Discussion
Here, for the first time we quantitatively explored energy fluxes of
canopy arthropod communities of tropical rainforest transformation
systems. Conversion of rainforest into plantations drastically altered
abundance, biomass and trophic structure of canopy arthropods, resulting
not only in substantially decreased energy fluxes, but also in shifts in
the relative importance of ecological functions such as
algae-microbivory, herbivory and predation. The observed shifts may have
far-reaching consequences for ecosystem functioning and underline the
importance to counteract the rapidly accelerating land-use changes in
tropical regions.
Total abundance and biomass of canopy arthropods strongly decreased from
rainforest and jungle rubber towards monoculture plantation systems of
rubber and oil palm, as has been shown previously for ants, spiders and
parasitoid wasps (Nazarreta et al. 2020; Azhar et al.2022; Ramos et al. 2022). The decrease of combined average
arthropod abundance across 12 major taxa by ca. 70 % from rainforest to
monoculture plantations of rubber and oil palm was even more severe than
reported for the abundance of soil invertebrates/arthropods at the same
study sites of ca. 60 % (Potapov et al. 2019a), suggesting more
pronounced effects of land-use changes on aboveground compared to
belowground invertebrates, as has been shown for temperate ecosystems
(Le Provost et al. 2021). Notably, differences in biomass of
canopy arthropods varied between the two landscapes studied, with
generally higher abundance and biomass in rainforests of Bukit Duabelas
than in Harapan. This was mainly due to high biomasses of large
herbivorous/algae-microbivorous Orthoptera and Blattodea in the former
and resulted in a more drastic decrease in biomass of up to 87 % from
rainforests to plantations in the Bukit Duabelas than the Harapan
landscape (ca. 70 %). The regional differences are presumably due to
differences in fertility and landscape heterogeneity, but in particular
the longer history of rainforest transformation in the Harapan than the
Bukit Duabelas landscape (Allen et al. 2015; Harrison &
Swinfield 2015; Guillaume et al. 2018; Sibhatu et al.2022). By contrast, rubber and oil palm plantations featured similarly
low abundance and biomass of canopy arthropods in both regions,
indicating that regional differences are levelled out by strong
disturbance such as the conversion of rainforest into plantation
systems. This highlights the importance of protecting intact tropical
ecosystems at landscape scale.
Taxonomic groups responded differentially to land-use changes. The
abundance and biomass of most arthropod groups decreased strongly from
rainforest towards plantation systems; loss of Collembola abundance was
most pronounced, with a loss of > 85 % from rainforest and
jungle rubber to oil palm plantations. Abundance of Formicidae was also
reduced by ca. 75 % from rainforest to plantations and biomass of
Blattodea even decreased by > 90 %. The strong reduction
in abundance and biomass of these taxa may be related to reduced habitat
complexity, aboveground plant biomass and diversity, and available food
sources (Novotny et al. 2006; Kotowska et al. 2015;
Drescher et al. 2016; Zemp et al. 2019). On the other
hand, abundance and biomass of some herbivorous taxa, such as
Lepidoptera and Curculionidae, were not reduced in oil palm plantations.
This is likely due to specialized herbivore species that thrive in oil
palm plantations, such as red palm weevils, bagworms and nettle
caterpillars, and to the introduced curculionid pollinatorElaeidobius kamerunicus , which is the dominating curculionid
species in oil palm plantations in our study region (Greathead 1983;
Kasmiatun et al. 2022).
Land-use changes also altered the trophic structure of canopy arthropod
communities. Biomass-weighted mean of trophic positions as indicated by
Δ15N values were significantly higher in rubber
plantations, indicating a higher proportion of predators. Low minimum
Δ15N values, with δ15N values being
in some cases more than 6 ‰ below those of canopy leaves, suggest that
some canopy arthropod taxa, such as Psocoptera, Collembola and
Blattodea, predominantly feed on algae or lichens which utilize
atmospheric nitrogen and typically are depleted in
δ15N compared to vascular plants (Chahartaghi et
al. 2005; Erdmann et al. 2007; Maraun et al. 2011).
Δ15N values of omnivores such as Hemiptera and
Formicidae, but also of higher trophic level taxa such as Diptera,
Staphylinidae and Araneae, were remarkably constant across land-use
systems. This suggests that, despite high diversity within taxonomic
groups (Basset 2001; Nazarreta et al. 2020; Ramos et al.2022), overall trophic niches and therefore ecological functions of
these supra-specific taxa bear phylogenetic signal, which was also
postulated for belowground systems (Potapov et al. 2019b). In
contrast to the relatively low Δ13C values in
plantation systems, in rainforest and jungle rubber canopy arthropods
were on average 5-6 ‰ enriched in 13C compared to
canopy leaves as potential basal resource; Δ13C maxima
in rainforest were even close to 9 ‰ above those of leaves. Part of the13C enrichment may be attributed to variations in13C signatures between leaves high and low in the
canopy, with the latter used for calibration in this study (van der
Merwe & Medina 1991; Hyodo et al. 2010). An additional cause may
be selective utilization of only specific plant/leaf components, such as
water-soluble amino acids and carbohydrates that are more easily
accessible to digestion and are typically enriched in13C compared to bulk tissue of leaves. Tropical leaves
feature high amounts of structural and hard-to-digest compounds, such as
lignin and cuticular waxes, that are more depleted in13C than other less condensed carbon compounds
(Pollierer et al. 2009). Given the diversity of herbivore feeding
strategies, including leaf chewing and mining, fruit eating as well as
xylem/phloem sucking (Novotny et al. 2010), selective utilization
of specific components is likely.
