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

Background: Together with the intensification of dry seasons in Neotropical regions, increasing deforestation is expected to exacerbate species extinctions, something that could lead to dramatic shifts in multitrophic communities and ecosystem functions. Recent studies suggest that the effects of habitat loss are greater where precipitation has decreased. Yet, experimental studies of the pure and interactive effects of drought and deforestation at ecosystem level remain scarce. Methods: Here, we used rainshelters and transplantation from rainforest to open areas of natural microcosms (the aquatic ecosystem and microbial-faunal food web found within the rainwater-filled leaves of tank bromeliads) to emulate drought and deforestation in a full factorial experimental design. We analysed the pure and interactive effects of our treatments on functional community structure (including microorganisms, detritivore and predatory invertebrates), and on leaf litter decomposition in tank bromeliad ecosystems. Results: Drought or deforestation alone had a moderate impact on biomass at the various trophic level, but did not eliminate species. However, their interaction synergistically reduced the biomass of all invertebrate functional groups and bacteria. Predators were the most impacted trophic group as they were totally eliminated, while detritivore biomass was reduced by about 95%. Fungal biomass was either unaffected or boosted by our treatments. Decomposition was essentially driven by microbial activity, and did not change across treatments involving deforestation and/or drought. Conclusions: Our results suggest that highly resistant microorganisms such as fungi (plus a few detritivores) maintain key ecosystem functions in the face of drought and habitat change. We conclude that habitat destruction compounds the problems of climate change, that the impacts of the two phenomena on food webs are mutually reinforcing, and that the stability of ecosystem functions depends on the resistance of a core group of organisms. 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.

Light intensity mediates phenotypic plasticity and leaf trait regionalization in a tank bromeliad.

BACKGROUND AND AIMS: Phenotypic plasticity allows plants to cope with environmental variability. Plastic responses to the environment have mostly been investigated at the level of individuals (plants) but can also occur within leaves. Yet the latter have been underexplored, as leaves are often treated as functional units with no spatial structure. We investigated the effect of a strong light gradient on plant and leaf traits and examined whether different portions of a leaf show similar or differential responses to light intensity. METHODS: We measured variation in 27 morpho-anatomical and physiological traits of the rosette and leaf portions (i.e. base and apex) of the tank bromeliad Aechmea aquilega (Bromeliaceae) when naturally exposed to a marked gradient of light intensity. KEY RESULTS: The light intensity received by A. aquilega had a strong effect on the structural, biochemical and physiological traits of the entire rosette. Plants exposed to high light intensity were smaller and had wider, shorter, more rigid and more vertical leaves. They also had lower photosynthetic performance and nutrient levels. We found significant differences between the apex and basal portions of the leaf under low-light conditions, and the differences declined or disappeared for most of the traits as light intensity increased (i.e. leaf thickness, adaxial trichome density, abaxial and adaxial trichome surface, and vascular bundle surface and density). CONCLUSIONS: Our results reveal a strong phenotypic plasticity in A. aquilega, particularly in the form of a steep functional gradient within the leaf under low-light conditions. Under high-light conditions, trait values were relatively uniform along the leaf. This study sheds interesting new light on the functional complexity of tank bromeliad leaves, and on the effect of environmental conditions on leaf trait regionalization.

Understanding the patterns and processes underlying water quality and pollution risk in West-Africa River using self-organizing maps and multivariate analyses.

Rivers are dynamic systems in complex interactions with their surrounding environments. Reliable and fast interpretation of water quality is therefore needed for sustainable river management. Unfortunately, water quality and environmental status interactions have not yet been documented sufficiently in West-Africa. This study explored the spatial-latitudinal and seasonal features of water quality along the Sô River Basin (SRB, West Africa) using self-organizing map (SOM) and principal component analysis. Twenty-two water quality variables were measured in the surface layer at 12 different sampling sites during a twenty-four-month period from July 2016 to June 2018. The results revealed three water quality groups, following an upstream-downstream pollution gradient: (1) upstream and middle reach sites with high dissolved oxygen and Secchi disk depth values, which are more suitable for the aquatic biota; (2) downstream sites with high concentrations of ammonium, biochemical oxygen demand, and heavy metals especially in flood period, reflecting both high organic and heavy metal pollution; and (3) brackish downstream sites characterized by less heavy metal and organic pollutions. No significant variation was observed between seasons. However, the SRB relatively suffered from higher risks of heavy metal contamination and organic pollution in wet seasons. Although hydroclimatic processes affect the water quality, anthropogenic inputs of point and non-point sources were identified and discussed as a more prominent factor contributing to variation in the water quality condition. These results offer insights into the water quality dynamics in river-estuary system as well as potential pollution sources, crucial for defining sanitation, and management measures.

