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Journal of Biology, Agriculture and Healthcare www.iiste.org
ISSN 2224-3208 (Paper) ISSN 2225-093X (Online)
Vol.3, No.9, 2013
49
Seasonal variation of litter arthropods in some Eucalyptus
plantations at the Arboretum of Ruhande in Rwanda
Donat Nsabimana
National University of Rwanda, Department of Biology, Faculty of Science, B.P. 117 Butare, Rwanda.
E-mail of the corresponding author: dnsabimana@nur.ac.rw
Abstract
The main objective of this study was to assess the seasonal variation of litter arthropods in seven Eucalyptus
plantation types and native Entandrophragma excelsum stands at the Arboretum of Ruhande, Rwanda.
Arthropods were collected using the 1m2
square pick–up point technique, killed using 10% formalin solution,
and transported to the laboratory for identification to the class level. The results indicate that the collected
arthropod individuals belong to five classes. Seasonality exerted a strong effect on the abundance and diversity
of litter arthropods. In total, 2828 arthropod individuals were collected in September 2012, 3458 individuals in
January 2013 and 4005 individuals in April 2013. The Class of insects was the most abundant with relative
frequency of 54.8%, 77.3% and 76.6% in September 2012, January 2013, and April 2013 sampling periods. The
negative effect of Eucalyptus plantations on arthropods abundance was not exclusively confirmed by the results
as some stands of Eucalyptus species had arthropod abundance comparable to those under native
Entandrophragma excelsum stands. It is recommended to replicate this study under forest plantations located in
other ecological zones in Rwanda, which will generate general information for better conservation of arthropod
diversity in Rwanda. It is also recommended to continue arthropod classification at family, genus and species
levels.
Keywords: Litter arthropods; Arthropod abundance; Arthropod diversity.
1. Introduction
Phylum Arthropoda is the largest in the animal kingdom, including more than one million species classified in
more than nine classes (McGavin, 2002). Arthropods are highly represented in all habitats (Duelli et al., 1999)
and may thus be used as indicators of environmental changes caused by land use changes, disturbance and
pollution (Rocha et al., 2010).
Soil and litter arthropods are important decomposers of organic matter, recycling nutrients and releasing the
energy locked in plant tissues (Petersen and Luxton, 1982; Kremen et al., 1993; Bardgett et al., 2005a; Bardgett
et al., 2005b; Coleman and Rieske, 2006) which are vital processes for the sustainability of nature and
unmanaged ecosystem (Lavelle et al., 2006). The breakdown of organic matter by arthropods is essential for the
production of minute organic matter consumable by fungi and bacteria and thus, minerals and nutrients of dead
organisms become readily available in the soil for plant uptake (FAO, 2013).
Variability in climatic variables such as temperature, humidity, rainfall, litter amount and slope of the terrain and
elevation, and soil nutrients influence the abundance and diversity of the Arthropods (Samson et al., 1997;
Townsend et al., 2008). Arthropod diversity is also dependent on habitat heterogeneity expressed as differences
in litter pool and food (e.g., palatable leaf litter, fruits, seeds, and herbivore frass), toxins, (e.g., phenols and
tannins) and structural complexity that creates habitat (e.g. branches and leaf litter depth) (William et al., 2000;
Dominy et al., 2003; Kaspari et al., 2003).
In Rwanda, forest plantations cover 10% of national territory, of which Eucalyptus plantation covers 65%
(Nsabimana et al., 2008). Thought it is know that forest ecosystems conserve largest biodiversity, arthropod
diversity has never been studied in Rwanda, suggesting a need for studying litter arthropods under these
plantation species. In spite of the generalized use of Eucalyptus in forestry in many parts of the World, there is
little information on its impact on the invertebrate fauna (Florence, 1985; Da Silva et al., 2008). In addition, the
results of previous studies carried out throughout the World, were not conclusive about the influence Eucalyptus
plantations on the abundance of invertebrates (Chander and Goyal, 1995).
This study aimed to test the hypothesis that Eucalyptus plantations may negatively affect the arthropod
communities, although most studies reported a negative influence on invertebrates (Ratsirarson et al., 2002)
resulting from the fact that Eucalyptus leaves have oil glands (Penfold and Willis, 1961) and other secondary
compounds such as tannins, phenols and surface waxes which avoid consumption by leaf-eating arthropods
(Ohmart et al., 1987; Larsson and Ohmart, 1988; Edwards and Wanjura, 1990).
The objectives of this study were to study the seasonal variation of litter arthropods under seven Eucalyptus
plantation types and a native Entandrophragma excelsum stand, established at one climatic zone at the
Arboretum of Ruhande in Rwanda, and thus document on ecological influence of these stands on arthropod
diversity. Specifically: (1) to investigate seasonal variation of litter Arthropods under some Eucalyptus
Journal of Biology, Agriculture and Healthcare www.iiste.org
ISSN 2224-3208 (Paper) ISSN 2225-093X (Online)
Vol.3, No.9, 2013
50
plantations; (2) to compare the abundance and diversity of litter arthropods in Eucalyptus and Entendrophragma
excelsum stands and (3) verify the hypothesis that Eucalyptus plantations reduce or increase inhabiting arthropod
diversity.
2. Materials and Methods
2.1 Study area
The Arboretum of Ruhande is situated at latitude 2°36´S and long. 29°44´E, in Southern Rwanda, nearby the
National University of Rwanda with an altitude ranging between 1,638 and 1,737 m (Nsabimana et al., 2009).
The climate in the region is characterized by a long-term average annual rainfall of 1246.4 mm with a bimodal
rainfall pattern, two rainfall seasons alternating with two dry seasons. The short wet season extends from mid-
September to December, a short dry season from January to February, a long wet season from March to May,
and a long dry season from June to the mid-September. The relative humidity has the minimum of 59% during
dry seasons and the maximum of 86% in wet seasons (Nsabimana et al., 2009).
The arboretum of Ruhande has the total area of about 200ha (Stanga, 1991) split up into 504 numbered plots.
