Interactive effects of drought and deforestation on multitrophic communities and aquatic ecosystem functions in the Neotropics—a test using tank bromeliads

Introduction

Decades of overharvesting, habitat destruction, biological invasions, ecosystem contamination and emission of greenhouse gases have led to the degradation of ecosystems worldwide (Maxwell et al., 2016; Urban et al., 2016). In particular, it is broadly acknowledged that habitat modification and climate change are among the greatest threats to biodiversity and ecosystem functions (Rice et al., 2018), and that the two phenomena are mutually reinforcing (Brook, Sodhi & Bradshaw, 2008; Lorenzen et al., 2011). The local to global components of environmental change (e.g., deforestation, precipitation change) are often studied in isolation (e.g., Bennett et al., 2019; Foden et al., 2019; Magioli et al., 2019; Nowakowski et al., 2017) though there is growing evidence of complex interactive effects between the various drivers of biodiversity decline (Murdoch, Mantyka-Pringle & Sharma, 2020; Oliver & Morecroft, 2014; Staudt et al., 2013). In most cases, the combined effects of multiple stressors on any given environmental variable are not simply additive and can result in an “ecological surprise” (Fong, Bittick & Fong, 2018; Paine, Tegner & Johnson, 1998). The interactive effects of stressors can be either greater (synergistic) or weaker (antagonistic) than the simple sum (additive) of the effects induced by individual stressors (Côté, Darling & Brown, 2016; Orr et al., 2020; Piggott, Townsend & Matthaei, 2015). To date, this question has been essentially examined in temperate regions of the northern hemisphere, leaving tropical regions overlooked (Oliver & Morecroft, 2014; Tyukavina et al., 2017). Paradoxically, tropical ecosystems could lose more species than their temperate counterparts, first because they contain a disproportionate number of the world’s species (Barlow et al., 2018), and second, because tropical species often have narrower physiological tolerances for climatic variation (Tewksbury, Huey & Deutsch, 2008).

Freshwaters are the most endangered ecosystems of the World (Jenkins, 2003). Threats include human activities that have local to regional impacts, to which global-scale stressors are superimposed (Dudgeon et al., 2006). These issues are particularly concerning in Neotropical regions where, together with increasing rates of deforestation and land conversion (Ríos-Touma & Ramírez, 2019; Schielein & Börner, 2018), the intensification of dry seasons is expected to exacerbate extinctions by reducing water availability (Seneviratne et al., 2021). On one hand, deforestation opens the canopy thus modifying food availability and increasing incident light in freshwater ecosystems. Under these circumstances, we expect algae to grow and proportions of invertebrate shredders should fall due to lower inputs of coarse detritus biomass (Barlow et al., 2018; Brito et al., 2020; Silva-Araújo et al., 2020). Thus, either grazer-scraper and collector taxa should dominate the invertebrate biomass (Brouard et al., 2012). On the other hand, different functional groups or biotic compartments could respond differently to drought-induced stress (Srivastava et al., 2020), leading to reconfigurations of the multitrophic communities. Owing to their larger body size and energetic demands, macro-organisms should notably show stronger responses, compared to the microorganisms (Vilmi et al., 2020). Finally, if the nature of the interaction between deforestation and drought (i.e., additive vs synergistic) and the subsequent effects on ecosystem functions remain to be specified, the interactive effects should be much stronger than the pure effects of each disturbance type in isolation. Indeed, food web-mediated effects due to deforestation such as the loss of entire functional groups (e.g., leaf shredders) will alter processing chains and species interactions, further weakening ecosystems in the face drought. Understanding the impacts of local and global disturbance, and perhaps more importantly their interactive effects on the structure of multitrophic aquatic communities is therefore an important step towards predicting the ecosystem-level consequences of environmental changes in the Neotropics.