Linkages between Sphagnum metabolites and peatland CO2 uptake are sensitive to seasonality in warming trends.

Plants produce a wide diversity of metabolites. Yet, our understanding of how shifts in plant metabolites as a response to climate change feedback on ecosystem processes remains scarce. Here, we test to what extent climate warming shifts the seasonality of metabolites produced by Sphagnum mosses, and what are the consequences of these shifts for peatland C uptake. We used a reciprocal transplant experiment along a climate gradient in Europe to simulate climate change. We evaluated the responses of primary and secondary metabolites in five Sphagnum species and related their responses to gross ecosystem productivity (GEP). When transplanted to a warmer climate, Sphagnum species showed consistent responses to warming, with an upregulation of either their primary or secondary metabolite according to seasons. Moreover, these shifts were correlated to changes in GEP, especially in spring and autumn. Our results indicate that the Sphagnum metabolome is very plastic and sensitive to warming. We also show that warming-induced changes in the seasonality of Sphagnum metabolites have consequences on peatland GEP. Our findings demonstrate the capacity for plant metabolic plasticity to impact ecosystem C processes and reveal a further mechanism through which Sphagnum could shape peatland responses to climate change.

Asynchronous recovery of predators and prey conditions resilience to drought in a neotropical ecosystem.

The predicted increase in the intensity and frequency of drought events associated with global climate change will impose severe hydrological stress to freshwater ecosystems, potentially altering their structure and function. Unlike freshwater communities' direct response to drought, their post-drought recovery capacities remain understudied despite being an essential component driving ecosystem resilience. Here we used tank bromeliad as model ecosystem to emulate droughts of different duration and then assess the recovery capacities of ecosystem structure and function. We followed macroinvertebrate predator and prey biomass to characterize the recovery dynamics of trophic structure (i.e. predator-prey biomass ratio) during the post-drought rewetting phase. We showed that drought significantly affects the trophic structure of macroinvertebrates by reducing the predator-prey biomass ratio. The asynchronous recovery of predator and prey biomass appeared as a critical driver of the post-drought recovery trajectory of trophic structure. Litter decomposition rate, which is an essential ecosystem function, remained stable after drought events, indicating the presence of compensatory effects between detritivores biomass and detritivores feeding activity. We conclude that, in a context of global change, the asynchrony in post-drought recovery of different trophic levels may impact the overall drought resilience of small freshwater ecosystems in a more complex way than expected.

Photosynthetic microorganisms effectively contribute to bryophyte CO2 fixation in boreal and tropical regions.

Photosynthetic microbes are omnipresent in land and water. While they critically influence primary productivity in aquatic systems, their importance in terrestrial ecosystems remains largely overlooked. In terrestrial systems, photoautotrophs occur in a variety of habitats, such as sub-surface soils, exposed rocks, and bryophytes. Here, we study photosynthetic microbial communities associated with bryophytes from a boreal peatland and a tropical rainforest. We interrogate their contribution to bryophyte C uptake and identify the main drivers of that contribution. We found that photosynthetic microbes take up twice more C in the boreal peatland (~4.4 mg CO2.h-1.m-2) than in the tropical rainforest (~2.4 mg CO2.h-1.m-2), which corresponded to an average contribution of 4% and 2% of the bryophyte C uptake, respectively. Our findings revealed that such patterns were driven by the proportion of photosynthetic protists in the moss microbiomes. Low moss water content and light conditions were not favourable to the development of photosynthetic protists in the tropical rainforest, which indirectly reduced the overall photosynthetic microbial C uptake. Our investigations clearly show that photosynthetic microbes associated with bryophyte effectively contribute to moss C uptake despite species turnover. Terrestrial photosynthetic microbes clearly have the capacity to take up atmospheric C in bryophytes living under various environmental conditions, and therefore potentially support rates of ecosystem-level net C exchanges with the atmosphere.