Each plot has 50 x 50m of size, with 207 native and exotic tree species of which 69 are Eucalyptus species
(Nsabimana et al., 2008). Many plantation species are replicated, which offer opportunity to study effects of
plantation species on different variables, including soil and biodiversity. The Arboretum of Ruhande houses a
diversity of vertebrates including small mammals, Monkeys (Chlorocebus aethiops, Blue monkeys), gazelles
(Gazella dama), birds, and bats which feed on a diversity of arthropods, including insects. Beside seeds
production and biodiversity conservation, the Arboretum of Ruhande is used for teaching and research purpose
by national teachers and students and those from foreign learning institutions (ISAR, 1987). The arboretum of
Ruhande was historically managed by catting herbaceous plants and shrubs and leaving them on the ground
(Nsabimana et al., 2009).
Seven Eucalyptus plantation types and one Entandrophragma excelsum stand were selected for the study. Each
plantation type was replicated three times, making 24 plots in total. Selected stand types and plot numbers at the
Arboretum of Ruhande are the following: Eucalyptus citriodora (plots 58, 211, 456), Eucalyptus grandis (plots
218, 220, 265), Eucalyptus maculata (plots 6, 446, 458), Eucalyptus maidenii (179, 377, 452), Eucalyptus
microcorys (plots 77, 367, 448), Eucalyptus saligna (plots 20, 375, 442), and Eucalyptus tereticornis (plots 109,
110, 540) and a stand which is native to Rwanda, Entandrophragma excelsum (plots 44, 54, 78). Three subplots
of 1m2
were selected randomly in each plot leaving 5m at the edge.
2.2 Arthropods data collection and identification and litter pH measurement
Litter arthropods were collected using the square pick-up point technique (Lamotte, 1969) during three seasons:
September 2012, January 2013 and April 2013. Aboveground litter was removed from the soil in a thin layer of
about 6cm depth (Jovon, 2011) and targeted arthropods were visually recognized and pulled out with sharp-
pointed forceps and fingers (Martin, 1977). Arthropods were collected into bottles containing a killing agent, 10%
formalin solution (Steyskal et al., 1986). The samples were then transported to the laboratory for further
identification using dichotomous keys in the literature (Scudder, 1993; Choate, 2003). Litter samples were also
collected on the date of arthropods sampling, and were oven- dried at 70°C for 48h. Thereafter they were milled
in a ball mill (Model: MM200, Retsch, Germany) for subsequent measurement of pH using litter powder water
suspension in the ratio 1:2.5, and the mixture was left to settle for one hour and then read pH using a glass
electrode.
2.3 Data analysis
Numbers of arthropod individuals per Class, were organized into excel sheets and analyzed using the
Biodiversity professional software (McAleece et al., 1997). Diversity indices such as Shannon and evenness
indices were calculated to determine the diversity of arthropods in different plantation types and to determine the
similarity of different plantation types respectively. Biodiversity Professional software calculates the Shannon-
weaver index H´ (Weaver and Shannon, 1949) using the following formula:
∑=
−=′
S
i
ii ppH
1
)ln(
N
n
p i
i =
Where: ni is the number of individuals in a species, i (the abundance of species i), S is the number of species, N
is the total number of individuals in a community (here N is the number of arthropods in each Class), pi is the
relative abundance of each species, calculated as the proportion of individuals of a given species i to the total
number of individuals in a community. A rich ecosystem with high species diversity has a large H´ value, while
an ecosystem with little diversity has a low H´ (Weaver and Shannon, 1949).
3. Results
In total, 2828 arthropod individuals were collected in September 2012 at the end of short dry season. The Class
Journal of Biology, Agriculture and Healthcare www.iiste.org
ISSN 2224-3208 (Paper) ISSN 2225-093X (Online)
Vol.3, No.9, 2013
51
of insects was the most abundant (54.8%) followed by the Class of Diplopoda (Table 1). Arthropod individuals
were the highest in the litter of Entandrophragma excelsum stand (24.6%) followed by Eucalyptus grandis and
Eucalyptus tereticornis stands (Table 1). The Class of insects was the most abundant in the litter of Arboretum
plantations, with 77.3% of all arthropods sampled in January 2013, and the Chilopoda were the least sampled.
The proportions of Arachnida, Crustacea and Diplopoda were almost comparable (Table 2). Arthropods
individuals were the highest in the litter of Eucalyptus saligna stand (19.5%) followed by Eucalyptus maidenii
stand (16.8%), while the arthropod individuals were the least abundant under Eucalyptus maculata stand (Table
2). A total of 4005 arthropod individuals were collected in April 2013, and the Class of insects was the most
dominant (76.6%), while Chilopoda were the least abundant among other arthropod classes (Table 3). The
arthropod individuals were the most dominant in the litter of Eucalyptus tereticornis stand followed by E.
saligna stand (Table 3).
In total, 10291 arthropod individuals were collected during 3 seasons, of which 27.5% were collected in shot dry
season (September 2012), 33.6% in shot wet season (January 2013), and 38.9% in long wet season (April 2013)
(Fig. 1). The Class of insects dominated other Classes in all seasons. The Diplopoda were more abundant in dry
season than in wet seasons (Fig. 1), and were not captured in Eucalyptus microcorys stand in all seasons. The
Arachnida abundance did not change significantly following the seasons (Fig. 1).
Table 1. Abundance of arthropod individuals as sampled in September 2012 in the litter of 8 plantation types in
the Arboretum of Ruhande and classified in their classes. Entandrophragma exc = Entandrophragma excelsum.
Plantation type Arachnida Chilopoda Crustacea Diplopoda Insecta Total
Individuals %
Entandrophragma exc. 61 15 13 349 259 697 24.65
Eucalyptus citriodora 22 6 4 37 131 200 7.07
Eucalyptus grandis 11 8 32 177 290 518 18.32
Eucalyptus maculata 19 3 8 19 104 153 5.41
Eucalyptus maidenii 54 0 40 16 206 316 11.17
Eucalyptus microcorys 24 4 24 0 101 153 5.41
Eucalyptus saligna 36 0 48 37 156 277 9.79
Eucalyptus tereticornis 73 1 57 80 303 514 18.18
Total individuals 300 37 226 715 1550 2828
Frequency (%) 10.6 1.3 8.0 25.3 54.8
Table 2. Abundance of arthropod individuals as sampled in January 2013 in the litter of 8 plantation types in the
Arboretum of Ruhande and classified in their classes. Entandrophragma exc = Entandrophragma excelsum.
