Drivers of elephant browsing damage on Acacia drepanolobium trees within the Mpala
CTFS- ForestGEO plot
Introduction
Savanna ecosystems cover a fifth of the earth’s land surface (Sankaran et al., 2005) and they host
a great diversity of both domestic and wild ungulates (Riginos et al., 2012, Reid, 2012). The
structure and function of savannas, including their ability support livestock production and wildlife
conservation (Reid, 2012, Du Toit and Cumming, 1999), nutrient and hydrological cycles (Padien
and Lajtha, 1992, Schlesinger et al., 1996, Joffre and Rambal, 1993), and carbon storage
(Kundhlande et al., 2000), is firmly hinged in a fine balance between tree and grass cover. While
encroachment of woody vegetation has become a primary conservation concern in some savannas
(Scholes and Archer, 1997, Angassa and Baars, 2000, van Auken, 2000), the converse is true in
others (O’connor et al., 2007). Understanding the drivers of vegetation dynamics is a primary goal
of ecologists and managers interested in maintaining the optimum balance between grass and tree
cover.
Herbivory is one of the major drivers that regulate tree cover in savanna ecosystems (Holdo et al.,
2013). Elephants, in particular cause significant reduction in tree density and cover (Kalwij et al.,
2010, Jacobs and Biggs, 2002, Barnes et al., 1994, Skarpe et al., 2004, Boundja and Midgley, 2010,
Birkett, 2002, Wahungu et al., 2011, O’connor et al., 2007), but their browsing intesity at the level
of individual trees may vary depending on how well the tree is defended against herbivory and the
level of nutritional rewards they obtain from feeding on individial trees.
One of the ways plants have been able to minimise browsing pressure is through evolution of insect
mutualism, where insect derive benefits such as shelter and nourishments from the host plants. In
exchange, the nsects protect the host tree against herbivores. Such insect-plant associations are
rampant in most ecosystems, and include a well studied relationship between ants and Acacia
drepanolobium trees in East Africa.
Acacia drepanolobium, a widely distributed tree in East African savanna ecosystems, forms nearly
mono-dominant stands in most clay-rich vertisols. While this tree has spines that could potentially
limit browsing pressure by many harbivore species in the region, these spines are not effective
deterents against elephant browsing (Goheen and Palmer, 2010). However, Acacia
drepanaolobium trees have evolved a highly specialised mutualistic relationship with ants that
deffend the trees against most herbvores, elephant included (Palmer et al., 2010). The trees grow
swollen thorn domatia that host exclusive colonies of four symbiotic ant species (Crematogaster
memosae, C. nigriceps, C. sjostedti, and Tetraponera penzigii). The ant colonies benefit from
shelter in the domatia and nourishment through nectar produced from extrafloral nectaries. In
exchange, they defend the tree against herbivores. However, there exists fundamental differences
in the level of defence provided by these four ant species, with C. memosae and C. nigriceps being
the most defensive and C. sjostedti and T. penzigii offering minimal defense. These differences in
defensive abilities of the ants may have imporatant implications on the level of elephant browse
damage on individual trees.
In addition, the level of browsing may also vary depending on the nutrient levels in individual
trees. Plant chemistry has strong influence on the diet selection by herbivores. Herbivores rely on
sensory perception to select food items with the required level of specific nutrient elements or to
avoid items that are chemically defended. As such, chemical cues produced by individual plants
could serve as attractants or repellants to herbivores. Although most studies relating plant
chemistry to herbivory tend to focus on differences across plants species, there exists important
intraspecific differences, even among plants growing in similar microenvironment, which could
influence the intensity of browsing.
In this study, we examine how ant mutualists interact with nutrient levels in individual trees to
influence elephant browsing in Acacia drepanolobioum trees. This is the first study examining the
interaction between these two drivers.
Materials and methods
Study site
This study was conducted at Mpala Research Centre (0o17`N, 37o52`E), located on the leeward
side of Mt. Kenya at an altitude of 1800m above sea level. The area receives a weakly trimodal
rainfall of 400-800mm annually, with a distinct dry season in December to March. Wild mesoherbivore species in the region include plains zebra (Equus burchelli), Grevy's zebra (Equus
grevyi) hartebeest (Alcelaphus buselaphus), oryx (Oryx beisa), buffalo (Syncerus caffer),
steinbuck (Raphicerus campestris), eland (Taurotragus oryx), and Grant’s gazelle (Gazella
granti). There are only two megaherbivores, giraffe (Giraffa camelopardalis), and elephant
(Loxodonta africana), of which elephants have the largest impact on trees (Kalwij et al., 2010,
Jacobs and Biggs, 2002, Barnes et al., 1994, Skarpe et al., 2004, Boundja and Midgley, 2010,
Birkett, 2002, Wahungu et al., 2011). Cattle are the primary livestock in the study area. Other
livestock species in the area include camels, sheep, goats and donkeys. Two main soil types exist
in the region; the red soil (oxisols) and the black cotton soils (vertisols). The focus for this study
was on the black cotton soil region. This region constitutes a third of total area under by the
Mpala CTFS-SIGEO plot and is dominated by A. drepanolobuim trees (constitute over 95% of
the overstorey plant community).
