The Science of the Total Environment 225 1999.

231240

Comparison of chemical elements in Dipterocarpaceae and

Euphorbiaceae from a tropical rain forest in Sarawak,
Malaysia
G. Breulmann a , K. Ogino a , B. Markert b,U , U.S. Leffler b , U. Herpin c ,
V. Weckert b , R. Konschak b , Y. Kikugawaa , T. Ohkubo d
a

School of En ironmental Sciences, Department of Ecosystem Studies, The Uni ersity of Shiga Prefecture, 2500 Hassaka,
Hikone 522-8533, Japan
b
International Graduate School (IHI) Zittau, Markt 23, 02763 Zittau, Germany
c
Federal Institute for Geosciences and Natural Resources, Stilleweg 2, 30655 Hanno er, Germany
d
Department of Forest Science, Faculty of Agriculture, Utsunomiya Uni ersity, Utsunomia 321-8505, Japan
Received 3 September 1998; accepted 12 October 1998

Abstract
Leaves of Dipterocarpaceae, a major canopy component tree, and Euphorbiaceae, predominantly occurring in the
second layer, were analysed for 43 chemical elements. The comparison between the two families revealed significantly lower concentrations for the vast majority of elements in Dipterocarpaceae. All elements except Cu, Cs and
Ce were found in higher concentrations in Euphorbiaceae. Furthermore, Euphorbiaceae showed a higher biological
variation for most elements indicated through higher coefficient of variances CV. values. The fingerprints revealed a
general tendency in both families investigated to exhibit rather low element concentrations compared to the
reference plant proposed by Markert 1996.. Out of the 43 chemical elements only Ni showed remarkable positive
deviations in both families, while the deviation of 6700% found for Co in Euphorbiaceae was striking. In
Dipterocarpaceae the elements N, Co, Cu, Mn, Li, Cs, Mg and Th were found in concentrations similar to the
reference plant while all other elements exhibited rather high negative deviations. In Euphorbiaceae more elements
occurred similar to the reference plant, however, the general tendency of negative deviations was obvious. Due to
their specific environment, trees from tropical forest might have a rather different chemistry from trees in the
Northern Hemisphere. 1999 Elsevier Science B.V. All rights reserved.
Keywords: Multi-element analysis; Dipterocarpaceae; Euphorbiaceae; Tropical rain forest; Trace elements; Plants;
Fingerprinting

Corresponding author.

0048-9697r99r$ - see front matter 1999 Elsevier Science B.V. All rights reserved.
P I I: S 0 0 4 8 - 9 6 9 7 9 8 . 0 0 3 6 9 - 6

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G. Breulmann et al. r The Science of the Total En ironment 225 (1999) 231240

1. Introduction

2. Material and methods

With respect to the dynamics of organic and

inorganic matter, tropical plant communities differ greatly from plant communities elsewhere due
to their special characteristics, such as the structure and composition of life forms, or the complex and multi-layered structure of the forests
with their wide floristic diversity of species Jayasekera, 1994.. In contrast to the temperate regions there are no marked seasonal variations in
the tropical rain forests. Uptake rates and interactions of chemical elements in tropical forests
are significantly affected by high levels of humidity, light intensity and temperature as well as by
differing life cycles compared to plants growing in
the Northern Hemisphere Epstein, 1972..
Dipterocarpaceae and Euphorbiaceae are predominately tropical in their distribution. The
mixed dipterocarp forests of the Lambir Hills
National Park shows a multi-layered structure.
The emergent trees are predominated by dipterocarp species whereas Euphorbiaceae occur mainly
in the second layer. Mixed dipterocarp forests are
the worlds main source of hardwood timber and
are therefore of considerable economic importance.
Trees of Dipterocarpaceae are in general
resinous whose resin properties have been described by Hegnauer 1966.; the most common
resins are oleoresins balms, resins.. Their volatile
portion contains sesquiterpenes, in some instances monoterpenoids. Dryobalanops aromatica
is known to produce Borneo camphor containing
borneol antipyretic s against fever, analgesic s
against pain, anti-inflammatory. Farnsworth and
Soejarto, 1991.. Terpenes are toxins and feeding
deterrents to herbivores Taiz and Zeiger, 1991..
Several genera of Euphorbiaceae represent
valuable resources of raw materials, e.g. rubber,
castor oil, cassava, tung oil, vegetable tallow, timber, purgatives or dyes Heywood, 1978.. The
presence of latex exudates is a characteristic to
this family Borriss and Libbert, 1984.. Hegnauer
1966. showed that the chemical constituents of
Euphorbiaceae are as heterogeneous as is their
morphology.