Plantation type Arachnida Chilopoda Crustacea Diplopoda Insecta Total
Individuals %
Entandrophragma exc. 55 7 15 80 234 391 11.3
Eucalyptus citriodora 18 11 12 28 212 281 8.13
Eucalyptus grandis 23 0 20 47 383 473 13.7
Eucalyptus maculata 11 3 11 22 108 155 4.48
Eucalyptus maidenii 27 1 47 7 498 580 16.8
Eucalyptus microcorys 36 6 41 0 347 430 12.4
Eucalyptus saligna 22 5 29 38 581 675 19.5
Eucalyptus tereticornis 53 2 101 8 309 473 13.7
Total individuals 245 35 276 230 2672 3458
Frequency (%) 7.08 1.01 7.98 6.65 77.27
Journal of Biology, Agriculture and Healthcare
ISSN 2224-3208 (Paper) ISSN 2225-093X (Online)
Vol.3, No.9, 2013
Table 3. Abundance of arthropod individuals as sampled in April 2013 in the litter of 8 plantation types in the
Arboretum of Ruhande and classified in the
Plantation type Arachnida
Entandrophragma exc. 52
Eucalyptus citriodora 32
Eucalyptus grandis 37
Eucalyptus maculata 22
Eucalyptus maidenii 37
Eucalyptus microcorys 22
Eucalyptus saligna 34
Eucalyptus tereticornis 43
Total individuals 279
Frequency (%) 6.96
Figure 1. Seasonal variation of litter arthropods abundance in the Arboretum of Ruhande.
The Shannon diversity indices Hʹ of litter arthropods sampled in September 2012 (end of shot dry season) was
the highest in the stand of Eucalyptus saligna
(Table 4). The Shannon indices of th
excelsum stand followed by Eucalyptus maculata
sampled in April 2013 resulted in Shannon diversity indices that were highest in
stand followed by Eucalyptus maculata
seasons, it can be suggested that on the average,
comparison to that of Entendrophragma excelsum
sampled in September 2012 were higher than those in wet seasons (Table 4). The Shannon diversity indices
correlated with litter pH (R2
= 0.66; p < 0.05; Fig.
0
500
1000
1500
2000
2500
3000
3500
Arachnida
Arthropodindividuals
Journal of Biology, Agriculture and Healthcare
093X (Online)
52
Abundance of arthropod individuals as sampled in April 2013 in the litter of 8 plantation types in the
Arboretum of Ruhande and classified in their classes. Entandrophragma exc = Entandrophragma excelsum.
Arachnida Chilopoda Crustacea Diplopoda Insecta
6 4 76 82
11 12 27 202
10 34 101 403
11 23 58 262
2 35 13 351
15 12 198
4 50 21 671
7 110 16 899
66 280 312 3068
1.64 6.99 7.79 76.60
. Seasonal variation of litter arthropods abundance in the Arboretum of Ruhande.
The Shannon diversity indices Hʹ of litter arthropods sampled in September 2012 (end of shot dry season) was
Eucalyptus saligna followed by E. tereticornis and Entandrophragma excelsum
(Table 4). The Shannon indices of the arthropods sampled in January 2013 are highest in
Eucalyptus maculata stand (Table 4). Biodiversity analysis of litter arthropods
sampled in April 2013 resulted in Shannon diversity indices that were highest in Entandrophragma excelsum
Eucalyptus maculata stand (Table 4). Considering the Shannon diversity indices for all
seasons, it can be suggested that on the average, Eucalyptus plantations had less litter arthropod diversity in
Entendrophragma excelsum stand (Table 4). Shannon diversity indices of litter arthropods
sampled in September 2012 were higher than those in wet seasons (Table 4). The Shannon diversity indices
= 0.66; p < 0.05; Fig. 2).
Chilopoda Crustacea Diplopoda
Dry Season
Shot wet season
Long wet season
www.iiste.org
Abundance of arthropod individuals as sampled in April 2013 in the litter of 8 plantation types in the
Entandrophragma excelsum.
Insecta Total
Individuals %
220 5.49
284 7.09
585 14.6
376 9.38
438 10.93
247 6.16
780 19.47
1075 26.84
4005
76.60
. Seasonal variation of litter arthropods abundance in the Arboretum of Ruhande.
The Shannon diversity indices Hʹ of litter arthropods sampled in September 2012 (end of shot dry season) was
Entandrophragma excelsum stands
e arthropods sampled in January 2013 are highest in Entandrophragma
stand (Table 4). Biodiversity analysis of litter arthropods
Entandrophragma excelsum
stand (Table 4). Considering the Shannon diversity indices for all
had less litter arthropod diversity in
Shannon diversity indices of litter arthropods
sampled in September 2012 were higher than those in wet seasons (Table 4). The Shannon diversity indices
Insecta
Journal of Biology, Agriculture and Healthcare www.iiste.org
ISSN 2224-3208 (Paper) ISSN 2225-093X (Online)
Vol.3, No.9, 2013
53
Table 4. Shannon diversity indices for litter arthropods sampled in September 2012, January 2013 and April
2013.
September 2012 January 2013 April 2013
Plantation type Shannon
index
Eveness Shannon
index
Eveness Shannon
index
Eveness
Entandrophragma
excelsum
0.471 0.292 0.48 0.298 0.542 0.337
Eucaltypus citriodora 0.441 0.275 0.382 0.298 0.422 0.337
Eucalytpus grandis 0.439 0.273 0.296 0.214 0.421 0.337
Eucalyptus maculata 0.439 0.273 0.426 0.298 0.426 0.337
Eucalytpus maidenii 0.431 0.311 0.235 0.298 0.311 0.337
Eucalyptus microcorys 0.413 0.298 0.289 0.208 0.308 0.222
Eucalyptus saligna 0.504 0.364 0.249 0.298 0.246 0.337
Eucalyptus tereticornis 0.493 0.306 0.41 0.298 0.264 0.337
Figure 2. Positive relationship between litter pH and Shannon diversity indices for the arthropods sampled in
September 2012.