Peatland microhabitat heterogeneity drives phototrophic microbe distribution and photosynthetic activity.

Phototrophic microbes are widespread in soils, but their contribution to soil carbon (C) uptake remains underexplored in most terrestrial systems, including C-accreting systems such as peatlands. Here, by means of metabarcoding and ecophysiological measurements, we examined how microbial photosynthesis and its biotic (e.g., phototrophic community structure, biomass) and abiotic drivers (e.g., Sphagnum moisture, light intensity) vary across peatland microhabitats. Using a natural gradient of microhabitat conditions from pool to forest, we show that the structure of phototrophic microbial communities shifted from a dominance of eukaryotes in pools to prokaryotes in forests. We identified five groups of co-occurring phototrophic operational taxonomic units with specific environmental preferences across the gradient. Along with such structural changes, we found that microbial C uptake was the highest in the driest and shadiest microhabitats. This study renews and improves current views on phototrophic microbes in peatlands, as the contribution of microbial photosynthesis to peatland C uptake has essentially been studied in wet microhabitats.

In situ resistance, not immigration, supports invertebrate community resilience to drought intensification in a Neotropical ecosystem.

While future climate scenarios predict declines in precipitations in many regions of the world, little is known of the mechanisms underlying community resilience to prolonged dry seasons, especially in 'naïve' Neotropical rainforests. Predictions of community resilience to intensifying drought are complicated by the fact that the underlying mechanisms are mediated by species' tolerance and resistance traits, as well as rescue through dispersal from source patches. We examined the contribution of in situ tolerance-resistance and immigration to community resilience, following drought events that ranged from the ambient norm to IPCC scenarios and extreme events. We used rainshelters above rainwater-filled bromeliads of French Guiana to emulate a gradient of drought intensity (from 1 to 3.6 times the current number of consecutive days without rainfall), and we analysed the post-drought dynamics of the taxonomic and functional community structure of aquatic invertebrates to these treatments when immigration is excluded (by netting bromeliads) or permitted (no nets). Drought intensity negatively affected invertebrate community resistance, but had a positive influence on community recovery during the post-drought phase. After droughts of 1 to 1.4 times the current intensities, the overall invertebrate abundance recovered within invertebrate life cycle durations (up to 2 months). Shifts in taxonomic composition were more important after longer droughts, but overall, community composition showed recovery towards baseline states. The non-random patterns of changes in functional community structure indicated that deterministic processes like environmental filtering of traits drive community re-assembly patterns after a drought event. Community resilience mostly relied on in situ tolerance-resistance traits. A rescue effect of immigration after a drought event was weak and mostly apparent under extreme droughts. Under climate change scenarios of drought intensification in Neotropical regions, community and ecosystem resilience could primarily depend on the persistence of suitable habitats and on the resistance traits of species, while metacommunity dynamics could make a minor contribution to ecosystem recovery. Climate change adaptation should thus aim at identifying and preserving local conditions that foster in situ resistance and the buffering effects of habitat features.

Comment on "Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances".

Van Klink et al (Reports, 24 April 2020, p. 417) argue for a more nuanced view of insect decline, and of human responsibility for this decline, than previously suggested. However, shortcomings in data selection and methodology raise questions about their conclusions on trends and drivers. We call for more rigorous methodology to be applied in meta-analyses of ecological data.

Extreme rainfall events alter the trophic structure in bromeliad tanks across the Neotropics.

Changes in global and regional precipitation regimes are among the most pervasive components of climate change. Intensification of rainfall cycles, ranging from frequent downpours to severe droughts, could cause widespread, but largely unknown, alterations to trophic structure and ecosystem function. We conducted multi-site coordinated experiments to show how variation in the quantity and evenness of rainfall modulates trophic structure in 210 natural freshwater microcosms (tank bromeliads) across Central and South America (18°N to 29°S). The biomass of smaller organisms (detritivores) was higher under more stable hydrological conditions. Conversely, the biomass of predators was highest when rainfall was uneven, resulting in top-heavy biomass pyramids. These results illustrate how extremes of precipitation, resulting in localized droughts or flooding, can erode the base of freshwater food webs, with negative implications for the stability of trophic dynamics.