2.1. Study site

The research site is located in the Lambir Hills
National Park 42N, 11350E. in the north west
of Borneo, approximately 30 km south of Miri,
the capital of the Fourth Division, Sarawak. The
climate around Miri including the Lambir Hills is
always wet but monsoonal due to distinct shifts in
the prevailing winds; the north monsoon known
as the wet Landas season from November to
February and the south monsoon from April to
September. The park consists of the central portion of the Lambir Hills with the highest peak of
rugged sandstone escarpment of 458 m in altitude
Yamakura et al., 1995a..
The mean annual temperature and precipitation are 26.6C and 2680 mm, respectively. In the
park, a research plot of 8 ha 200 = 400 m. was
set up under the auspices of the Canopy Biology
Program in Sarawak CBPS.. The CBPS was initiated in the international co-operative project
Long-term Ecological Research Project at Lambir Hills National Park, Sarawak by Forest Department Sarawak; Harvard University, US;
Ehime University, Osaka City University, Kyoto
University and several other Japanese universities
in 1992 Inoue and Hamid, 1995..
The topography of the Lambir Hills National
Park is characterized by a hilly and undulating
terrain with steep slopes including scars of landslides. Yamakura et al. 1995b. reports that 85%
of the total park area represent slopes, while the
other 15% consist of ridges and valleys, which
dissect the park area and seem to give rise to
finely fragmented local habitats for plants.
Wall 1962. reported six major soil groups in
the Lambir Hills National Park; immature alluvial
soils around riverbanks, red-yellow podsols ultisols. on slopes and ridges, podsols around the hill
summit of Bukit Lambir, and immature regosols
on very steep slopes. Parent materials are tertiary
sandstone andror shale Hirai et al., 1995.. The
research plot is located on a clayey soil site near
the headquarters of Lambir Hills National Park.
The soil nutrient . heterogeneity in the Lambir

G. Breulmann et al. r The Science of the Total En ironment 225 (1999) 231240

park is likely high, even on the microsite scale

due to the undulating terrain, steepness of slopes
or edaphic heterogeneity in combination with biotic factors like soil fauna. Detailed information
on soil properties in the research plot is not yet
available.
The plot is covered by a well developed mixed
dipterocarp forest at altitudes of 100200 m above
sea level, which is regarded as having one of the
richest lowland rain forest floras of the Old World
Inoue et al., 1994.. The emergent trees are dominated by dipterocarp trees and consist of the
following families: Dipterocarpaceae Shorea spp.,
Dipterocarpus spp., Dryobalanops spp.., Leguminosae Koompassia excelsa, Sindora spp., Dialium
spp.. and Sapotaceae Madhuca crassipes.. In the
second layer more families occur, e.g. Anacardiaceae, Burseraceae, Euphorbiaceae, Moraceae,
Myristicaceae, Myrtaceae, etc. Nagamasu et al.,
1994..
2.2. Sampling and instrumental analyses
The sampling was performed during two visits
end of 1993; end of 1994. to the Lambir Hills
National Park in the central part of the research
plot ; 1.38 ha., in which all trees with diameter
at breast height DBHs 130 cm. G 10 cm were
tagged and recorded by Ohkubo et al. personal
communication.. The collected leaves were
cleaned with tissue paper soaked with distilled
water. All samples were pre-dried in a field drying-oven for 48 h. After drying the samples for 48
h at 80C at Ehime University, Matsuyama, Japan,
they were homogenised with agate mortar and
pestle to reduce the risk of contamination. The
digestion and the instrumental measurement were
carried out in different institutes in Japan and
Germany. In all cases a wet digestion was performed, however, different digestion solutions and
analytical instruments were utilized in accordance
with the respective laboratory facilities.
The samples collected during the first visit were
digested in a mixture of HNO3 and HClO4 in an
aluminium block. The instrumental analysis was
performed by inductively coupled plasma atomic
emission spectroscopy ICPrAES., Seiko SPS
1500 VR, for Al, Mn, Fe, Cu, Zn, Sr, B, Ba and by