Whilst experiments are widely used to test specific hypotheses regarding the effects of environmental change, emulating effects of local (e.g., deforestation) and global stressors (e.g., precipitation change) at the whole-community and/or -ecosystem level in natural environments is challenging. For instance, drought cannot be manipulated at the extent of large macrocosms, and natural ecosystems are usually too diverse in size or shape to form actual replicates. Natural microcosms such as plant-held waters and their aquatic communities are relevant model system to test ecological hypotheses in experimental research (Srivastava et al., 2004). Native to the Neotropics, the Bromeliaceae family comprises more than 3,700 species of flowering plant, half of them being tank-forming bromeliads (Givnish et al., 2014). Tank bromeliads have leaves arranged in rosettes that collect rainwater (up to several litres) and litter from overhanging trees. These tanks are a suitable habitat for specialized aquatic organisms ranging from prokaryotes to predatory invertebrates, assembled in multi-trophic communities (Brouard et al., 2012). Tank bromeliads are highly replicated in nature and span a broad range of environments. Because they can be easily transplanted (the roots primarily have and anchoring role), can be exhaustively sampled, and host co-evolved species, tank bromeliads were deemed relevant systems to test the effects of multiple stressors at ecosystem level in manipulative experiments conducted in nature (Céréghino et al., 2022; Romero et al., 2020; Srivastava et al., 2020; Trzcinski et al., 2016).

In this study, we used the tank bromeliad ecosystem to tease out the pure and interactive effects of deforestation and drought on freshwater food webs and ecosystem functions in Neotropical environments. Specifically, we used cross-habitat transplantation and rainout shelters to examine how emulated canopy trimming and drought, and their interaction, affect the various functional components of aquatic communities, and subsequently, ecosystem functions. We used detrital decomposition, a key ecosystem process in nutrient and carbon cycling, as a proxy of ecosystem functioning (Benfield, Fritz & Tiegs, 2017; Gessner et al., 2010). We tested three hypotheses. First, if understorey environments determine the main energy pathways in aquatic ecosystems (Brouard et al., 2012; Neres-Lima et al., 2017), then deforestation alone should primarily impact the “brown”, benthic to pelagic energy pathway (Lorion & Kennedy, 2009). More specifically, we predicted a decline in the overall biomass of detritivores, including macro- and micro-organisms that breakdown coarse particulate organic matter (CPOM), and those that process the resulting fine particulate organic matter (FPOM). As a result, we’d expect decomposition to be adversely affected by deforestation (Silva-Junior et al., 2014). Second, if water shrinkage selects against organisms with a large body size and higher energetic demand (Ledger et al., 2013; Ruiz et al., 2022) and/or with a pelagic life style (Aspin et al., 2019), then drought alone should cause a decline in predator biomass while favouring benthic detritivores. Subsequently, predation release could foster detritivore activity and, therefore, drought could indirectly increase detrital decomposition (Amundrud & Srivastava, 2016). Third, if deforestation and drought disassemble food webs both from the bottom and from the top (see above predictions), then we expect their interactive effects to be much stronger than the sum of their pure effects because the disruption of trophic interactions and processing chains will prevent shifts to alternative states and cause a collapse of communities and ecosystem functions.