Despite relatively constant trophic levels of taxonomic groups, the
biomass distribution among trophic levels, as indicated by
Δ15N classes, differed significantly between land-use
systems, but this also varied between landscapes. The shift from a
close-to-normal biomass distribution in rainforests, in particular in
Bukit Duabelas, to more uneven distributions in oil palm and rubber,
suggests that, in line with our first hypothesis, land-use
intensification decreases trophic redundancy and causes a more scattered
distribution of trophic niches, possibly mitigated by reduced resource
diversity (Krause et al. 2020). Low trophic redundancy may
increase the vulnerability to the loss of trophic functions and to
extinction cascades in intensively managed land-use systems (Sanderset al. 2018).
In line with our second hypothesis, energy fluxes were remarkably
reduced by rainforest conversion into plantations. Total energy fluxes
were reduced by up to 75 % in rubber and oil palm plantations compared
to rainforest, and reduced by > 30 % compared to jungle
rubber, mirroring the reductions in biomass. As energy fluxes can be
used to infer ecosystem multifunctionality and stability (Barneset al. 2018; Manning et al. 2018; Potapov 2022), the
strong reduction in energy fluxes in plantation systems points to the
loss of ecosystem functions and potentially to the deterioration of
ecosystem stability. Significantly lower total energy fluxes in
plantations compared to rainforests contrast findings from soil food
webs at our study sites, where the presence of earthworms as large
detritivores in plantations counterbalanced declined energy fluxes in
other trophic groups (Potapov et al. 2019a). However, energy
fluxes to canopy arthropods were not only just reduced, but shifted
among different trophic groups, such as herbivores, algae-microbivores
and predators, representing different ecosystem functions. Importantly,
shifts in energy fluxes and respective functions were similar, but not
congruent with shifts in biomass among trophic groups. This highlights
that energy flux approaches go beyond biomass-based approaches by also
considering metabolic rates and assimilation efficiencies of consumers,
as well as trophic structure and preferred prey, thereby more
realistically reflecting community functioning.
In rainforests, algae-microbivory was the most important feeding
strategy, followed by herbivory, while both of these feeding types were
equally important in jungle rubber. Such high energy fluxes to
algae-microbivores have not been demonstrated before for canopy
arthropods and suggest that tropical canopy food webs more heavily rely
on resources other than higher plants, with algae and microorganisms
playing an even greater role than tissue of higher plants such as
leaves. In contrast to vascular plant epiphytes, microbiota in tropical
forest canopies are not well-studied (Nakamura et al. 2017).
Microbial communities differ strongly with vertical stratification in
tropical forests and are responsible for decomposition of suspended
detrital substrates (Gora et al. 2019). Fungi, algae and lichens
can significantly contribute to the diet of leaf litter and
bark-inhabiting Oribatida and Collembola (Chahartaghi et al.2005; Erdmann et al. 2007; Susanti et al. 2019).
Potentially, due to the low resource quality and high lignin and wax
contents of leaves of tropical trees, these resources are of particular
relevance for arthropods in the canopy of tropical rainforests. This
calls for further studies to disentangle microbial contributions from
fungi, bacteria and algae to the diet of canopy arthropods and how they
are influenced by land-use change.
While rainforest and jungle rubber were characterized by pronounced
energy fluxes to algae-microbivores and herbivores, predation was the
main feeding type in rubber. Food webs with pronounced energy fluxes to
lower trophic levels, i.e. bottom heavy food webs, as in rainforest and
jungle rubber, are assumed to be more stable than those with higher
fluxes to high trophic levels (Rip & McCann 2011; Barnes et al.2018). The strong reduction in energy fluxes to lower trophic levels and
the concomitant shift to fluxes at higher trophic levels in rubber
plantations are likely related to the conversion from evergreen to
deciduous forest, causing temporal gaps in resource availability for
herbivores and, due to faster replacement of leaves, lower
algae-microbial colonization. As more energy is required to support high
trophic levels, there is potentially an overall faster transfer and
higher loss of energy along food chains in rubber plantations. This
faster transfer may contribute to higher carbon and nutrient losses in
rubber plantations (De Ruiter et al. 1993; Barnes et al.2018; Guillaume et al. 2018). On the other hand, a significantly
higher ratio of herbivory compared to predation, as in oil palm
plantations, may indicate reduced pest control and concomitantly higher
losses of oil palm tissue to herbivore pests, necessitating higher use
of pesticides (Corley & Tinker 2015).
Here, for the first time we documented the dramatic impacts of tropical
land-use change on abundance, biomass, trophic structure and functioning
of canopy arthropod communities. We showed that the conversion of
rainforest into rubber and oil palm plantations not only strongly
reduces energy fluxes, but also alters ecological functions, shifting
from stable systems with high energy fluxes at lower trophic levels and
high trophic redundancy in rainforest to more contrasting trophic niches
in plantation systems. While oil palm plantations were characterized by
a high ratio of herbivory to predation suggesting reduced pest control,
predation was dominant in rubber plantations, providing the risk of
higher energy and nutrient losses. Together, our findings indicate that
the conversion of rainforest into plantation systems compromises
ecosystem multifunctionality and stability, and suggest high sensitivity
of rainforests to even low levels of disturbance such as selective
logging. A combined food web approach, not only considering changes in
abundance and biomass, but also in trophic structure and energy fluxes
is promising to comprehensively trace changes in ecological functions
due to land-use change and may provide a reliable basis to foster
informed management decisions.