Managing plantations to promote useful ecological processes and buffer

against drought.
Amy E. Eycott1, Andreas D. Advento2, Sarah H. Luke1, Mohammad Naim2, Jean-Pierre
Caliman2, Edgar C. Turner1
1
Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK. 2 SMART
Research Institute (SMARTRI), Jl. Teuku Umar No.19, Pekanbaru, Riau, Indonesia.

ABSTRACT
Drought sharply reduces oil palm productivity and preliminary data suggest that ecological
functions in oil palm ecosystems become rapidly vulnerable during ENSO-related drought.
With a predicted increase in the variability of strength and frequency of ENSO, the income
and food security of millions of people depend on the oil palm ecosystem’s resilience. As
large-scale oil palm plantations are a relatively recent phenomenon, the effect of ENSO on oil
palm ecosystems is difficult to predict.

Using data from the long-term, large-scale experimental project, the Biodiversity and
Ecosystem Function in Tropical Agriculture Project, we assessed the potential of different
understory management strategies in buffering useful ecosystem processes against the effects
of drought. The key processes we address in this poster are predation (as a means of reducing
herbivory without pesticide) and seed predation. We set out sunflower seeds and mealworm
larvae in stands with different vegetation management, approximately every four months
from May 2016 to August 2017. We used cages and grease (seeds only) to test the role of
vertebrate and invertebrate predators/granivores, and tested predation at both ground and
canopy level. These exclusion and stratum variables had a much stronger effect than either
experimental round or vegetation management. Preliminary analysis does however suggest
that granivory is lower during wetter seasons.

INTRODUCTION
For much of Southeast Asia the El Niño Southern Oscillation (ENSO) causes drought, with
associated increased risks of fire and crop failure. Drought has severe effects on ecosystem
processes and associated services across the land-use gradient. From this point of view, El
Niño is an issue for the livelihoods of all inhabitants of one of the most densely populated
regions of the globe, affecting their food supplies, water and air quality (e.g. Suresh et al.
2013; Paterson et al. 2013; Field et al. 2016).

By far the greatest change in land-use in the Southeast Asia region over the past thirty years
has been the conversion of forest to oil palm plantation (Carlson et al. 2012). This has caused
considerable environmental damage to a region of extremely high biodiversity (Wilcove et al.
2013). Indonesian palm oil production increased twenty-six-fold 1983-2013, while in
Malaysia the increase was six-fold over the same time period (FAOSTAT 2017); the total
area of oil palm plantation in these two countries now exceeds 11.5 million hectares
(FAOSTAT 2017).

Despite the relatively low biodiversity of oil palm plantations compared with other land uses,
e.g. logged forest, oil palm plantations are not biological deserts and a novel ecosystem has
developed with some characteristic features, for example older growth areas are more diverse
(Azhar et al. 2011, Ghazali et al. 2011). Invertebrates in southeast Asian tropical areas are
thought to be living near their thermal optimum (Luke et al. 2017) and so the high
temperatures in oil palm plantations (and under potential climate change) may inhibit
invertebrate diversity and function. Sensitive vegetation management can enhance
biodiversity of non-target groups (e.g. butterflies) or improve landscape permeability for
some species unable to persist in the plantations (Koh 2008), though not for the most
sensitive groups (Yue et al. 2015). There is less information available on the role of
vegetation management in supporting ecological function.

Drought has a negative impact on oil palm yield which can be described using standardised
equations but with considerable variability in actual response (Carr 2011). Drought is also
predicted to have impacts on the abundance of species relevant to key ecosystem functions
and services, such as detritivores and crop pests, and on ecosystem-scale processes such as
carbon cycling, but these key parameters have not been measured in oil-palm systems
exposed to drought – indeed, despite their fundamentally important contribution to oil palm
health and wider ecosystem services they have rarely been measured in oil palm at all
(Dislich et al. 2017).

OBJECTIVES
Our main objective was to test whether changes in ecological function, specifically predation
and granivory, during dry periods could be lessened by allowing greater understorey
complexity. Within this, we aimed to tease apart the roles of different groups (vertebrates vs
invertebrates, canopy vs ground-dwellers).

