad diet, and are associated with abundant understory cover (Yoon, 1992; Lee et al., 2008). The densities of small rodents were different between the pre and post-thinning sessions, suggesting that individual species were influenced by tree thinning in the studied Japanese larch plantation.

Dramatic changes in the density of small rodents were observed in the post-thinning session in this study. In general, forest management changes the habitat structure by removing vegetation (Hunter, 1999). The conservation and management of biodiversity can be achieved by a combination of forest practices that provide a diverse forest age, class, structure, and function (Kang et al., 2013b; Hwang et al., 2014). Human-induced changes, such as thinning in silvicultured plantations, have direct influences on animal populations (Schmid-Holmes and Drickamer, 2001).

The changes in habitat variables and structure that result from tree thinning will likely positively affect some animal species (Homyack et al., 2004). Especially, small rodents are frequently positively related with more dense habitats, which are characterized by a high understory cover (Greenberg et al., 2006; Knapp et al., 2013). Higher canopy coverage might limit important resources for small rodents by reducing the understory structure and vegetation (Sollmann et al., 2015). Downed trees are also an important habitat factor, as they support food resources and provide cover from predators (Ecke et al., 2002; Vanderwel et al., 2010).

In this study, Apodemus agrarius was positively associated with ground vegetation and downed trees. Thinning resulted in a substantially denser coverage of ground vegetation in the post-thinning session than in the pre-thinning session. Moreover, the volume of downed trees was dramatically increased by tree thinning (Table 1). The denser ground vegetation and higher volume of downed trees provides a suitable microhabitat for food resources, such as lichen, fungi, and insects (Zabel and Anthony, 2003). However, the volume of downed trees was not a significant predictor of the best model in this study. Moreover, the number of standing trees ha-1 was negatively associated with the density of A. agrarius. This suggests that the decrease of number of standing trees ha-1 caused by thinning would be beneficial to the species.

An area with a high amount available resource could affect the survival and reproduction of animals (Lindström, 1999). Our study supported the prediction that animal reproduction is affected by tree thinning. Based on the number of juveniles, reproduction in the study species was significantly higher in the post- than in pre-thinning session. Given the response in small rodents to tree thinning, as well as the increase in ground vegetation and decrease of standing trees ha-1 in the studied Japanese larch plantation, it is possible that the small rodent populations in this landscape could benefit from tree thinning to increase their survival and reproduction.

The presence of relatively higher ground cover after tree thinning could explain the increased presence of these species, considering that ground cover is an ecologically important habitat variable for them (Amacher et al., 2008; Moreira-Arce et al., 2015); it provides a substrate for the maintenance of food and shelter (Sullivan and Sullivan, 2001). Moreover, there could be potential increase in the damage to plantations caused by the thinning increasing the small rodent density in post-thinning (Lee et al., 2017).

We conclude that small rodent populations will respond to changes in habitat caused by tree thinning. Japanese larch plantation managed with well-developed ground vegetation and a high volume of downed trees could sustain small rodents. An increase in the density of small rodents might be positively related to the density of predators. Therefore, if these habitat variables are enhanced in these man-made habitats, tree thinning might be regarded as an important forest management method for the conservation of biodiversity in Japanese larch plantations.

 

ACKNOWLEDGEMENTS

This study was supported by the Forest Science and Technology Project (Grant No: S121315L140100) of the Korea Forest Service, Republic of Korea. This research was supported by the Chung-Ang University Graduate Research Scholarship in 2017.

 

Conflict of interest statement

We declare that we have no conflict of interest.

 

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Pakistan Journal of Zoology

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Vol. 51, Iss. 6, Pages 1999-2399

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