Materials and Methods

Experimental set up

We tested the pure and interactive effects of deforestation and drought, including sequential and simultaneous effects, on functional community structure and leaf litter decomposition. Prior to the experiment, we selected 50 and 20 mature A. aquilega that naturally grew in the forest and open area, respectively, to end up with ten replicates per treatment (see below). All plants had similar vegetative traits (number of leaves = 13 ± 3, plant diameter = 107.9 ± 38.21 cm, water holding capacity), to avoid habitat-size effects on community diversity (Petermann et al., 2015). These plants were never used in any experiment before. The experiment started with the pure effect of deforestation. First, twenty bromeliads of the forested area were transplanted to the open area to emulate a deforestation event. Two enclosures (one fine- and one coarse-mesh enclosure) were immersed in an intermediate well of each of the 70 plants. After 105 days, we subjected bromeliads to a drought event of 65 days, which corresponds to the most extreme event recorded in the area over the past 20 years. To emulate drought, we placed transparent rainshelters 1 m above the plants. These rainshelters prevent natural water inputs without affecting macroinvertebrate colonisation or increasing air temperature (Marino et al., 2017). Ten of the transplanted bromeliads (sequential effect), 10 bromeliads in the forest as well as ten bromeliads in the open area were exposed to the drought event starting at day 105. An additional set of ten bromeliads were transplanted from the forest to the open area and directly exposed to drought (simultaneous effect). Finally, 10 unmanipulated plants in the forest and in the open area were used as controls. The percentages of total incident radiation above the bromeliads (IR) were calculated using hemispherical photographs and an image processing software (Gap Light Analyzer 2.0) as described in Leroy et al. (2009). In total, the experiment comprised seven treatments with ten replicates each (Fig. 1): forest control (T1), deforestation (T2), drought in the forest (T3), deforestation followed by drought (T4), deforestation and drought simultaneously (T5), open area control (T6), and drought in the open area (T7). Interactive effects were tested both sequentially (T4) and simultaneously (T5) to further examine whether a recovery time between two disturbances affects the extent ecosystem responses (Gunderson, Armstrong & Stillman, 2016).

Results

Effects of deforestation and drought on habitat conditions

Control bromeliads from the forest held significantly less water, compared to control bromeliads from the open area (pairwise post-hoc tests; p < 0.0001) (Fig. 2, Table S1). In the forest, drought significantly reduced the water volume (WV) held by bromeliads (mean ± SE values: control forest = 512 ± 99 mL, drought = 48 ± 16 mL; p < 0.0001). The transplantation of forest bromeliads to the open area (“deforestation”) did not significantly alter WV (deforestation group = 562 ± 64 mL, p > 0.0500). However, the combination of drought and deforestation dried out almost all transplanted bromeliads (WV = 0 mL in each bromeliad, except for one plant subjected to simultaneous disturbances), so there was highly significant difference in pairwise comparisons testing combined disturbances vs control or vs drought alone in the forest (p < 0.0001 for all). In the open area, WV was significantly reduced by drought (control open = 1,490 ± 242 mL, drought = 149 ± 45 mL; p < 0.0001). The mean incident radiation was 58 ± 4% in the open area, significantly higher than that recorded in the forest (19 ± 1%; p < 0.0001), (Fig. 2, Table S1).

Invertebrate biomass

The list of invertebrates and associated feeding groups is given in Table S2. The comparison of control groups of bromeliads (forest vs open) showed that the biomass of predators did not differ significantly between habitats (Mann-Whitney U: W = 45.5, p > 0.0500), and that the biomass of detritivorous prey was significantly lower in the open area (Mann-Whitney U: W = 87, p < 0.0100; Fig. 3A).

Deforestation did not alter predator biomass (Table 1, p > 0.0500), but significantly decreased the biomass of detritivorous prey (Table 1, p < 0.0500). Drought did not significantly impact prey biomass in the forest (Table 1, p > 0.0500), and in the open area (Mann-Whitney U: W = 73, p > 0.0500). However, drought significantly decreased the biomass of predators, both in the forest (Table 1, p < 0.0010) and in the open area (Mann-Whitney U: W = 81.5, p < 0.0500). Finally, the interactive effect of deforestation and drought almost eliminated the predator species (Table 1, p < 0.0001), and dramatically decreased the biomass of prey (Table 1, p < 0.0001, Fig. 3A, see also Figs. S1 and S2). Overall, prey that were able to resist and maintain populations in bromeliads subject to deforestation x drought were Trentepohlia sp. (shredder), Chironomini, Aulophorus superterrenus and Elpidium bromeliarum (collector-gatherers) (Fig. S2).

Table 1:

Post-hoc dunnett tests with Bonferroni correction, comparing the biomass of the various invertebrate feeding groups in control vs treatment bromeliads.