233

atomic absorption spectrophotometry AAS., Shimadzu AA-640-12, for Ca, Mg, Na and K at the
College of Agriculture, Kyoto University.
The samples collected during the second visit
were digested in a mixture of H 2 SO4 and H 2 O 2
Fentons reaction. using a sandbath. The instrumental measurement was performed by
ICPrAES, Shimadzu ICPS-1000 IV, for Zn, Fe,
Cu, Sr, Al at the Faculty of Agriculture, Kochi
University. K was analyzed by AAS, Shimadzu
AA-630-02 at the Faculty of Agriculture, Ehime
University.
All samples were digested again in HNO3 using
high pressure Teflon vessels with quartz glass
inserts. The instrumental measurement was performed by inductively coupled plasma mass spectrometry ICPrMS., Perkin Elmer Elan 5000 for
approximately 80 chemical elements at the International Graduate School Zittau, Germany. Several elements were excluded from this paper as
the results were either always below the detection
limit or showed rather erratic values.
The N content was measured by an automatic
Kjeldahl device, Gerhardt Vapodest-6, at University of Osnabruck,
Germany.
The accuracy of the digestion procedures was
checked by use of Standard Reference Material
NIST 1571, Orchard Leaves, and NIST 1572, Citrus Leaves, from the National Bureau of Standards, Washington. The certified values and the
values obtained for the respective measurement
are shown in Table 1. The elements not included
in this table are not certified.
For several elements we performed two measurements for the same sample. These values we
averaged if the deviation between the values obtained was less than 10%. In case the deviation
exceeded 10%, one value was selected on the
basis of the Standard Reference Material for the
respective measurement.
The data presented in this paper are based on
the taxonomical level of the family and represent
the mean concentration of the leaf samples for
Dipterocarpaceae 18 species. and Euphorbiaceae 5 species.. Species differences were not
considered. The comparison on the basis of
species for the respective family can be found in
Breulmann et al. 1997, 1998..

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G. Breulmann et al. r The Science of the Total En ironment 225 (1999) 231240

Table 1
Comparison of certified values and values obtained for the Standard Reference Materials
Certified values

Citrus leaves NBS 1571.

Ca %.
K %.
Mg %.
Na
Sr
Al
Fe
Zn
Mn
Ba
Cu
Pb
Rb
As
Cr
Ni
Mo

Obtained values at
Zittau

Kyoto

Kochi

3.15" 0.10
1.82" 0.06
0.58" 0.03
160 " 20
100 " 2
92 " 15
90 " 10
29 " 2
23 " 2
21 " 3
16.5" 1
13.3" 2.4
4.84" 0.06
3.10" 0.30
0.8" 0.2
0.6" 0.3
0.17" 0.09

3.04
1.77
0.45
139.34
87.48
62.31
90.68
25.30
20.34
17.79
13.86
11.21
4.44
2.90
1.08
0.65
0.12

2.55
1.42
0.44
128.47
89.68
74.00
82.00
26.93
19.03
23.01
13.61
n.d.
n.d.
n.d.
n.d.
n.d.
n.d.

n.d.
n.d.
n.d.
n.d.
88.35
67.80
72.08
32.66
n.d.
n.d.
12.62
n.d.
n.d.
n.d.
n.d.
n.d.
n.d.