Resource availability drives bacterial succession during leaf-litter decomposition in a bromeliad ecosystem.

Despite the growing number of investigations on microbial succession during the last decade, most of our knowledge on primary succession of bacteria in natural environments comes from conceptual models and/or studies of chronosequences. Successional patterns of litter-degrading bacteria remain poorly documented, especially in undisturbed environments. Here we conducted an experiment with tank bromeliads as natural freshwater microcosms to assess major trends in bacterial succession on two leaf-litter species incubated with or without animal exclusion. We used amplicon sequencing and a co-occurrence network to assess changes in bacterial community structure according to treatments. Alpha-diversity and community complexity displayed the same trends regardless of the treatments, highlighting that primary succession of detrital-bacteria is subject to resource limitation and biological interactions, much like macro-organisms. Shifts in bacterial assemblages along the succession were characterized by an increase in uncharacterized taxa and potential N-fixing bacteria, the latter being involved in positive co-occurrence between taxa. These findings support the hypothesis of interdependence between taxa as a significant niche-based process shaping bacterial communities during the advanced stage of succession.

Ecological response to altered rainfall differs across the Neotropics.

There is growing recognition that ecosystems may be more impacted by infrequent extreme climatic events than by changes in mean climatic conditions. This has led to calls for experiments that explore the sensitivity of ecosystems over broad ranges of climatic parameter space. However, because such response surface experiments have so far been limited in geographic and biological scope, it is not clear if differences between studies reflect geographic location or the ecosystem component considered. In this study, we manipulated rainfall entering tank bromeliads in seven sites across the Neotropics, and characterized the response of the aquatic ecosystem in terms of invertebrate functional composition, biological stocks (total invertebrate biomass, bacterial density) and ecosystem fluxes (decomposition, carbon, nitrogen). Of these response types, invertebrate functional composition was the most sensitive, even though, in some sites, the species pool had a high proportion of drought-tolerant families. Total invertebrate biomass was universally insensitive to rainfall change because of statistical averaging of divergent responses between functional groups. The response of invertebrate functional composition to rain differed between geographical locations because (1) the effect of rainfall on bromeliad hydrology differed between sites, and invertebrates directly experience hydrology not rainfall and (2) the taxonomic composition of some functional groups differed between sites, and families differed in their response to bromeliad hydrology. These findings suggest that it will be difficult to establish thresholds of "safe ecosystem functioning" when ecosystem components differ in their sensitivity to climatic variables, and such thresholds may not be broadly applicable over geographic space. In particular, ecological forecast horizons for climate change may be spatially restricted in systems where habitat properties mediate climatic impacts, and those, like the tropics, with high spatial turnover in species composition.

Highly modular pattern in ant-plant interactions involving specialized and non-specialized myrmecophytes.

Because Tachia guianensis (Gentianaceae) is a "non-specialized myrmecophyte" associated with 37 ant species, we aimed to determine if its presence alters the ant guild associated with sympatric "specialized myrmecophytes" (i.e., plants sheltering a few ant species in hollow structures). The study was conducted in a hilly zone of a neotropical rainforest where two specialized myrmecophytes grow at the bottom of the slopes, another at mid-slope, and a fourth on the hilltops. Tachia guianensis, which occurred everywhere, had its own guild of associated ant species. A network analysis showed that its connections with the four other myrmecophytes were rare and weak, the whole resulting in a highly modular pattern of interactions with one module (i.e., subnetwork) per myrmecophyte. Three ant species parasitized three out of the four specialized myrmecophytes (low nestedness noted), but were not or barely associated with T. guianensis that therefore did not influence the parasitism of specialized myrmecophytes.

An arboreal spider protects its offspring by diving into the water of tank bromeliads.