Data collection
We searched for trees with fresh (one day old) elephant browse damage within the study site. For
each of the browsed trees, we selected the nearest tree with similar height and crown structure, or
similar diameter. For both the browsed and unbrowsed trees, we measured the tree height and
diameter at 15cm, identified the resident ant species and estimated their colony density, and
collected 20 grams of bark and leaf samples for nutrient analyses.
The four symbiotic ant species in the study area can be easily distinguished by their color and body
size. To obtain an index of colony density, we gently tapped the tree and counted the number of
ants swarming, on four preselected 15 cm shoots, within 10 seconds.
To compare the nutrient quality of browsed and unbrowsed trees, we analyzed both leaf and bark
tissue samples the following nutrient elements; crude protein (CP), Phosphorus (P), Potassium
(K), Calcium (Ca), Magnesium (Mg), Sodium (Na), Iron (Fe), Manganese (Mn), Zinc (Zn) and
Copper (Cu). We also determined acid detergent fiber (ADF) in the leaf and bark tissues. For each
tree, approximately 20 grams of the bark was stripped from the base of the trees. Also, 20 grams
of fresh growth leaves were clipped from each tree. The tissue samples were air dried to constant
weight then ground separately. We used wet chemistry technique to analyze the proportions the
various micronutrients.
For the browsed trees, we recorded the details and extent of elephant damage, including (i) the
nature of damage i.e. broken branch or stem, bark stripped, pushed over or uprooted, and (ii) the
relative proportion of the part of the tree that is actually browsed (in a scale of 0 to 5; where 0= no
damage; 1= branch tips browsed; 2=branches browsed and broken; 3=20-50% canopy destruction;
4= more than 50% canopy destruction; 5=tree completely pushed over or 100% canopy
destruction)
Data analyses
The total number of ants swarming in each of the four-15m branches per tree was summed to
obtain an index of colony density per tree. A relative proportion of elephant browse damage per
tree was obtained by converting the damage scores to midpoints of their corresponding percentage
damage class. The content per sample of various nutrient elements was expressed as percentage of
the total dry weight. Both the proportion of elephant browse damage and the content of various
nutrient elements were arcsine transformed to convert them from binomial distribution to normal
distribution for valid application of parametric statistics. We used one-way ANOVA to test for
differences in level of browse as a function of ant species occupancy and colony density. We fit
linear models to test for the relationship between the proportion of elephant browse damage and
the level of various nutrient elements. We used Factorial ANOVA to test for the interactive effect
of ant species, colony density, and level of various nutrient element on the proportion of elephant
browse damage on individual trees.
Results
We sampled a total of 353 trees, 46% of which were occurred in the CTFS plot while the rest
were located adjacent to the plot. Majority of the trees sampled were occupied by either C.
sjostedi (37%), C. mimosa (32%) or T. penzigii (12%), with only a few trees being occupied by
C. nigriceps (1%) and 18% having no ants (Figure 1). Ant occupancy depended on the height of
individual trees (χ2 = 13.39, p= 0.04). Generally T. penzigii occupied short trees while C.
nigriceps occupied intermediate height classes and C. sjostedti occupied tall trees (especially
those with cavities on the stem). However, C. mimosae occupied trees in all height classes.
The average number of ants swarming on a 60m branch (an index of colony density) varied
significantly across ant species. The response was highest among C. mimosae ants, followed by
C. nigrceps, T. penzigi and lowest among C. sjostedti ants (Figure 2).
Figure 1: Number of trees occupied
by different ant species
Figure 2: Index of colony density in each of
the four ant species
The intensity of elephant browse damage varied significantly with ant occupancy (F=5.13;
p=0.002) and height of the tree (F=31.94; p<0.001), but not with colony density (F=0.89,
p=0.35). Trees having no ants experienced the highest damage and those occupied by T. penzigi
experienced the least damage (Figure 3). Generally tall trees were more vulnerable than shorter
trees (Figure 4).
Figure 3: variation in intensity of elephant
browse damage as a function of ant occupancy
Figure 4: Elephant browse damage per tree height class
Concentration of most mineral elements (K, N, P, Mn, Cu, Zn, and Fe) was higher in leaves than
in the bark tissues (Figure 5). Polyphenols, NDF, Ca and Na were higher in bark samples than
leaf samples (Figure 5).