MATERIALS AND METHODS

Site
The study was carried out in Indonesia, where half of the world’s palm oil is produced
(FAOSTAT 2017). The two main oil palm growing areas in Indonesia are Sumatra and
Kalimantan, of which Sumatra is the drier. The site was two estates in Siak Regency of Riau
Province owned by Pt SMART Tbk: Ujung Tanjung and Kandista. These are estates planted
1987-1995 on mineral soils.
The experimental set-up consists of six sets of plots in triplets, established under the
Biodiversity and Ecosystem Function in Tropical Agriculture (BEFTA) project (Foster et al.,
2014). We manipulated vegetation in 150 x 150 m subplots in two plots of each three: one
where the understory growth is maximized as far as possible (enhanced complexity) using
only manual cutting around the harvesting circle and path, and another where all understory
vegetation is sprayed with herbicides (reduced complexity). As a control, the third plot in
each triplet is treated by standard GAR practice (normal complexity) in which the cicle and
path are sprayed but the inbetween vegetation is allowed to grow. These treatments have been
applied continuously since 2013.

Predation and granivory tests

The basic unit for the predation tests was six mealworms glued onto a piece of oil palm frond
trimmed so that ca. 10 cm of each of six leaflets was visible. We then applied the exclusion
and stratum treatments in factorial combinations: caged and uncaged, canopy and ground.
The cages are rat traps wired closed: metal grid boxes approximately 35 x 20 x 14 cm, with
no holes wider than 1cm. Three sets of the four possible treatment combinations were placed
in each plot, using palms selected by random-number generator.

The basic unit for the granivory test was ten shelled sunflower seeds placed on a paper disc of
approx. 15 cm diameter, covered by a polystyrene disposable plate at approx. 10cm above the
soil surface in order to keep the rain off. For each replicate four treatments were applied: two
of the paper discs had 1cm of thick chassis grease applied round the edge and two were in
cages such that there were cage + grease, cage only, grease only, and open. The tests were
replicated three times in each plot, spaced evenly about 65 m from the centre of the plot.

All samples were placed out in the field for approximately 24 hours before being assessed.

Analysis
Here we present somewhat preliminary analyses, though the data gathering is complete and
we have error-checked 50% of the data, finding an acceptable error rate of <1%. Statistical
analyses were performed in R version 3.4.3 (R Core Team, 2017). The data have been
analysed using mixed effects models and a gaussian error distribution (function glmer in the
lme4 package, Bates et al. 2015), with triplet being used as a random effect, study period,
worm/seed treatment and plot treatment as fixed, factor effects, and starting values take from
simplified models. There was insufficient power to include any interaction terms.

RESULTS
Predation
The vertical stratum (canopy vs. ground) had the strongest effect, with the most predation
occurring at ground level on uncaged baits (Figure 1, n = 1266). Period was also significant,
with the El Niño record (May 2016) having significantly higher predation rates than all other
periods except August 2017. Predation was slightly higher in the normal and reduced plots,
having on average 0.25 more mealworms removed (out of 6) in the reduced plots compared
with the enhanced plots, and 0.35 more in the normal plots (these values are taken from the
regression models, such that they take into account the other variables; see Appendix for
details of parameter estimates).

Figure 1. Boxplots for the mealworms removed after 24 hours. The central bar marks the
median value, the white box shows the interquartile range, the whiskers two standard
deviations from the mean (approximates to a 95% CI) and the spots the outliers. The rows
show the different vegetation treatments and the columns show the different bait treatments.

Granivory
Granivory was only measured from August 2016 to August 2017 (Figure 2, n = 1079). Again,
the bait treatment had the most consistent, significant effect. The caged, grease-barrier
treatment had the lowest seed removal and the open samples the highest. October 2016 and
August 2017 had significantly higher seed removal rates than other months (see Appendix for
details). There was no significant effect of vegetation management.
Figure 2. Boxplots for the seeds removed after 24 hours. The central bar marks the median
value, the white box shows the interquartile range, the whiskers two standard deviations from
the mean (approximates to a 95% CI) and the spots the outliers. The rows show the different
vegetation treatments and the columns show the different bait treatments.