4. Discussion
This study is the first that has examined the likely impact of wet and dry seasons on leaf litter arthropods in a
number of Eucalyptus plantation types and Entendrophragma excelsum stands at the Arboretum of Ruhande,
Rwanda. Seasonality has affected the abundance and diversity of litter arthropods, with wet seasons having the
higher number of arthropods (Fig. 1). This may be explained by the fact that the litter biomass was greater in wet
seasons than in dry season (Pearson et al., 1986). It may also result from the development of understory
vegetation that could be eaten by the arthropods during wet seasons (Pereira et al., 2001). Seasonal variability is
also linked to temperature change, which determines the growth rate of arthropods (Wolda, 1988).
Seasonality of litter arthropods has been studied by many authors. For instance, most arthropod groups had high
number of individuals during wet seasons but declined during dry month in an Australian rain forest (Frith and
Frith, 1990). Similar finding was observed in Amazonian forest, Brasir (Silveira et al., 2009). Arthropod
abundance in wet season was of 2.3 times higher than that in dry season as observed in a tropical oceanic island
(Tanaka and Tanaka, 1982). The abundance of arthropods in wet seasons were very high comparable to those in
dry seasons in a lowland forest in Southern Peru (Pearson et al., 1986). It was noted that climatic seasons tend to
translate into seasonal activity patterns in living organisms including arthropods which became active only at
certain times of the year (Wolda, 1988).
y = 0.0798x + 0.0594
R² = 0.6584
0.3
0.35
0.4
0.45
0.5
0.55
4 4.5 5 5.5 6
Shannonindex
Litter pH
Journal of Biology, Agriculture and Healthcare www.iiste.org
ISSN 2224-3208 (Paper) ISSN 2225-093X (Online)
Vol.3, No.9, 2013
54
In this study, the abundance of litter arthropods increased from 27.5% in September 2012, to 33.6% in January
2013 (shot wet season) and 38.9% in April 2013 (long wet season) (Fig. 1). These figures indicate that the litter
invertebrates increase with the precipitation, but heavy rainfall tends to decrease litter amount and soil
invertebrate densities (Chiba et al., 1975). Shannon indices of arthropods sampled in September 2012 were
higher than those in other seasons (Table 4), indicating that the heavy rain tends to decrease arthropods diversity
as it was also noted by Chiba et al. (1975).
The Eucalyptus plantations have been more blamed worldwide to affect negatively litter arthropods (Zahn et al.,
2009) suggesting that some Eucalyptus species do not allow development of understory vegetation which may be
feed by arthropods (Pereira et al., 2001). The Eucalyptus species are also blamed for having poor organic carbon
(Signihal et al., 1975; Balagopalan and Jose, 1995; Animon et al., 1999). It has also been suggested that some
Eucalyptus species are efficient competitors for water from soil (Poore and Fries, 1985). Having oil glands in
their leaves (Penfold and Wills, 1961) and tough leathery leaves (Edward and Wanjura, 1990) have been also
included among reasons to blame Eucalyptus plantations to limit development of litter arthropods.
However, the results of this study show that the stands of E. tereticornis, E. saligna, and E. grandis have a
greater abundance of arthropods than the litter of Entendrophragma excelsum stand that has been used for
comparison (Tables 1–3). These Eucalyptus stands allow the growth of herbs and shrubs of various types, which
serve as food to inhabiting arthropods (Pereira et al., 2001). It was noted that high vegetation diversity supports
in turn a high invertebrate diversity (Teodorescu and Cogalniceanu, 2002) and the poor undergrowth of
herbaceous plants result in reduced arthropods abundance (Mallick and Pati, 1996).
The Class of insects has remained most dominant among arthropods collected in all seasons (Tables 1–3; Fig. 1),
this may be explained by the fact that the Class of insects has Hymenoptera order which is worldwide abundant
(Chavhan et al., 2011), including Formicidae (ants) which prefer wet litter habitat conditions and deep litter
depth (Sabu, 2005) and increasing with the increase of their specific food resources such as larva and other
arthropods (Samson et al., 1997; Shattock and Barnet, 2001). Insects are also able to adapt to the extreme
environmental conditions such as rain, high humidity and low litter temperature (Stork, 1988; Basu, 1997).
The Centipedes remained the fewest in all seasons that we sampled (Fig. 1) and under all plantation types. This
may be because they do not eat litter; they are primarily carnivorous, eating marine insects (Chamberlin, 1920).
On the other hand, Millipedes were higher in dry season (Fig. 1) and it was contrary to previous finding that they
usually have their highest activity in spring and autumn (Voigtländer, 1996; Tajovsky, 2000). This high number
may support the note by Berg and Hemerik (2004) that some millipedes do not have ecological preference.
On the average, the arthropods diversity (Shannon index) in Eucalyptus stands was lower than that in
Entendrophragma excelsum stands (Table 4). This may result from multiple reasons: Eucalyptus stands have less
understory vegetation types (Pereira et al., 2001); they are poor in organic carbon (Animon et al., 1999); their
effectiveness in competition for water (Poore and Fries, 1985); having leaves that leachate directly on certain
species of arthropods (Canhoto and Laranjeira, 2007; Zahn et al., 2009) and their influence on soil and litter pH
which has shown correlation with diversity indices (Fig. 2). All these conditions can unfavour the establishment
of certain species of arthropods in Eucalyptus stands.
5. Conclusions
The present results provide an overview on the seasonal variation of litter arthropods in some Eucalyptus
plantations at the Arboretum of Ruhande. The study confirms that the seasonality has an effect on the abundance
and diversity of arthropods, with highest figures in wet seasons. The negative effect of Eucalyptus plantations on
arthropods abundance was not exclusively confirmed as some stands of Eucalyptus species had arthropod
abundance comparable to those under native Entandrophragma excelsum stands. The Class of insects was the
most abundant in all seasons with relative frequency of 54.8%, 77.3% and 76.6% in September 2012, January
2013, and April 2013 sampling periods respectively. This study need to be repeated under forest plantations
located in different ecological zones in Rwanda.
