Werner Et Al 2012 Epiphytic Biomass of A Tropical Montane Forest Varies With Topography
Werner Et Al 2012 Epiphytic Biomass of A Tropical Montane Forest Varies With Topography
Werner Et Al 2012 Epiphytic Biomass of A Tropical Montane Forest Varies With Topography
Functional Ecology, Institute of Biology and Environmental Sciences, University of Oldenburg, Carl-von-Ossietzkystrae 9-11, 26111 Oldenburg, Germany
Plant Ecology, Institute of Plant Sciences, Untere Karspule 2, University of Gottingen, 37073 Gottingen, Germany
Institute of Botany (210), University of Hohenheim, Garbenstrae 30, 70593 Stuttgart, Germany
Institute of Soil Science, University of Hannover, Herrenhauser Strae 2, 30419 Hannover, Germany
(Accepted 22 September 2011)
Abstract: The spatial heterogeneity of tropical forest epiphytes has rarely been quantified in terms of biomass. In
particular, the effect of topographic variation on epiphyte biomass is poorly known, although forests on ridges and
ravines can differ drastically in stature and exposure. In an Ecuadorian lower montane forest we quantified epiphytic
biomass along two gradients: (1) the twigbranchtrunk trajectory, and (2) the ridgeravine gradient. Twenty-one
trees were sampled in each of three forest types (ridge, slope, ravine positions). Their epiphytic biomass was extrapolated
to stand level based on basal areaepiphyte load relationships, with tree basal areas taken from six plots of 400 m2
each per forest type. Our results document the successional addition and partial replacement of lichens by bryophytes,
angiosperms and finally dead organic matter along the twigbranchtrunk trajectory. Despite having the highest tree
basal area, total epiphytic biomass (mean SD) of ravine forest was significantly lower (2.6 0.7 Mg ha1 ) than
in mid-slope forest (6.3 1.1 Mg ha1 ) and ridge forest (4.4 1.6 Mg ha1 ), whereas maximum bryophyte water
storage capacity was significantly higher. We attribute this pattern to differences in forest dynamics, stand structure and
microclimate. Although our study could not differentiate between direct effects of slope position (nutrient availability,
mesoclimate) and indirect effects (stand structure and dynamics), it provides evidence that fine-scale topography needs
to be taken into account when extrapolating epiphytic biomass and related matter fluxes from stand-level data to the
regional scale.
Key Words: carbon storage, crown humus, dead organic matter, Ecuador, epiphytes, maximum water storage capacity,
succession, topographic heterogeneity
INTRODUCTION
Epiphytes can strongly increase the retention of
atmospheric water and mineral nutrients by tropical
forests (Bruijnzeel et al. 2011, Cavelier et al. 1997,
Holwerda et al. 2010, Tobon et al. 2010, Umana &
Wanek 2010). Epiphytic biomass can account for over
80% of non-woody canopy biomass (Nadkarni et al.
2004) and store up to 50 Mg ha1 of water (Pocs
1980). By increasing the spatial heterogeneity of canopy
throughfall, epiphytes may even drive niche availability
and recruitment of terrestrial plants (Oesker et al. 2010,
Zimmermann et al. 2007).
Moist-forest epiphytes typically show marked succession as primary twigs grow in diameter and age, with
lichens pioneering before bryophytes become dominant,
24
F. A. WERNER ET AL.
which is relatively open and stunted (812 m tall). Midslope forest is intermediate in terms of tree species composition and structure (canopy height 1218 m). Concurrent
with soil nutrient concentrations, tree basal area
increment and turnover decrease strongly from ravines
to ridges (Homeier et al. 2008, 2010; Wilcke et al. 2008).
(Gunter
et al. 2008) in two neighbouring microcatchments. Fifteen canopy and subcanopy trees of
various size classes were randomly selected in ravine
forest (20002100 m asl), mid-slope forest (20502150
m) and ridge-top forest (21002200 m). Six additional
understorey treelets per forest type (mostly saplings;
Appendix 1) were sampled exclusively for the projection of
epiphytic biomass to area. Trees that had suffered damage
from felling were omitted. Extensive data on the local tree
species composition (Homeier et al. 2010) suggest that our
samples were representative of the local tree communities
(Appendix 1).
