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.

When the "satisficing" is the new "fittest": how a proscriptive definition of adaptation can change our view of cognition and culture.

Since Darwin's theory of evolution, adaptationism is frequently invoked to explain cognition and cultural processes. Adaptationism can be described as a prescriptive view, as phenotypes that do not optimize fitness should not be selected by natural selection. From an epistemological perspective, the principle of a prescriptive definition of adaptation seems incompatible with recent advances in epigenetics, evolutionary developmental biology, ethology, and genomics. From these challenges, a proscriptive view of adaptation has emerged, postulating that phenotypes that are not deleterious will be evolutionary maintained. In this epistemological investigation, we examine how the shift from adaptationism to a proscriptive view changes our view of cognition and culture. We argue that, while adaptationism leads to cognitivism and a view of culture as strategies to optimize overall fitness, the proscriptive definition favors embodied theories of cognition and a view of culture as the cumulative diffusion of behaviors allowed by the constraints of reproduction.

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.

Biogeomorphological eco-evolutionary feedback between life and geomorphology: a theoretical framework using fossorial mammals.

Engineer organisms not only adapt to pre-existing environmental conditions but also co-construct their physical environment. By doing so, they can subsequently change selection pressures for themselves and other species, as well as change community and ecosystem structures and functions. Focusing on one representative example, i.e., fossorial mammals, we show that geomorphological Earth system components are crucial for understanding and quantifying links between evolutionary and ecosystem dynamics and that feedbacks between geomorphology and engineer organisms constitute a major driver of geomorphological organization on the Earth's surface. We propose a biogeomorphological eco-evolutionary feedback synthesis from the gene to the landscape where eco-evolutionary feedbacks are mediated by the geomorphological dimensions of a niche that are affected by engineer organisms, such as fossorial mammals. Our concept encompasses (i) the initial responses of fossorial mammals to environmental constraints that enhance the evolution of their morphological and biomechanical traits for digging in the soil; (ii) specific adaptations of engineer fossorial mammals (morphological, biomechanical, physiological and behavioural feedback traits for living in burrows) to their constructed geomorphological environment; and (iii) ecological and evolutionary feedbacks diffusing at the community and ecological levels. Such a new perspective in geomorphology may lead to a better conceptualization and analysis of Earth surface processes and landforms as parts of complex adaptive systems in which Darwinian selection processes at lower landscape levels lead to self-organization of higher-level landforms and landscapes.

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.

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.

An uneasy alliance: a nesting association between aggressive ants and equally fierce social wasps.

Although the Neotropical territorially dominant arboreal ant Azteca chartifex Forel is very aggressive towards any intruder, its populous colonies tolerate the close presence of the fierce polistine wasp Polybia rejecta (F.). In French Guiana, 83.33% of the 48 P. rejecta nests recorded were found side by side with those of A. chartifex. This nesting association results in mutual protection from predators (i.e., the wasps protected from army ants; the ants protected from birds). We conducted field studies, laboratory-based behavioral experiments and chemical analyses to elucidate the mechanisms allowing the persistence of this association. Due to differences in the cuticular profiles of the two species, we eliminated the possibility of chemical mimicry. Also, analyses of the carton nests did not reveal traces of marking on the envelopes. Because ant forager flows were not perturbed by extracts from the wasps' Dufour's and venom glands, we rejected any hypothetical action of repulsive chemicals. Nevertheless, we noted that the wasps "scraped" the surface of the upper part of their nest envelope using their mandibles, likely removing the ants' scent trails, and an experiment showed that ant foragers were perturbed by the removal of their scent trails. This leads us to use the term "erasure hypothesis." Thus, this nesting association persists thanks to a relative tolerance by the ants towards wasp presence and the behavior of the wasps that allows them to "contain" their associated ants through the elimination of their scent trails, direct attacks, "wing-buzzing" behavior and ejecting the ants.

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.

Ants impact the composition of the aquatic macroinvertebrate communities of a myrmecophytic tank bromeliad.

In an inundated Mexican forest, 89 out of 92 myrmecophytic tank bromeliads (Aechmea bracteata) housed an associated ant colony: 13 sheltered Azteca serica, 43 Dolichoderus bispinosus, and 33 Neoponera villosa. Ant presence has a positive impact on the diversity of the aquatic macroinvertebrate communities (n=30 bromeliads studied). A Principal Component Analysis (PCA) showed that the presence and the species of ant are not correlated to bromeliad size, quantity of water, number of wells, filtered organic matter or incident radiation. The PCA and a generalized linear model showed that the presence of Azteca serica differed from the presence of the other two ant species or no ants in its effects on the aquatic invertebrate community (more predators). Therefore, both ant presence and species of ant affect the composition of the aquatic macroinvertebrate communities in the tanks of A. bracteata, likely due to ant deposition of feces and other waste in these tanks.