2.76" 0.05

Osnabruck

2.58

Orchard leaves NBS 1572.

N %.

All data are in mgrkg dry wt. with exception of Ca, K, Mg and N given in %.
n.d.s not determined.

3. Results and discussion

In Fig. 1 the mean concentrations of Dipterocarpaceae and Euphorbiaceae are shown as

stacked columns. In the figure the total concentration of both families represents 100%. Obviously nearly all elements were found in higher
concentrations in Euphorbiaceae. Out of the 43
elements analyzed Cu, Cs and Ce showed a higher
mean concentration in Dipterocarpaceae, with Cu
being the only element with essential character
for plants.
An exceptionally high difference was found for
Co; the mean concentration of Euphorbiaceae
was more than 100 times higher than in the
Dipterocarpaceae Table 2.. Most higher plants
are reported to contain less than 1 mgrkg dry wt.
Co Adriano, 1986; Kovacs et al., 1994.. Jayasekera 1993. reported somewhat higher Co concen-

trations 1.86 mgrkg dry wt.. in Allophylus arians Sapindaceae., a densitydominant tree
species from a montane rain forest in Sri Lanka.
The Co concentrations in two out of the investigated species of Euphorbiaceae, i.e. Koilodepas
lae igatum and Trigonostemon sp. no . aff. ionthocarpus, were substantially higher with 15.35 mgrkg
dry wt. and 18.94 mgrkg dry wt., respectively
Breulmann et al., 1997.. The status of Co as a
micro-nutrient is not yet certain, however, it has
been shown that deficiency of Co can lead to
chlorosis and leaf-drop Berrie et al., 1987.. Co is
essential for the nitrogen fixing system of Rhizobium bacteria in symbiosis with Leguminosae
Epstein, 1972; Markert, 1998.. Non-nodule nitrogen fixing bacteria living on and in the leaves
have been reported for several non-Leguminosae
Jones, 1982; Whitmore, 1985.. Higher Co concentrations could therefor be beneficial for the N
fixation.

G. Breulmann et al. r The Science of the Total En ironment 225 (1999) 231240

Fig. 1. Comparison of the mean concentrations in Dipterocarpaceae and Euphorbiaceae. The total concentration of both families represents 100%.

235

G. Breulmann et al. r The Science of the Total En ironment 225 (1999) 231240

236

Table 2
Mean concentrations in leaves of Dipterocarpaceae and Euphorbiaceae

Dipterocarpaceae
Euphorbiaceae

Dipterocarpaceae
Euphorbiaceae

Dipterocarpaceae
Euphorbiaceae

Dipterocarpaceae
Euphorbiaceae

NU

SiU

CoU

Cr

CuU

Fe

MnU

MoU

NiU

VU

ZnU

1.41
13.
1.61
17.

217.33
123.
532.68
49.

0.11
78.
13.61
84.

0.47
24.
0.53
47.

5.96
28.
4.72
29.

38.44
30.
45.04
36.

204.04
79.
600.73
57.

0.0097
89.
0.0261
77.

3.26
57.
9.88
100.

0.0191
43.
0.0351
65.

11.44
31.
15.97
29.

Li

Na

KU

Rb

CsU

MgU

CaU

SrU

Ba

AlU

0.11
83.
0.22
160.

67.64
35.
172.61
218.

0.92
29.
2.02
71.

13.06
30.
15.19
67.

0.11
75.
0.06
113.

0.17
33.
0.26
58.

0.30
52.
0.64
48.

15.13
51.
37.43
45.

17.18
52.
22.43
60.

18.82
33.
23.34
51.

22.38
26.
40.19
69.