We distinguished six substrate classes: twigs (02
cm diameter), thin branches (>25 cm), medium-sized
branches (>510 cm), large branches (>1020 cm),
major limbs (>20 cm) and trunks. Sampled substrate
sections ranged from 10 cm (trunks and larger branches)
to 100 cm (twigs) in length. Where applicable, we
randomly took biomass samples from all diameter classes
of three major branches per tree (one from upper, midand lower canopy each). In trunks, one sample was
taken from base, mid-section and upper section each.
We visually estimated the total length of twigs/branches
within each branch class of a sampling tree to allow for
an extrapolation of total biomass per tree, while trunk
lengths were measured with a tape.
In total, 710 samples were taken, transferred in plastic
bags to the field station Estacion Cientfica San Francisco,
and separated in the laboratory. We distinguished
between bryophytes, macrolichens (foliose and fruticose
growth types), pteridophytes, angiosperms and dead
organic (biological) matter (DBM henceforth; canopy
humus and epiphyte litter). Samples were oven-dried to
constant weight at 70 C and weighed with an electronic
balance (Navigator, Ohaus, Pine Brook, NJ, USA). In
order to project our data to forest area, we measured the
diameter at breast height (dbh) for all tree trunks of dbh
5 cm in 18 plots of 20 20 m, six each in ravine, slope
and ridge position. These plots were set up in mature forest
stands at 19602210 m within RBSF.
Prior to analysis we divided raw sample dry weights by
sample area (cylinder length perimeter) and averaged
25
Table 1. Epiphytic biomass (g m2 substrate surface) in three adjacent montane forest types in south-east Ecuador. Given is the mean SE (median).
Biomass data for branches is ordered by diameter class, while data for trunks are treated as trunks irrespective of diameter. Different superscript
letters mark parameters showing significant differences (P < 0.05; Scheffe post hoc tests following ANCOVA) between forest types after false
discovery rate correction. Note that branches > 20 cm diameter were not tested for significant differences.
Substrate diam. (cm)
Ravine forest
02
25
510
1015
> 20
Trunk
Slope forest
02
25
510
1015
> 20
Trunk
Ridge forest
02
25
510
1015
> 20
Trunk
Lichens
Bryophytes
Pteridophytes
Angiosperms
Dead organic
matter
Total epiphytic
biomass
15
15
15
12
5
15
19 6(12)
61 18(38)
28 7(22)
32 11(20)
11 5(11)
9ab 3(4)
19 6(8)
57 12(52)
72 13(50)
121 47(68)
106 35(64)
44a 11(28)
0.1 0.1(0.0)
5 3(0.0)
6 3(0.0)
35 17(9)
2 1(2)
3 1(0.2)
4 2(0.0)
26 15(2)
73 43(5)
211 155(32)
70 52(7)
30a 11(10)
3 2(0.0)
6a 3(2)
39a 30(6)
191 114(10)
90 45(49)
34a 22(6)
45a 12(33)
155 28(146)
216 68(132)
591 275(234)
279 120(189)
120 33(85)
15
15
14
7
3
15
24 7(13)
59 21(30)
47 21(8)
20 11(6)
11 9(3)
3a 2(0.4)
18 8(6)
71 25(24)
95 23(58)
58 25(54)
16 14(3)
52ab 12(51)
7 5(0.0)
3 2(0.0)
8 5(0.1)
8 5(4)
1 1(0.0)
34 13(18)
13 6(6)
29b 10(16)
68ab 18(47)
118 48(43)
144 123(41)
631b 250(210)
79b 21(57)
214 45(142)
354 62(405)
381 135(232)
281 245(74)
958 311(517)
15
15
13
6
0
15
24 7(16)
58 14(60)
33 7(28)
20 6(16)
()
16b 4(9)
14b 9(1)
58 25(22)
95 21(58)
170 38(152)
()
99b 16(61)
1 1(0.0)
25 18(0.0)
24 11(3)
59 56(2)
()
30 9(18)
18 13(1)
43b 18(14)
115b 50(77)
536 202(358)
()
431b 255(108)
70b 34(17)
243 69(92)
604 282(425)
1527 504(1233)
()
1065 425(423)
18 7(6)
52 20(12)
137 40(70)
178 69(85)
110 109(3)
237ab 72(160)
13 7(0.2)
60 24(17)
337 221(59)
742 365(511)
()
490b 318(66)
RESULTS
Total biomass density consistently increased with branch
diameter from the outer to the inner crown. This pattern
was apparent for all individual components except for
lichens, which instead peaked on thin branches of 2
5 cm diameter. Highest biomass density of angiosperms
and DBM was found on branches of 1020 cm diameter
(ravine forest) or on trunks (slope and ridge forest;
Table 1). In relative terms, the contribution of lichens
to total biomass was greatest on twigs 2 cm, bryophytes
peaked on thin branches of 25 cm, angiosperms on
branches of 1020 cm diameter, and DBM on trunks
(Figure 1).