A mimetic nesting association between a timid social wasp and an aggressive arboreal ant.

In French Guiana, the arboreal nests of the swarm-founding social wasp Protopolybia emortualis (Polistinae) are generally found near those of the arboreal dolichoderine ant Dolichoderus bidens. These wasp nests are typically protected by an envelope, which in turn is covered by an additional carton 'shelter' with structure resembling the D. bidens nests. A few wasps constantly guard their nest to keep D. bidens workers from approaching. When alarmed by a strong disturbance, the ants invade the host tree foliage whereas the wasps retreat into their nest. Notably, there is no chemical convergence in the cuticular profiles of the wasps and ants sharing a tree. The aggressiveness of D. bidens likely protects the wasps from army ant raids, but the ants do not benefit from the presence of the wasps; therefore, this relationship corresponds to a kind of commensalism.

Hollow Internodes Permit a Neotropical Understory Plant to Shelter Multiple Mutualistic Ant Species, Obtaining Protection and Nutrient Provisioning (Myrmecotrophy).

The Neotropical understory plant Tachia guianensis (Gentianaceae)-known to shelter the colonies of several ant species in its hollow trunks and branches-does not provide them with food rewards (e.g., extrafloral nectar). We tested whether these ants are opportunistic nesters or whether mutualistic relationships exist as for myrmecophytes or plants sheltering ant colonies in specialized hollow structures in exchange for protection from enemies and/or nutrient provisioning (myrmecotrophy). We noted 37 ant species sheltering inside T. guianensis internodes, three of them accounting for 43.5% of the cases. They protect their host plants from leaf-cutting ant defoliation and termite damage because individuals devoid of associated ants suffered significantly more attacks. Using the stable isotope 15N, we experimentally showed that the tested ant species furnish their host plants with nutrients. Therefore, a mutualism exists. However, because it is associated with numerous ant species, T. guianensis can be considered a nonspecialized myrmecophyte.

The predatory behavior of the Neotropical social wasp Polybia rejecta.

We experimentally studied the predatory behavior of Polybia rejecta (Vespidae, Polistinae, Epiponini) towards 2-88 mm-long insects attracted to a UV light trap. Foragers, which began to hunt at 6:30, selected 4-14 mm-long prey insects. Prey detection by sight by hovering wasps was confirmed using decoys. After the wasps landed and walked along a sinuous path, prey were detected by contact or from a distance (1-3cm). This was followed by seizure, stinging (contrarily to most other known cases), prey manipulation and retrieval. Prey that flew off might be caught in flight. The prey load, representing 30.7% of a forager's weight, was optimized by capturing up to six small prey or two medium-sized prey successively (both of which might be consumed in situ). The foragers cut off the wings of larger prey or cut them into two pieces and returned to gather the second piece. The handling time increased exponentially with the weight of the prey. Partial loading (i.e., retrieving a load much inferior to the maximum possible) was likely related to social facilitation, a form of nest-based recruitment that was demonstrated through the experimental elimination of local enhancement by removing foragers (both mechanisms favor the exploitation of favorable patches).

Ant-lepidopteran associations along African forest edges.

Working along forest edges, we aimed to determine how some caterpillars can co-exist with territorially dominant arboreal ants (TDAAs) in tropical Africa. We recorded caterpillars from 22 lepidopteran species living in the presence of five TDAA species. Among the defoliator and/or nectarivorous caterpillars that live on tree foliage, the Pyralidae and Nymphalidae use their silk to protect themselves from ant attacks. The Notodontidae and lycaenid Polyommatinae and Theclinae live in direct contact with ants; the Theclinae even reward ants with abundant secretions from their Newcomer gland. Lichen feeders (lycaenid; Poritiinae), protected by long bristles, also live among ants. Some lycaenid Miletinae caterpillars feed on ant-attended membracids, including in the shelters where the ants attend them; Lachnocnema caterpillars use their forelegs to obtain trophallaxis from their host ants. Caterpillars from other species live inside weaver ant nests. Those of the genus Euliphyra (Miletinae) feed on ant prey and brood and can obtain trophallaxis, while those from an Eberidae species only prey on host ant eggs. Eublemma albifascia (Erebidae) caterpillars use their thoracic legs to obtain trophallaxis and trophic eggs from ants. Through transfer bioassays of last instars, we noted that herbivorous caterpillars living in contact with ants were always accepted by alien conspecific ants; this is likely due to an intrinsic appeasing odor. Yet, caterpillars living in ant shelters or ant nests probably acquire cues from their host colonies because they were considered aliens and killed. We conclude that co-evolution with ants occurred similarly in the Heterocera and Rhopalocera.