Univariate response	Control vs treatment	Estimate	SE	DF	Lower.CL	Upper.CL	T ratio	P value
Predators	FC – Deforestation	−5.3	3.69	45	−14.9	4.29	−1.437	0.6301
	FC – Forest drought	−16.5	3.69	45	−26.1	−6.91	−4.475	0.0002
	FC – D + Dr	−27.6	3.69	45	−37.2	−18.01	−7.485	<0.0001
	FC – D_Dr	−26.1	3.69	45	−35.7	−16.51	−7.079	<0.0001
Prey	FC – Deforestation	−10.35	3.85	45	−20.4	−0.336	−2.689	0.0400
	FC – Forest drought	−2.15	3.85	45	−12.2	7.864	−0.559	1.0000
	FC – D + Dr	−28.05	3.85	45	−38.1	−18.036	−7.289	<0.0001
	FC – D_Dr	−26.70	3.85	45	−36.7	−16.686	−6.938	<0.0001
FPOM consumers	FC – Deforestation	−9.9	5.08	45	−23.1	3.31	−1.950	0.2298
	FC – Forest drought	−12.1	5.08	45	−25.3	1.16	−2.373	0.0879
	FC – D + Dr	−24.9	5.08	45	−38.1	−11.69	−4.904	0.0001
	FC – D_Dr	−25.1	5.08	45	−38.4	−11.94	−4.953	<0.0001
CPOM consumers	FC – Deforestation	−6.65	3.67	45	−16.20	2.9	−1.812	0.3065
	FC – Forest drought	4.00	3.67	45	−5.55	13.5	1.090	1.0000
	FC – D + Dr	−26.05	3.67	45	−35.60	−16.5	−7.099	<0.0001
	FC – D_Dr	−27.80	3.67	45	−31.35	−12.3	−5.941	<0.0001

DOI: 10.7717/peerj.17346/table-1

Note:

FC, forest control; D + Dr, deforestation and drought sequentially; D_Dr, deforestation and drought simultaneously; p-value in bold denote significant effects (p < 0.05). Estimate, contrast of means; SE, standard error; DF, degree of freedom; Lower and Upper CL, confidence limits for the mean.

When detritivores were further categorized by the size of ingested particles, the biomass of FPOM and CPOM consumers was significantly higher in the forested area compared to the open area (Fig. 3B; FPOM consumers, Mann-Whitney U: W = 77, p < 0.0500; CPOM consumers, Mann-Whitney U: W = 83.5, p < 0.0500). Neither deforestation nor drought alone significantly altered the biomass of FPOM and CPOM consumers (Table 1, p > 0.0500 in all tests). Similarly, FPOM and CPOM consumers were not significantly impacted by drought in the open area (FPOM consumers, Mann Whitney U: W = 67, p > 0.0500; CPOM consumers, Mann-Whitney U: W = 53.5, p > 0.0500). However, the combined effect of deforestation and drought, either sequentially or simultaneously, had a strong negative impact on the biomass of both groups (Table 1, p ≤ 0.0001).

Discussion

We found that deforestation and drought alone had a moderate impact on the aquatic ecosystem of tank bromeliads, but that their combination had deleterious, synergistic effects on multitrophic communities. In line with our first and second hypotheses, deforestation negatively affected detritivore biomass (but did not eliminate species, see Fig. S2) and drought significantly reduced predator biomass in both forest and open areas, which could induce a change in the overall structure of multitrophic communities (see also Romero et al., 2020). Though we expected litter decomposition to be affected by changes in invertebrate biomass, we did not detect food-web mediated effects of drought or deforestation alone on decomposition. These results suggest that individual species and the aquatic ecosystem of tank bromeliads are relatively resistant to each of these disturbance types. Our third hypothesis of a stronger effect of combined disturbances was verified, as the combination of deforestation and drought synergistically reduced the biomass of all invertebrate functional groups and bacteria, whatever the sequence of the disturbance types. Among the various trophic levels, predators were virtually eliminated while detritivore biomass was strongly depleted (Table 1, Figs. 3A and 3B). Nevertheless, contrary to our assumptions, decomposition was not sensitive to any of our treatments involving deforestation and/or drought (Table 3 and Fig. 3D). We note that fungi, key players of the decomposition process (Pascoal & Cássio, 2004), were either unaffected or boosted by our treatments (Table 2 and Fig. 3C). As decomposition was essentially microbial in treatment and control groups, our results further suggest that a core group of highly-resistant microorganisms plus a few invertebrate detritivores (among which Tipulidae are shredders), ensure the stability of key ecosystem functions across environments (Dézerald et al., 2013), and in the face of local to global environmental change. Moreover, our experiment demonstrates that even an intrinsically-resistant Neotropical ecosystem, that has the capacity to maintain its structure and functioning when exposed to a single disturbance type, can experience dramatic changes in food web structure when exposed to a combination of local- and global-scale disturbances. Assuming that taking global action is more challenging than taking local-regional actions, policy-makers should be encouraged to implement environmental action plans that will halt habitat destruction, to dampen any detrimental interactive effect with the impacts of global climate change.