Epiphytic biomass tended to be highest in ridge
forest and lowest in ravine forest and slope forest,
but patterns were variable among substrate classes
with regard to several biomass components. Generally,
greatest differences between forest types were found for
trunks, which showed significantly different biomass
densities of lichens, bryophytes, angiosperms and DBM
(Table 1). Related to high variability, branches only
exhibited statistically significant differences in terms of
DBM (branch diameters 25 and 510 cm) and total
epiphytic biomass (twigs < 2 cm).
In all forest types, total epiphytic biomass and most
of its individual components (except pteridophytes in
slope forest) were closely related to tree size. A linear
model provided a better fit to the relationship of epiphytic
26
F. A. WERNER ET AL.
Figure 1. The relative contribution of individual biomass components (macrolichens, bryophytes, pteridophytes, angiosperms, dead organic matter
(DBM)) to total epiphytic biomass in lower montane forest, south-east Ecuador. Shown are mean SE of three adjacent forest types in ridge, slope
and ravine position. Biomass data for branches is ordered by diameter class, data for trunks are treated as trunks irrespective of diameter. Absolute
values are shown in Table 1.
27
Table 2. Coefficients from linear regression (y = mx) of epiphytic biomass versus tree basal area in three adjacent
montane forest types in south-east Ecuador. All regressions yielded significant relationships (P < 0.001).
Lichens
Ravine forest
Slope forest
Ridge forest
Vascular
plants
Bryophytes
Dead organic
matter
Total biomass
R2
R2
R2
R2
R2
0.72
0.42
0.92
3.1
5.1
7.8
0.81
0.62
0.89
14.2
13.0
21.7
0.71
0.85
0.53
15.3
43.7
75.8
0.52
0.57
0.69
17.2
97.1
67.0
0.71
0.76
0.74
49.8
159
172
by Kurschner
& Parolly (2004) made for closely
corresponding forest types in the same area (3.69.5
mm). While maximum water storage capacities used for
calculations are identical, and tree surface estimates very
similar between the two studies, the bryophyte densities
Table 3. Tree basal area and estimates of epiphytic biomass (kg ha1 ) across three adjacent forest types of south-east Ecuador, based
on the regression slope of epiphytic biomass versus tree basal area (Table 2). Given is the mean SD from six plots; the range of
the 2.597.5% confidence interval of the estimate is added in parentheses. Different superscript letters indicate significant differences
between forest types (ANOVA and Scheffe post hoc test; P < 0.05).
Biomass (kg ha1 )
Basal area (m2
ha1 )
Ravine forest
54.8 a 13.8
Slope forest
39.5 a 6.2
Ridge forest
25.8 b 9
Lichens
Bryophytes
Vascular plants
Total biomass
162 a 43
(117207)
204 a 34
(98309)
200 a 70
(173228)
732 a 193
(569895)
520 a 87
(337703)
560 a 195
(472648)
126 a 33
(355942)
1174 b 9
(9501399)
1422 b 42
(8232021)
888 a 235
(5091267)
3877 b 647
(23675387)
1730 a 603
(12122247)
2570 a 679
(18303310)
6346 b 1059
(47297963)
4446 b 1550
(32655623)
28
Transregional context
Our epiphytic biomass values are within the lower range
of other moist montane tropical sites (Figure 3), showing
that high diversity of epiphytes (Liede & Breckle 2007,
Noske et al. 2008) is not necessarily coupled with high
epiphyte biomass density. Multiple regression analysis of
potential epiphytic biomass predictors available for the
studies compared in Figure 3 (elevation, stand height,
precipitation, an index of aridity (precipitation/potential
evapotranspiration), incidence of fog) did not yield
a significant model (results not shown). Clearly, the
available number of studies from tropical forests remains
too low to untangle a complex set of predictors.