GaU

In

TlU

Sn

PbU

AsU

SbU

Bi

IU

YU

LaU

0.01
91.
0.05
205.

0.0002
59.
0.0002
90.

0.0025
90.
0.0100
126.

0.0365
30.
0.0381
27.

0.28
57.
0.48
100.

0.0327
57.
0.2326
184.

0.0002
141.
0.0005
102.

0.0012
65.
0.0014
207.

0.17
81.
0.25
53.

0.0089
89.
0.0161
69.

0.0050
61.
0.0082
76.

CeU

Pr

Nd

EuU

Tb

Th

TiU

ZrU

NbU

0.0851
163.
0.0238
75.

0.0011
70.
0.0015
80.

0.0028
83.
0.0039
75.

0.0006
62.
0.0008
62.

0.0001
92.
0.0001
96.

0.0026
99.
0.0040
86.

0.0012
97.
0.0018
69.

2.02
22.
3.13
25.

0.0052
37.
0.0100
75.

0.0003
114.
0.0011
93.

The values are given in mgrkg dry wt. except for N, K, Mg and Ca in %..
An asterisk indicates significance of t values at 0.01 probability level.
Values in parentheses indicate the coefficient of variance in %..

The mean concentrations of all elements for

both families are given in Table 2, where an
asterisk indicates significance of the t values at
0.01 probability level. The majority of elements
showed significantly higher concentrations in Euphorbiaceae. Out of the 43 elements analysed, 15
elements, i.e. Cr, Fe, Li, Na, Rb, Ba, B, In, Sn, Bi,
Pr, Nd, Tb, Th and U showed non-significant
differences. The lower element concentrations
found in the overstory trees of Dipterocarpaceae
in contrast to the mainly in the second layer
occurring Euphorbiaceae correspond with the results of certain other studies conducted in tropical forests. Breulmann 1996. reported generally
higher element concentrations in understory trees
than in overstory trees in Sarawak, Malaysia, Golley et al. 1975. observed this phenomena in
Panamanian Forest and it was also found in an
ongoing study on Hill Evergreen Forest in Thailand Pampasit, personal communication.. It is
suggested that biota living in profusion on the

understory compartments are instrumental in

concentrating mineral elements in lower strata of
the forest possibly due to factors like lower radiation and higher humidity.
The coefficient of variance CV. indicates the
relative degree of deviations from the mean value.
N, the most abundant element, showed the lowest
CV value in both families with 13% and 17% in
Dipterocarpaceae and Euphorbiaceae, respectively Table 2.. All elements regarded as essential showed CV values below 100%, with the
highest CV 89%. occurring for Mo Dipterocarpaceae.. The elements N, Cu, Zn, Ca, Sn, Eu, Tb
and Ti showed similar CV values in both families,
while the majority of the remaining elements
showed higher CV values in Euphorbiaceae. This
indicates a wider distribution range of those elements concentrations around the mean and
thereby a higher biological variation in the Euphorbiaceae.
The fingerprints of the selected chemical ele-