We see at least two non-mutually exclusive explanations for the weak effects of deforestation or drought on aquatic ecosystems: (i) the ability of physical habitats (here the bromeliad rosette) to buffer changes in hydrology and resource inputs (Fernandez Barrancos, Reid & Aronson, 2017), and (ii) the ability of organisms to behaviourally and/or physiologically cope with these changes. First, tank bromeliads have evolved to capture and retain water and detritus so the system itself is relatively resistant to dry periods, and able to collect various types of palatable detritus in any habitat type (litter, dust, dead insects, faeces, etc.). The multiple leaves divide the overall water volume, thus reducing evaporation rates during a drought, or despite changes in canopy cover that alter ambient humidity and throughfall. For instance, it takes up to 7 weeks to completely dry out a small bromeliad in the forest in the absence of rainfall (Dézerald et al., 2015). Here, only three out of 20 bromeliads subjected to drought completely dried out, and all bromeliads subjected to deforestation kept a water volume superior to 100 mL, the threshold for the presence of large odonate larvae (predators) in tank bromeliads (Srivastava et al., 2020). This physical buffering effect that benefits to aquatic micro- to macro-organisms can be extended to other lentic freshwater ecosystems such as ponds and pools, where habitat complexity (e.g., surface:volume ratio, porosity, drainage basin area) dampen the effects of environmental change (Kebede et al., 2006). Second, species tend to be generalists and/or have evolved tolerance and resistance traits that allow ecological adaptation to changing conditions (Dézerald et al., 2015; Strachan, Chester & Robson, 2015). We know for instance that bromeliads host a core of generalist species (including invertebrates and microorganisms) that is relatively constant across Neotropical environments (open savannah, primary and secondary forest, plantations) and across large regional scales, so that plasticity in basal resource use is widespread and shifts in food web structure are mostly related to the addition or loss of top-predators (Dézerald et al., 2013; Romero et al., 2020). A more recent study further showed that the median lethal time (LT50) of bromeliad invertebrate populations experimentally subjected to desiccation varies from 4 to 19 days depending on the species. The literature and our results therefore support the idea that the plant-held waters of Neotropical forests host multitrophic communities that are resistant to drought and deforestation, provided that these changes are not combined.

The interactive effect of deforestation and drought was much higher than the sum of individual effects, for entire invertebrate populations or even functional groups (e.g., predators) were wiped out, and the biomass of bacteria decreased significantly when it was not affected by each disturbance in isolation (Tables 1 and 2; Fig. 3). This result means that a negative synergism (sensu Piggott, Townsend & Matthaei, 2015) of two disturbances that each have moderate effects drove mortality beyond the physical and biological buffering capacities of the system. Synergistic interactions could be generated by different types of effects: (i) interaction chain effects (Buma, 2015), e.g., if deforestation enhances drought severity by increasing evaporation rates (ii) interaction modification effects (Trzcinski et al., 2016), e.g., if the per capita effects of deforestation on aquatic organisms is enhanced by drought, and (iii) interaction exposure effects, e.g., if preceding deforestation altered the taxonomic and/or functional structure of communities further exposed to drought (Shinoda & Akasaka, 2020). As the outcomes of simultaneous and sequential disturbances were not different, we can reasonably exclude exposure effects. Because the outcome of the interaction was to dry out bromeliads (something that did not happen with drought or deforestation alone), we further conclude that most of the observed impacts on multitrophic communities can be attributed to interaction chain effects.