Acknowledgements
The author is grateful to the authority of the Arboretum of Ruhande that authorized to conduct this study under
their forest plantations and to BSc students Sebera F., J.D. Dusabimana, and C.S. Iradukunda who have assisted
in field data collection.
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  • 1. Journal of Biology, Agriculture and Healthcare www.iiste.org ISSN 2224-3208 (Paper) ISSN 2225-093X (Online) Vol.3, No.9, 2013 49 Seasonal variation of litter arthropods in some Eucalyptus plantations at the Arboretum of Ruhande in Rwanda Donat Nsabimana National University of Rwanda, Department of Biology, Faculty of Science, B.P. 117 Butare, Rwanda. E-mail of the corresponding author: dnsabimana@nur.ac.rw Abstract The main objective of this study was to assess the seasonal variation of litter arthropods in seven Eucalyptus plantation types and native Entandrophragma excelsum stands at the Arboretum of Ruhande, Rwanda. Arthropods were collected using the 1m2 square pick–up point technique, killed using 10% formalin solution, and transported to the laboratory for identification to the class level. The results indicate that the collected arthropod individuals belong to five classes. Seasonality exerted a strong effect on the abundance and diversity of litter arthropods. In total, 2828 arthropod individuals were collected in September 2012, 3458 individuals in January 2013 and 4005 individuals in April 2013. The Class of insects was the most abundant with relative frequency of 54.8%, 77.3% and 76.6% in September 2012, January 2013, and April 2013 sampling periods. The negative effect of Eucalyptus plantations on arthropods abundance was not exclusively confirmed by the results as some stands of Eucalyptus species had arthropod abundance comparable to those under native Entandrophragma excelsum stands. It is recommended to replicate this study under forest plantations located in other ecological zones in Rwanda, which will generate general information for better conservation of arthropod diversity in Rwanda. It is also recommended to continue arthropod classification at family, genus and species levels. Keywords: Litter arthropods; Arthropod abundance; Arthropod diversity. 1. Introduction Phylum Arthropoda is the largest in the animal kingdom, including more than one million species classified in more than nine classes (McGavin, 2002). Arthropods are highly represented in all habitats (Duelli et al., 1999) and may thus be used as indicators of environmental changes caused by land use changes, disturbance and pollution (Rocha et al., 2010). Soil and litter arthropods are important decomposers of organic matter, recycling nutrients and releasing the energy locked in plant tissues (Petersen and Luxton, 1982; Kremen et al., 1993; Bardgett et al., 2005a; Bardgett et al., 2005b; Coleman and Rieske, 2006) which are vital processes for the sustainability of nature and unmanaged ecosystem (Lavelle et al., 2006). The breakdown of organic matter by arthropods is essential for the production of minute organic matter consumable by fungi and bacteria and thus, minerals and nutrients of dead organisms become readily available in the soil for plant uptake (FAO, 2013). Variability in climatic variables such as temperature, humidity, rainfall, litter amount and slope of the terrain and elevation, and soil nutrients influence the abundance and diversity of the Arthropods (Samson et al., 1997; Townsend et al., 2008). Arthropod diversity is also dependent on habitat heterogeneity expressed as differences in litter pool and food (e.g., palatable leaf litter, fruits, seeds, and herbivore frass), toxins, (e.g., phenols and tannins) and structural complexity that creates habitat (e.g. branches and leaf litter depth) (William et al., 2000; Dominy et al., 2003; Kaspari et al., 2003). In Rwanda, forest plantations cover 10% of national territory, of which Eucalyptus plantation covers 65% (Nsabimana et al., 2008). Thought it is know that forest ecosystems conserve largest biodiversity, arthropod diversity has never been studied in Rwanda, suggesting a need for studying litter arthropods under these plantation species. In spite of the generalized use of Eucalyptus in forestry in many parts of the World, there is little information on its impact on the invertebrate fauna (Florence, 1985; Da Silva et al., 2008). In addition, the results of previous studies carried out throughout the World, were not conclusive about the influence Eucalyptus plantations on the abundance of invertebrates (Chander and Goyal, 1995). This study aimed to test the hypothesis that Eucalyptus plantations may negatively affect the arthropod communities, although most studies reported a negative influence on invertebrates (Ratsirarson et al., 2002) resulting from the fact that Eucalyptus leaves have oil glands (Penfold and Willis, 1961) and other secondary compounds such as tannins, phenols and surface waxes which avoid consumption by leaf-eating arthropods (Ohmart et al., 1987; Larsson and Ohmart, 1988; Edwards and Wanjura, 1990). The objectives of this study were to study the seasonal variation of litter arthropods under seven Eucalyptus plantation types and a native Entandrophragma excelsum stand, established at one climatic zone at the Arboretum of Ruhande in Rwanda, and thus document on ecological influence of these stands on arthropod diversity. Specifically: (1) to investigate seasonal variation of litter Arthropods under some Eucalyptus