Particularly scarce are data from the Old World, moist
lowland forests, montane forests other than cloud forests,
and seasonally dry woodlands as a whole. Nonetheless,
the data suggest a key role of moisture availability.
Epiphytic biomass at our site was similar to another
study from a montane non-cloud forest (Edwards & Grubb
1977), whereas several forests frequently submersed in
clouds greatly exceeded these values, confirming that
F. A. WERNER ET AL.
Conclusions
Our study shows that three sources of heterogeneity
(branch diameter, tree size, topographic position and
resulting differences in stand structure) strongly affect
quantity and quality of epiphytic biomass in tropical
forests. The significant differences in amount and
composition of epiphytic matter between adjacent forest
types have general implications for resource availability to
other canopy biota, and the cycling of water and nutrients.
Although our study could not differentiate between
direct effects of slope position (nutrient availability,
mesoclimate) and indirect effects (stand structure and
dynamics), it provides evidence that fine-scale topography
needs to be taken into account when extrapolating
epiphytic biomass and related matter fluxes from standlevel data to regional scale.
ACKNOWLEDGEMENTS
We thank Ute Knorr, Daniela Sellbrink and Fabian
Schroder for their excellent help with field and laboratory
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31
Appendix 1.Host trees sampled for epiphytic biomass in three adjacent forest types in montane south-east Ecuador.
Forest type
Species
Family
dbh (cm)
Stratum
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Ravine
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Slope
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Ridge
Melastomataceae
Meliaceae
Bignoniaceae
Euphorbiaceae
Lauraceae
Rubiaceae
Tiliaceae
Cecropiaceae
Euphorbiaceae
Meliaceae
Staphyleaceae
Meliaceae
Sapindaceae
Moraceae
Magnoliaceae
Solanaceae
Mimosaceae
Urticaceae
Cyatheaceae
Rubiaceae
Euphorbiaceae
Alzateaceae
Clusiaceae
Alzateaceae
Myrtaceae
Sapindaceae
Euphorbiaceae
Myrtaceae
Lauraceae
Euphorbiaceae
Lauraceae
Araliaceae
Melastomataceae
Clusiaceae
Symplocaceae
Rubiaceae
Melastomataceae
Rosaceae
Lecythidaceae
Rubiaceae
Melastomataceae
Myrsinaceae
Euphorbiaceae
Clethraceae
Euphorbiaceae
Clethraceae
Melastomataceae
Myrtaceae
Melastomataceae
Podocarpaceae
Clusiaceae
Lauraceae
Podocarpaceae
Melastomataceae
Clusiaceae
Cunoniaceae
Myrtaceae
Alzateaceae
Chloranthaceae
Lauraceae
Cunoniaceae
Cyatheaceae
Aquifoliaceae
64.5
58.3
45.7
45.4
38.2
37.9
37.1
36.1
31.8
28.0
25.6
24.5
22.9
20.8
20.1
14.6
12.4
10.5
5.7
3.0
1.4
41.4
35.7
33.7
24.6
22.0
21.3
19.2
19.1
18.8
16.6
15.0
13.4
12.2
11.6
8.0
6.1
5.1
4.4
2.2
2.0
0.8
31.9
26.4
24.9
22.6
19.8
18.5
17.5
14.4
12.1
11.5
9.9
9.5
8.9
8.6
8.2
7.3
7.0
6.1
3.0
2.5
1.1
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Understorey
Understorey
Understorey
Understorey
Understorey
Understorey
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Understorey
Understorey
Understorey
Understorey
Understorey
Understorey
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Canopy
Understorey
Understorey
Understorey
Understorey
Understorey
Understorey