DISCUSSIONS

Ecological function
Both predation and granivory are important ecological functions in the oil palm ecosystem.
Most often, all of the seeds and all of the mealworms had been taken, implying active
predator and granivore communities in all types of stands in all seasons. Ants played a strong
role in removing both sunflower seeds and mealworms, whereas vertebrates were most active
in removing mealworms. This contrasts with the results of Ewers et al. (2015) who used very
similar methods in logged and primary forest in Sabah, Borneo who found vertebrates most
active in removing both mealworms and seeds. We cannot distinguish between birds and
rodents in removing mealworms or seeds, but the lower predation of mealworms in the
canopy than in the ground layer may hint at rodents playing a stronger role.

Implications for plantation management

Our data for mealworms are an approximation for caterpillars, while our sunflower seeds can
be seen as stand-ins for weed seeds. Thus an oil palm plantation with high predation of
mealworms and granivory of sunflower seeds is one where useful consumers are active. The
time period in which the data were gathered had a rather inconsistent effect but there was
high mealworm predation during El Niño, implying that a lack of predators does not
contribute to El Niño-drought related yield losses.

The vegetation management also did not have a consistent effect on predation and granivory.
Enhanced vegetation management slightly reduced the level of mealworm predation, which is
a challenging outcome for proponents of less intensive vegetation management. Enhanced
vegetation may provide concealment for prey, or simply provide a greater abundance of prey
items for the predator population. However, the ‘normal’ practice in the study plantations is
already considerably less intensive than elsewhere, with herbicide only applied around the
palm circle and on the path. We saw no evidence that this practice should not continue.

CONCLUSIONS
The El Niño drought’s negative effects were not caused by a lack of predators for the insect
herbivores in oil palm plantation, but may have reduced other ecological functions such as
granivory. Invertebrates and vertebrates play slightly different roles in plantations with
vertebrates more focussed on predation. Current best-practice vegetation management
provides a ‘happy balance’ between predators and their invertebrate prey, but does not appear
to mitigate the effects of the El Niño drought.

ACKNOWLEDGEMENTS
This research was supported by the UK Natural Environment Research Council. We thank
the Ministry of Research, Technology and Higher Education of the Republic of Indonesia for
permission for A Eycott, S Luke and E Turner to work in Indonesia. We thank all the
SMARTRI staff who have assisted this research in the field and the BEFTA project in
general.

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APPENDIX: Parameter estimates for statistical model outputs

Mealworms. Note that the model was according to mealworms remaining, such that a
negative value for the parameter estimate means higher predation.

Estimate Std. Error t value Pr(>|z|)

(Intercept) 0.09684 0.16851 0.575 0.565514
wormtreatRemain_base_nocage -0.26278 0.10125 -2.595 0.009450 **
wormtreatRemain_top_cage 0.25406 0.07933 3.202 0.001363 **
wormtreatRemain_top_nocage 0.02467 0.08680 0.284 0.776220
Treatmentnormal -0.37056 0.07571 -4.895 9.85e-07 ***
Treatmentreduced -0.25828 0.07169 -3.603 0.000315 ***
Period2016_07 0.89014 0.13533 6.578 4.78e-11 ***
Period2016_10 0.36217 0.15182 2.385 0.017057 *
Period2017_02 0.70180 0.13952 5.030 4.90e-07 ***
Period2017_05 0.46018 0.14793 3.111 0.001866 **
Period2017_08 0.05435 0.17092 0.318 0.750502
Seeds. Note that the model was according to seeds remaining, such that a negative value for
the parameter estimate means higher predation.

Estimate Std. Error t value Pr(>|z|)

(Intercept) 0.99173 0.10270 9.656 < 2e-16 ***
seedstreatremain_cage_grease 0.96165 0.09418 10.211 < 2e-16 ***
seedstreatremain_open -0.11687 0.13218 -0.884 0.376600
seedstreatremain_open_grease 0.76014 0.09714 7.825 5.07e-15 ***
Treatmentnormal -0.05919 0.05930 -0.998 0.318204
Treatmentreduced -0.03067 0.05852 -0.524 0.600193
Period2016_10 -0.27088 0.08140 -3.328 0.000876 ***
Period2017_02 0.04877 0.06806 0.717 0.473630
Period2017_05 0.09633 0.06667 1.445 0.148455
Period2017_08 -0.69706 0.11023 -6.324 2.55e-10 ***