  • 2. Journal of Biology, Agriculture and Healthcare www.iiste.org ISSN 2224-3208 (Paper) ISSN 2225-093X (Online) Vol.3, No.9, 2013 50 plantations; (2) to compare the abundance and diversity of litter arthropods in Eucalyptus and Entendrophragma excelsum stands and (3) verify the hypothesis that Eucalyptus plantations reduce or increase inhabiting arthropod diversity. 2. Materials and Methods 2.1 Study area The Arboretum of Ruhande is situated at latitude 2°36´S and long. 29°44´E, in Southern Rwanda, nearby the National University of Rwanda with an altitude ranging between 1,638 and 1,737 m (Nsabimana et al., 2009). The climate in the region is characterized by a long-term average annual rainfall of 1246.4 mm with a bimodal rainfall pattern, two rainfall seasons alternating with two dry seasons. The short wet season extends from mid- September to December, a short dry season from January to February, a long wet season from March to May, and a long dry season from June to the mid-September. The relative humidity has the minimum of 59% during dry seasons and the maximum of 86% in wet seasons (Nsabimana et al., 2009). The arboretum of Ruhande has the total area of about 200ha (Stanga, 1991) split up into 504 numbered plots. Each plot has 50 x 50m of size, with 207 native and exotic tree species of which 69 are Eucalyptus species (Nsabimana et al., 2008). Many plantation species are replicated, which offer opportunity to study effects of plantation species on different variables, including soil and biodiversity. The Arboretum of Ruhande houses a diversity of vertebrates including small mammals, Monkeys (Chlorocebus aethiops, Blue monkeys), gazelles (Gazella dama), birds, and bats which feed on a diversity of arthropods, including insects. Beside seeds production and biodiversity conservation, the Arboretum of Ruhande is used for teaching and research purpose by national teachers and students and those from foreign learning institutions (ISAR, 1987). The arboretum of Ruhande was historically managed by catting herbaceous plants and shrubs and leaving them on the ground (Nsabimana et al., 2009). Seven Eucalyptus plantation types and one Entandrophragma excelsum stand were selected for the study. Each plantation type was replicated three times, making 24 plots in total. Selected stand types and plot numbers at the Arboretum of Ruhande are the following: Eucalyptus citriodora (plots 58, 211, 456), Eucalyptus grandis (plots 218, 220, 265), Eucalyptus maculata (plots 6, 446, 458), Eucalyptus maidenii (179, 377, 452), Eucalyptus microcorys (plots 77, 367, 448), Eucalyptus saligna (plots 20, 375, 442), and Eucalyptus tereticornis (plots 109, 110, 540) and a stand which is native to Rwanda, Entandrophragma excelsum (plots 44, 54, 78). Three subplots of 1m2 were selected randomly in each plot leaving 5m at the edge. 2.2 Arthropods data collection and identification and litter pH measurement Litter arthropods were collected using the square pick-up point technique (Lamotte, 1969) during three seasons: September 2012, January 2013 and April 2013. Aboveground litter was removed from the soil in a thin layer of about 6cm depth (Jovon, 2011) and targeted arthropods were visually recognized and pulled out with sharp- pointed forceps and fingers (Martin, 1977). Arthropods were collected into bottles containing a killing agent, 10% formalin solution (Steyskal et al., 1986). The samples were then transported to the laboratory for further identification using dichotomous keys in the literature (Scudder, 1993; Choate, 2003). Litter samples were also collected on the date of arthropods sampling, and were oven- dried at 70°C for 48h. Thereafter they were milled in a ball mill (Model: MM200, Retsch, Germany) for subsequent measurement of pH using litter powder water suspension in the ratio 1:2.5, and the mixture was left to settle for one hour and then read pH using a glass electrode. 2.3 Data analysis Numbers of arthropod individuals per Class, were organized into excel sheets and analyzed using the Biodiversity professional software (McAleece et al., 1997). Diversity indices such as Shannon and evenness indices were calculated to determine the diversity of arthropods in different plantation types and to determine the similarity of different plantation types respectively. Biodiversity Professional software calculates the Shannon- weaver index H´ (Weaver and Shannon, 1949) using the following formula: ∑= −=′ S i ii ppH 1 )ln( N n p i i = Where: ni is the number of individuals in a species, i (the abundance of species i), S is the number of species, N is the total number of individuals in a community (here N is the number of arthropods in each Class), pi is the relative abundance of each species, calculated as the proportion of individuals of a given species i to the total number of individuals in a community. A rich ecosystem with high species diversity has a large H´ value, while an ecosystem with little diversity has a low H´ (Weaver and Shannon, 1949). 3. Results In total, 2828 arthropod individuals were collected in September 2012 at the end of short dry season. The Class
  • 3. Journal of Biology, Agriculture and Healthcare www.iiste.org ISSN 2224-3208 (Paper) ISSN 2225-093X (Online) Vol.3, No.9, 2013 51 of insects was the most abundant (54.8%) followed by the Class of Diplopoda (Table 1). Arthropod individuals were the highest in the litter of Entandrophragma excelsum stand (24.6%) followed by Eucalyptus grandis and Eucalyptus tereticornis stands (Table 1). The Class of insects was the most abundant in the litter of Arboretum plantations, with 77.3% of all arthropods sampled in January 2013, and the Chilopoda were the least sampled. The proportions of Arachnida, Crustacea and Diplopoda were almost comparable (Table 2). Arthropods individuals were the highest in the litter of Eucalyptus saligna stand (19.5%) followed by Eucalyptus maidenii stand (16.8%), while the arthropod individuals were the least abundant under Eucalyptus maculata stand (Table 2). A total of 4005 arthropod individuals were collected in April 2013, and the Class of insects was the most dominant (76.6%), while Chilopoda were the least abundant among other arthropod classes (Table 3). The arthropod individuals were the most dominant in the litter of Eucalyptus tereticornis stand followed by E. saligna stand (Table 3). In total, 10291 arthropod individuals were collected during 3 seasons, of which 27.5% were collected in shot dry season (September 2012), 33.6% in shot wet season (January 2013), and 38.9% in long wet season (April 2013) (Fig. 1). The Class of insects dominated other Classes in all seasons. The Diplopoda were more abundant in dry season than in wet seasons (Fig. 1), and were not captured in Eucalyptus microcorys stand in all seasons. The Arachnida abundance did not change significantly following the seasons (Fig. 1). Table 1. Abundance of arthropod individuals as sampled in September 2012 in the litter of 8 plantation types in the Arboretum of Ruhande and classified in their classes. Entandrophragma exc = Entandrophragma excelsum. Plantation type Arachnida Chilopoda Crustacea Diplopoda Insecta Total Individuals % Entandrophragma exc. 61 15 13 349 259 697 24.65 Eucalyptus citriodora 22 6 4 37 131 200 7.07 