Whilst bacterial biomass declined under the interactive effects of deforestation and drought, fungi were resistant to even the harshest experimental conditions emulated. In presence of invertebrates, fungal biomass was even boosted by severe disturbances (Table 2, Figs. 3 and S3). Similar observations in different ecosystems type and at different latitudes (Li et al., 2023; Yuste et al., 2011), lead to the general conclusion that fungi are much more tolerant to drought than bacteria because they evolved desiccation-tolerance traits such as thick cell walls and osmolytes (Treseder et al., 2010). Interestingly, fungi can replace bacteria in the decomposition process under high stress conditions (Yuste et al., 2011). Assuming that decomposition in tank bromeliads is mostly driven by microbial activity (Leroy et al., 2017; this study), and that fungi can remain active under extremely dry conditions (Allison et al., 2013), it is therefore not surprising that decomposition did not decline in manipulated bromeliads (see also Schaeffer et al., 2017; Schimel, Balser & Wallenstein, 2007), including the driest conditions created by drought x deforestation. Together with the literature, our results support the ideas that (i) fungal hyphae play a crucial role for the persistence of detrital decomposition, a key ecological process in Neotropical ecosystems and in other ecosystems worldwide, in the face of environmental change (Banerjee et al., 2016; Philippot, Griffiths & Langenheder, 2021), and (ii) a drier world resulting from the interaction of habitat destruction and global climate change might favour microbial communities dominated by fungi (Treseder et al., 2018). We finally note that a few invertebrate species were able to maintain populations under interactive effects, namely Aulophorus superterrenus (Annelid, Oligochaeta), Elpidium bromeliarum (Crustacea, Ostracoda), an unidentified Chironomini (Insecta, Chironomidae), and Trentepohlia sp. (Insecta, Tipulidae). These species are among the commonest, both in terms of occurrence and number of individuals, in tank bromeliads of French Guiana whatever the habitat type (Dézerald et al., 2017; Jabiol et al., 2009). This suggests that only ubiquist species will resist the interactive effects of deforestation and drought while both frequent and rare species will be eliminated, probably to the detriment of unique functional trait combinations (Céréghino et al., 2022).

Conclusions

To the best of our knowledge, this study is the first attempt to understand the combined effect of drought and deforestation at the level of an entire freshwater ecosystem in the Neotropics, a region of the World that both hosts species-rich ecosystems and is particularly subject to these disturbances. We acknowledge that our model system, the bromeliad ecosystem, is quite resistant in the face of deforestation or drought (see also Bonhomme et al., 2021). In other freshwater ecosystems such as streams for instance, either drought or deforestation can lead to much stronger changes in decomposition rates following to a decline in shredders diversity and density (e.g., Lake, 2003; Lima et al., 2022; Silva-Araújo et al., 2020; Tanaka et al., 2015). However, if these systems are more sensitive than bromeliads to either deforestation or drought, we can then conclude from our results that, even if drought or deforestation have moderate or even short-term impacts, a combination of the two disturbances will generally have deleterious effects on freshwater biodiversity and ecosystem functions (Taniwaki et al., 2017). Beyond the ecological implications, the results and conclusions reported in this study provide important insights to decision makers. Not only global climate change and habitat destruction operate at different spatial and temporal scales, but political agreements of global extent are much more difficult to obtain than regional-national actions (Galaz, 2022). Therefore, whilst it would take decades or centuries to counteract the negative effects of climate change, action could theoretically be taken to halt habitat destruction with the aim to mitigate the drastic effects local x global environmental change on freshwater ecosystems.

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