G. Breulmann et al. r The Science of the Total En ironment 225 (1999) 231240

ments against the reference plant proposed by

Markert 1996. are shown in Fig. 2. The reference plant, comparable to reference man established by the ICRP 1975., allows the establishment of fingerprints. These fingerprint
graphs are generated by standardizing the values
of the reference plant and by graphically displaying positive or negative percentage deviations of
the plant types from the normal values of the
reference plant. One advantage of the fingerprint graphs is the ability to portray element
distribution patterns within a plant species or
family. in detail without having to spread out any
concentration ranges of elements, which occur in
varying orders of magnitude, and without having
to resort logarithmic scales. Likewise, by standardization based on the reference plant, not
only are extremely high element concentrations
in a sample taken into consideration, but also
minimal values of individual elements are considered to the same degree Markert, 1996..
Dipterocarpaceae as well as Euphorbiaceae
showed substantially lower concentrations for the
majority of elements compared to the reference
plant. Nickel was found in higher concentrations
in both families. Jayasekera 1993. found higher
Ni concentrations in all five investigated tree
species of tropical forest in Sri Lanka and suggested it might be attributed to a higher uptake of
Ni at lower pH values prevailing in the soil as
reported by Baumeister and Ernst 1978. and
Adriano 1986.. The soil pH in the Lambir Hills
National Park was in the range 4.25.2 Hirai et
al., 1995..
The Dipterocarpaceae showed a conspicuous
positive deviation solely for Ni, whereas Mn and
Mg occurred in similar concentrations to the reference plant. N, Co, Cu, Li, Cs, and Th showed
negative deviations of less than 50%, while all
other elements showed rather large negative deviations, revealing comparatively low element concentrations.
The Euphorbiaceae showed striking positive
deviations for Co and Ni with 6700% and 559%,
respectively. Manganese and As were found in
elevated concentrations, however, the deviations
were less remarkable. Compared to the Dipterocarpaceae more elements occurred within the

237

range of the reference plant, i.e. N, Si, Li, Na, K,

Ca, Sr, Ba, B, Al, Th and Ti, however, the general
tendency of negative deviations is obvious also for
the Euphorbiaceae.
Despite of the significantly different concentrations found for the majority of elements investigated in Dipterocarpaceae and Euphorbiaceae,
both families showed substantially lower concentrations compared to the reference plant. In this
context is has to be remembered that organisms
are quite diverse and highly adaptive in the element requirements and particularly in their tolerances. Although it is perfectly normal for plants
to be different from the reference plant, the
results suggest possibly low element requirements
for both families investigated. Due to the specific
environment in an ecosystem without marked
seasonal variations, predominantly poor soils and
factors like high levels of precipitation, humidity,
light intensity or temperature, trees from tropical
rainforests might have a rather different chemistry from trees of the Northern Hemisphere.
More information is needed to understand the
dynamics and characteristics of chemical elements in tropical forests.
4. Concluding remarks
This paper provides the concentrations of 43
chemical elements in Dipterocarpaceae and Euphorbiaceae from a mixed dipterocarp forest in
Sarawak, Malaysia.
The overstory trees of Dipterocarpaceae
showed significantly lower concentrations for the
majority of elements than the Euphorbiaceae occurring predominantly in the second layer.
A comparison with the reference plant proposed by Markert 1996. revealed rather low concentrations for most elements. The positive deviations for Ni occurring in both families were attributed to a possibly higher uptake at lower pH
values in the soil. Moreover the Euphorbiaceae
showed rather large positive deviations for Mn
and As. Striking was the difference in the Co
contents with 6700%. In general both families
showed rather low element concentrations.
A physiological explanation of the results obtained is only possible to a certain extent, as the

238
G. Breulmann et al. r The Science of the Total En ironment 225 (1999) 231240

Fig. 2. Fingerprints of Dipterocarpaceae and Euphorbiaceae showing the relative deviation.

G. Breulmann et al. r The Science of the Total En ironment 225 (1999) 231240

function of most elements analysed is not yet

understood. Furthermore differences occuring in
the element contents are element- and plantspecific Markert, 1993.. Recently it has become
apparent that the determination of essentialities
of microelements is difficult, especially in the
trace range. However, the list of micronutrients is
likely to increase in the future and the increased
utilisation of instrumental multi-element techniques biological investigations will probably ensure that essential characteristics of further
chemical elements will be recognised in the future.
From the toxicological and nutrient physiological point of view a characterisation of ecosystems
on a chemical basis provides important information on the concentrations, effects and reactions
of individual elements in different systems
Markert, 1995; Rossbach et al., 1992.. So far the
interest has been mainly focused on data of the
Northern Hemisphere, but from the biogeochemical scope urgently needs to be extended
to cover tropical and subtropical systems.

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