Eucalyptus grandis 11 8 32 177 290 518 18.32 Eucalyptus maculata 19 3 8 19 104 153 5.41 Eucalyptus maidenii 54 0 40 16 206 316 11.17 Eucalyptus microcorys 24 4 24 0 101 153 5.41 Eucalyptus saligna 36 0 48 37 156 277 9.79 Eucalyptus tereticornis 73 1 57 80 303 514 18.18 Total individuals 300 37 226 715 1550 2828 Frequency (%) 10.6 1.3 8.0 25.3 54.8 Table 2. Abundance of arthropod individuals as sampled in January 2013 in the litter of 8 plantation types in the Arboretum of Ruhande and classified in their classes. Entandrophragma exc = Entandrophragma excelsum. Plantation type Arachnida Chilopoda Crustacea Diplopoda Insecta Total Individuals % Entandrophragma exc. 55 7 15 80 234 391 11.3 Eucalyptus citriodora 18 11 12 28 212 281 8.13 Eucalyptus grandis 23 0 20 47 383 473 13.7 Eucalyptus maculata 11 3 11 22 108 155 4.48 Eucalyptus maidenii 27 1 47 7 498 580 16.8 Eucalyptus microcorys 36 6 41 0 347 430 12.4 Eucalyptus saligna 22 5 29 38 581 675 19.5 Eucalyptus tereticornis 53 2 101 8 309 473 13.7 Total individuals 245 35 276 230 2672 3458 Frequency (%) 7.08 1.01 7.98 6.65 77.27
  • 4. Journal of Biology, Agriculture and Healthcare ISSN 2224-3208 (Paper) ISSN 2225-093X (Online) Vol.3, No.9, 2013 Table 3. Abundance of arthropod individuals as sampled in April 2013 in the litter of 8 plantation types in the Arboretum of Ruhande and classified in the Plantation type Arachnida Entandrophragma exc. 52 Eucalyptus citriodora 32 Eucalyptus grandis 37 Eucalyptus maculata 22 Eucalyptus maidenii 37 Eucalyptus microcorys 22 Eucalyptus saligna 34 Eucalyptus tereticornis 43 Total individuals 279 Frequency (%) 6.96 Figure 1. Seasonal variation of litter arthropods abundance in the Arboretum of Ruhande. The Shannon diversity indices Hʹ of litter arthropods sampled in September 2012 (end of shot dry season) was the highest in the stand of Eucalyptus saligna (Table 4). The Shannon indices of th excelsum stand followed by Eucalyptus maculata sampled in April 2013 resulted in Shannon diversity indices that were highest in stand followed by Eucalyptus maculata seasons, it can be suggested that on the average, comparison to that of Entendrophragma excelsum sampled in September 2012 were higher than those in wet seasons (Table 4). The Shannon diversity indices correlated with litter pH (R2 = 0.66; p < 0.05; Fig. 0 500 1000 1500 2000 2500 3000 3500 Arachnida Arthropodindividuals Journal of Biology, Agriculture and Healthcare 093X (Online) 52 Abundance of arthropod individuals as sampled in April 2013 in the litter of 8 plantation types in the Arboretum of Ruhande and classified in their classes. Entandrophragma exc = Entandrophragma excelsum. Arachnida Chilopoda Crustacea Diplopoda Insecta 6 4 76 82 11 12 27 202 10 34 101 403 11 23 58 262 2 35 13 351 15 12 198 4 50 21 671 7 110 16 899 66 280 312 3068 1.64 6.99 7.79 76.60 . Seasonal variation of litter arthropods abundance in the Arboretum of Ruhande. The Shannon diversity indices Hʹ of litter arthropods sampled in September 2012 (end of shot dry season) was Eucalyptus saligna followed by E. tereticornis and Entandrophragma excelsum (Table 4). The Shannon indices of the arthropods sampled in January 2013 are highest in Eucalyptus maculata stand (Table 4). Biodiversity analysis of litter arthropods sampled in April 2013 resulted in Shannon diversity indices that were highest in Entandrophragma excelsum Eucalyptus maculata stand (Table 4). Considering the Shannon diversity indices for all seasons, it can be suggested that on the average, Eucalyptus plantations had less litter arthropod diversity in Entendrophragma excelsum stand (Table 4). Shannon diversity indices of litter arthropods sampled in September 2012 were higher than those in wet seasons (Table 4). The Shannon diversity indices = 0.66; p < 0.05; Fig. 2). Chilopoda Crustacea Diplopoda Dry Season Shot wet season Long wet season www.iiste.org Abundance of arthropod individuals as sampled in April 2013 in the litter of 8 plantation types in the Entandrophragma excelsum. Insecta Total Individuals % 220 5.49 284 7.09 585 14.6 376 9.38 438 10.93 247 6.16 780 19.47 1075 26.84 4005 76.60 . Seasonal variation of litter arthropods abundance in the Arboretum of Ruhande. The Shannon diversity indices Hʹ of litter arthropods sampled in September 2012 (end of shot dry season) was Entandrophragma excelsum stands e arthropods sampled in January 2013 are highest in Entandrophragma stand (Table 4). Biodiversity analysis of litter arthropods Entandrophragma excelsum stand (Table 4). Considering the Shannon diversity indices for all had less litter arthropod diversity in Shannon diversity indices of litter arthropods sampled in September 2012 were higher than those in wet seasons (Table 4). The Shannon diversity indices Insecta
  • 5. Journal of Biology, Agriculture and Healthcare www.iiste.org ISSN 2224-3208 (Paper) ISSN 2225-093X (Online) Vol.3, No.9, 2013 53 Table 4. Shannon diversity indices for litter arthropods sampled in September 2012, January 2013 and April 2013. September 2012 January 2013 April 2013 Plantation type Shannon index Eveness Shannon index Eveness Shannon index Eveness Entandrophragma excelsum 0.471 0.292 0.48 0.298 0.542 0.337 Eucaltypus citriodora 0.441 0.275 0.382 0.298 0.422 0.337 Eucalytpus grandis 0.439 0.273 0.296 0.214 0.421 0.337 Eucalyptus maculata 0.439 0.273 0.426 0.298 0.426 0.337 Eucalytpus maidenii 0.431 0.311 0.235 0.298 0.311 0.337 Eucalyptus microcorys 0.413 0.298 0.289 0.208 0.308 0.222 Eucalyptus saligna 0.504 0.364 0.249 0.298 0.246 0.337 Eucalyptus tereticornis 0.493 0.306 0.41 0.298 0.264 0.337 Figure 2. Positive relationship between litter pH and Shannon diversity indices for the arthropods sampled in September 2012. 