Cupiennius salei (Ctenidae) individuals frequently live in association with tank bromeliads, including Aechmea bracteata, in Quintana Roo (Mexico). Whereas C. salei females without egg sacs hunt over their entire host plant, females carrying egg sacs settle above the A. bracteata reservoirs they have partially sealed with silk. There they avoid predators that use sight to detect their prey, as is known for many bird species. Furthermore, if a danger is more acute, these females dive with their egg sacs into the bromeliad reservoir. An experiment showed that this is not the case for males or females without egg sacs. In addition to the likely abundance of prey found therein, the potential of diving into the tank to protect offspring may explain the close association of this spider with bromeliads. These results show that, although arboreal, C. salei evolved a protective behavior using the water of tank bromeliads to protect offspring.

Simulated drought regimes reveal community resilience and hydrological thresholds for altered decomposition.

Future climate scenarios forecast a 10-50% decline in rainfall in Eastern Amazonia. Altered precipitation patterns may change important ecosystem functions like decomposition through either changes in physical and chemical processes or shifts in the activity and/or composition of species. We experimentally manipulated hydroperiods (length of wet:dry cycles) in a tank bromeliad ecosystem to examine impacts on leaf litter decomposition. Gross loss of litter mass over 112 days was greatest in continuously submersed litter, lowest in continuously dry litter, and intermediate over a range of hydroperiods ranging from eight cycles of 7 wet:7 dry days to one cycle of 56 wet:56 dry days. The resilience of litter mass loss to hydroperiod length is due to a shift from biologically assisted decomposition (mostly microbial) at short wet:dry hydroperiods to physicochemical release of dissolved organic matter at longer wet:dry hydroperiods. Biologically assisted decomposition was maximized at wet:dry hydroperiods falling within the range of ambient conditions (12-22 consecutive dry days) but then declined under prolonged wet:dry hydroperiods (28 and 56 dry days. Fungal:bacterial ratios showed a similar pattern as biologically assisted decomposition to hydroperiod length. Our results suggest that microbial communities confer functional resilience to altered hydroperiod in tank bromeliad ecosystems. We predict a substantial decrease in biological activity relevant to decomposition under climate scenarios that increase consecutive dry days by 1.6- to 3.2-fold in our study area, whereas decreased frequency of dry periods will tend to increase the physicochemical component of decomposition.

Terrestrial support of aquatic food webs depends on light inputs: a geographically-replicated test using tank bromeliads.

Food webs of freshwater ecosystems can be subsidized by allochthonous resources. However, it is still unknown which environmental factors regulate the relative consumption of allochthonous resources in relation to autochthonous resources. Here, we evaluated the importance of allochthonous resources (litterfall) for the aquatic food webs in Neotropical tank bromeliads, a naturally replicated aquatic microcosm. Aquatic invertebrates were sampled in more than 100 bromeliads within either open or shaded habitats and within five geographically distinct sites located in four different countries. Using stable isotope analyses, we determined that allochthonous sources comprised 74% (±17%) of the food resources of aquatic invertebrates. However, the allochthonous contribution to aquatic invertebrates strongly decreased from shaded to open habitats, as light incidence increased in the tanks. The density of detritus in the tanks had no impact on the importance of allochthonous sources to aquatic invertebrates. This overall pattern held for all invertebrates, irrespective of the taxonomic or functional group to which they belonged. We concluded that, over a broad geographic range, aquatic food webs of tank bromeliads are mostly allochthonous-based, but the relative importance of allochthonous subsidies decreases when light incidence favors autochthonous primary production. These results suggest that, for other freshwater systems, some of the between-study variation in the importance of allochthonous subsidies may similarly be driven by the relative availability of autochthonous resources.

Unexpectedly high bacteriochlorophyll a concentrations in neotropical tank bromeliads.

The contribution of bacteriochlorophyll a (BChl a) to photosynthetically driven electron transport is generally low in aquatic and terrestrial systems. Here, we provide evidence that anoxygenic bacterial phototrophy is widespread and substantial in water retained by tank bromeliads of a primary rainforest in French Guiana. An analysis of the water extracted from 104 randomly selected tank bromeliads using infrared fluorimetry suggested the overall presence of abundant anoxygenic phototrophic bacterial populations. We found that purple bacteria dominated these populations responsible for unusually high BChl a/chlorophyll a ratios (>50%). Our data suggest that BChl a-based phototrophy in tank bromeliads can have significant effects on the ecology of tank-bromeliad ecosystems and on the carbon and energy fluxes in Neotropical forests.