Figure 4: Differences in proportion of various nutrient elements between leaf and bark tissue
samples
The intensity of elephant damage varied depending on the concentration of various mineral
elements in leaves, and the ant species occupying the tree. After controlling for differences in
colony densities, the level of elephant browse damage was negatively correlated with level of
polyphenols and NDF on leaf samples. For polyphenols, this negative relationship was also
dependent on the resident ant species (Table 1). Depending on the ant species, elephants browsed
more on trees with greater concentrations of iron (Fe), Magnesium (Mg) and crude nitrogen (N),
(Table 1). The level of elephant browse damage was also positively influenced by the
concentration of phosphorus (P), sodium (Na), potassium (K), and zinc (Zn), but [unlike iron
(Fe), Magnesium (Mg) and crude nitrogen (N)] the strength of this relationship did not vary
depending on the ant species occupying the tree (non-significant interaction; Table 1).
Table 1: general linear model for the effect of ant species, ant colony density, and the level of
various nutrient elements (content) in individual trees.
Element
Ca
Cu
Fe
K
Mg
Mn
N
Na
NDF
P
Polyphenols
Zn
Source of Variation
ant species
ant density
content
ant species*content
ant species
ant density
content
ant species*content
ant species
ant density
content
ant species*content
ant species
ant density
content
ant species*content
ant species
ant density
content
ant species*content
ant species
ant density
content
ant species*content
ant species
ant density
content
ant species*content
ant species
ant density
content
ant species*content
ant species
ant density
content
ant species*content
ant species
ant density
content
ant species*content
ant species
ant density
content
ant species*content
ant species
ant density
content
ant species*content
DF
2
1
1
2
2
1
1
2
2
1
1
2
2
1
1
2
2
1
1
2
2
1
1
2
2
1
1
2
2
1
1
2
2
1
1
2
2
1
1
2
2
1
1
2
2
1
1
2
SS
127.44
6.82
61.68
150.85
119.43
67.67
54.77
193.03
110.26
84.70
206.63
225.82
42.24
42.55
174.73
129.10
159.75
89.63
83.20
208.61
161.13
77.57
143.85
136.89
143.04
81.04
210.20
228.94
153.99
35.32
104.37
151.86
137.24
62.21
2.65
216.56
55.13
81.03
179.10
167.87
217.97
126.63
143.13
282.01
49.53
65.37
134.12
163.57
F
2.57
0.27
2.48
3.04
2.08
2.35
1.91
3.36
2.74
4.21
10.28
5.61
0.72
1.44
5.92
2.19
3.08
3.46
3.21
4.02
2.54
2.44
4.53
2.16
3.12
3.54
9.18
5.00
3.45
1.58
4.67
3.40
2.54
2.30
0.10
4.01
1.22
3.58
7.92
3.71
5.17
6.01
6.79
6.69
0.81
2.15
4.41
2.69
P
0.12
0.61
0.14
0.09
0.17
0.15
0.19
0.07
0.11
0.06
0.01
0.02
0.51
0.26
0.03
0.16
0.09
0.09
0.10
0.04
0.12
0.15
0.06
0.16
0.08
0.09
0.01
0.03
0.07
0.23
0.04
0.07
0.12
0.16
0.76
0.04
0.33
0.08
0.02
0.06
0.03
0.03
0.02
0.01
0.47
0.17
0.06
0.11
Conclusion and recommendations
This pilot study explored factors that influence the intensity of browse damage on Acacia
drepanolobium trees, a keystone plants species in most ‘black cotton’ soil ecosystems in East
Africa. Consistent with previous studies, this study found strong influence of ant mutualists of
herbivory in Acacia drepanolobium trees. In addition, we report on the influence of plant
chemistry on the level of browse damage on Acacia drepanolobium and explore potential
interactions with insect mutualists. This information is critical in understanding drivers of
vegetation structure and dynamics in savanna ecosystems. However, inferences from this study
are to some extent constrained by the small sample size. For example, we did not have sufficient
replicates for trees occupied by T. penzigii and C. nigriceps. To gain better understanding of the
strength of various drivers of elephant browsing on Acacia drepanolobium, we recommend a
more extensive survey involving more replicates.
Acknowledgements
This work would not have been accomplished without support from the Smithsonian Tropical
Research Institute through the Center for Tropical Forest Science (CTFS) grant. I am indebted to
Godfrey Amoni, Mathew Lokidongoi, John Luchukiya, Fredrich Erii, and Jackson Ekadeli for
their invaluable help with field work. Much thanks to Nicholas Kungu for help with laboratory
analyses. Thanks to Staline Kibet and the CTFS proposal review panel for their constrictive
review and suggestions towards improving this work.
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