4. Discussion This study is the first that has examined the likely impact of wet and dry seasons on leaf litter arthropods in a number of Eucalyptus plantation types and Entendrophragma excelsum stands at the Arboretum of Ruhande, Rwanda. Seasonality has affected the abundance and diversity of litter arthropods, with wet seasons having the higher number of arthropods (Fig. 1). This may be explained by the fact that the litter biomass was greater in wet seasons than in dry season (Pearson et al., 1986). It may also result from the development of understory vegetation that could be eaten by the arthropods during wet seasons (Pereira et al., 2001). Seasonal variability is also linked to temperature change, which determines the growth rate of arthropods (Wolda, 1988). Seasonality of litter arthropods has been studied by many authors. For instance, most arthropod groups had high number of individuals during wet seasons but declined during dry month in an Australian rain forest (Frith and Frith, 1990). Similar finding was observed in Amazonian forest, Brasir (Silveira et al., 2009). Arthropod abundance in wet season was of 2.3 times higher than that in dry season as observed in a tropical oceanic island (Tanaka and Tanaka, 1982). The abundance of arthropods in wet seasons were very high comparable to those in dry seasons in a lowland forest in Southern Peru (Pearson et al., 1986). It was noted that climatic seasons tend to translate into seasonal activity patterns in living organisms including arthropods which became active only at certain times of the year (Wolda, 1988). y = 0.0798x + 0.0594 R² = 0.6584 0.3 0.35 0.4 0.45 0.5 0.55 4 4.5 5 5.5 6 Shannonindex Litter pH
  • 6. Journal of Biology, Agriculture and Healthcare www.iiste.org ISSN 2224-3208 (Paper) ISSN 2225-093X (Online) Vol.3, No.9, 2013 54 In this study, the abundance of litter arthropods increased from 27.5% in September 2012, to 33.6% in January 2013 (shot wet season) and 38.9% in April 2013 (long wet season) (Fig. 1). These figures indicate that the litter invertebrates increase with the precipitation, but heavy rainfall tends to decrease litter amount and soil invertebrate densities (Chiba et al., 1975). Shannon indices of arthropods sampled in September 2012 were higher than those in other seasons (Table 4), indicating that the heavy rain tends to decrease arthropods diversity as it was also noted by Chiba et al. (1975). The Eucalyptus plantations have been more blamed worldwide to affect negatively litter arthropods (Zahn et al., 2009) suggesting that some Eucalyptus species do not allow development of understory vegetation which may be feed by arthropods (Pereira et al., 2001). The Eucalyptus species are also blamed for having poor organic carbon (Signihal et al., 1975; Balagopalan and Jose, 1995; Animon et al., 1999). It has also been suggested that some Eucalyptus species are efficient competitors for water from soil (Poore and Fries, 1985). Having oil glands in their leaves (Penfold and Wills, 1961) and tough leathery leaves (Edward and Wanjura, 1990) have been also included among reasons to blame Eucalyptus plantations to limit development of litter arthropods. However, the results of this study show that the stands of E. tereticornis, E. saligna, and E. grandis have a greater abundance of arthropods than the litter of Entendrophragma excelsum stand that has been used for comparison (Tables 1–3). These Eucalyptus stands allow the growth of herbs and shrubs of various types, which serve as food to inhabiting arthropods (Pereira et al., 2001). It was noted that high vegetation diversity supports in turn a high invertebrate diversity (Teodorescu and Cogalniceanu, 2002) and the poor undergrowth of herbaceous plants result in reduced arthropods abundance (Mallick and Pati, 1996). The Class of insects has remained most dominant among arthropods collected in all seasons (Tables 1–3; Fig. 1), this may be explained by the fact that the Class of insects has Hymenoptera order which is worldwide abundant (Chavhan et al., 2011), including Formicidae (ants) which prefer wet litter habitat conditions and deep litter depth (Sabu, 2005) and increasing with the increase of their specific food resources such as larva and other arthropods (Samson et al., 1997; Shattock and Barnet, 2001). Insects are also able to adapt to the extreme environmental conditions such as rain, high humidity and low litter temperature (Stork, 1988; Basu, 1997). The Centipedes remained the fewest in all seasons that we sampled (Fig. 1) and under all plantation types. This may be because they do not eat litter; they are primarily carnivorous, eating marine insects (Chamberlin, 1920). On the other hand, Millipedes were higher in dry season (Fig. 1) and it was contrary to previous finding that they usually have their highest activity in spring and autumn (Voigtländer, 1996; Tajovsky, 2000). This high number may support the note by Berg and Hemerik (2004) that some millipedes do not have ecological preference. On the average, the arthropods diversity (Shannon index) in Eucalyptus stands was lower than that in Entendrophragma excelsum stands (Table 4). This may result from multiple reasons: Eucalyptus stands have less understory vegetation types (Pereira et al., 2001); they are poor in organic carbon (Animon et al., 1999); their effectiveness in competition for water (Poore and Fries, 1985); having leaves that leachate directly on certain species of arthropods (Canhoto and Laranjeira, 2007; Zahn et al., 2009) and their influence on soil and litter pH which has shown correlation with diversity indices (Fig. 2). All these conditions can unfavour the establishment of certain species of arthropods in Eucalyptus stands. 5. Conclusions The present results provide an overview on the seasonal variation of litter arthropods in some Eucalyptus plantations at the Arboretum of Ruhande. The study confirms that the seasonality has an effect on the abundance and diversity of arthropods, with highest figures in wet seasons. The negative effect of Eucalyptus plantations on arthropods abundance was not exclusively confirmed as some stands of Eucalyptus species had arthropod abundance comparable to those under native Entandrophragma excelsum stands. The Class of insects was the most abundant in all seasons with relative frequency of 54.8%, 77.3% and 76.6% in September 2012, January 2013, and April 2013 sampling periods respectively. This study need to be repeated under forest plantations located in different ecological zones in Rwanda. Acknowledgements The author is grateful to the authority of the Arboretum of Ruhande that authorized to conduct this study under their forest plantations and to BSc students Sebera F., J.D. Dusabimana, and C.S. Iradukunda who have assisted in field data collection. References Animon, M.M., Ashokan, P.K., Sudhakar, K., Jayashankar, S., Dhanesh, K.P. (1999). Physicochemical and Biological properties of soil under Acacia auriculiformis and Eucalyptus tereticornis plantation. 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