The effects of food web structure on ecosystem function exceeds those of precipitation.

Ecosystems are being stressed by climate change, but few studies have tested food web responses to changes in precipitation patterns and the consequences to ecosystem function. Fewer still have considered whether results from one geographic region can be applied to other regions, given the degree of community change over large biogeographic gradients. We assembled, in one field site, three types of macroinvertebrate communities within water-filled bromeliads. Two represented food webs containing both a fast filter feeder-microbial and slow detritivore energy channels found in Costa Rica and Puerto Rico, and one represented the structurally simpler food webs in French Guiana, which only contained the fast filter feeder-microbial channel. We manipulated the amount and distribution of rain entering bromeliads and examined how food web structure mediated ecosystem responses to changes in the quantity and temporal distribution of precipitation. Food web structure affected the survival of functional groups in general and ecosystem functions such as decomposition and the production of fine particulate organic matter. Ecosystem processes were more affected by decreased precipitation than were the abundance of micro-organisms and metazoans. In our experiments, the sensitivity of the ecosystem to precipitation change was primarily revealed in the food web dominated by the single filter feeder-microbial channel because other top-down and bottom-up processes were weak or absent. Our results show stronger effects of food web structure than precipitation change per se on the functioning of bromeliad ecosystems. Consequently, we predict that ecosystem function in bromeliads throughout the Americas will be more sensitive to changes in the distribution of species, rather than to the direct effects caused by changes in precipitation.

The dynamics of ant mosaics in tropical rainforests characterized using the Self-Organizing Map algorithm.

Ants, the most abundant taxa among canopy-dwelling animals in tropical rainforests, are mostly represented by territorially dominant arboreal ants (TDAs) whose territories are distributed in a mosaic pattern (arboreal ant mosaics). Large TDA colonies regulate insect herbivores, with implications for forestry and agronomy. What generates these mosaics in vegetal formations, which are dynamic, still needs to be better understood. So, from empirical research based on 3 Cameroonian tree species (Lophira alata, Ochnaceae; Anthocleista vogelii, Gentianaceae; and Barteria fistulosa, Passifloraceae), we used the Self-Organizing Map (SOM, neural network) to illustrate the succession of TDAs as their host trees grow and age. The SOM separated the trees by species and by size for L. alata, which can reach 60 m in height and live several centuries. An ontogenic succession of TDAs from sapling to mature trees is shown, and some ecological traits are highlighted for certain TDAs. Also, because the SOM permits the analysis of data with many zeroes with no effect of outliers on the overall scatterplot distributions, we obtained ecological information on rare species. Finally, the SOM permitted us to show that functional groups cannot be selected at the genus level as congeneric species can have very different ecological niches, something particularly true for Crematogaster spp., which include a species specifically associated with B. fistulosa, nondominant species and TDAs. Therefore, the SOM permitted the complex relationships between TDAs and their growing host trees to be analyzed, while also providing new information on the ecological traits of the ant species involved.

Tank bromeliads as natural microcosms: a facultative association with ants influences the aquatic invertebrate community structure.

Many tank bromeliads have facultative relationships with ants as is the case in French Guiana between Aechmea aquilega (Salib.) Griseb. and the trap-jaw ant, Odontomachus haematodus Linnaeus. Using a redundancy analysis, we determined that the presence of O. haematodus colonies is accompanied by a greater quantity of fine particulate organic matter in the water likely due to their wastes. This increase in nutrient availability is significantly correlated with an increase in the abundance of some detritivorous taxa, suggesting a positive bottom-up influence on the aquatic macroinvertebrate communities living in the A. aquilega wells. On the other hand, the abundance of top predators is negatively affected by a lower number of available wells due to ant constructions for nesting, releasing a top-down pressure that could also favor lower trophic levels.