Desiccation resistance traits predict freshwater invertebrate survival and community response to drought scenarios in a Neotropical ecosystem
Introduction
Drought is currently a major threat to biodiversity and ecosystem functioning (IPCC, 2013; Srivastava et al. 2020a), notably in tropical regions where a decrease in water availability is expected to exacerbate extinctions (Hugueny et al., 2011, Oberdorff et al., 2015). Understanding and anticipating how species will cope with droughts has never been more important as the urgency to better predict future ecosystem functioning grows. The autecology of species and the resulting trait-based framework could provide relevant functional indicators for scientists to predict individual- to ecosystem-level responses to climate change, and for environmental managers to implement climate change adaptation plans (Dias et al., 2013, Piano et al., 2019, Wieczynski et al., 2019, Schleuning et al., 2020). The rationale is that the physiological, biological, behavioural, and ecological attributes of species directly describe their interactions with the biotic and abiotic environment (Wilman et al., 2014). In particular, species responses to drought events depend both on physiological tolerance and resistance to desiccation (Pallarés et al., 2016), and on behavioural traits such as avoidance or migration to refuge microhabitats that trigger rapid responses to unsuitable conditions (Dézerald et al., 2015, Strachan et al., 2015). Assuming however that physiological limitations are the most fundamental constraints on species distributions across spatial scales (Kearney and Porter, 2009, Start et al., 2018), traits that confer physiological tolerance and/or resistance to desiccation stress could be among the best indicators of biodiversity responses to drought across ecosystems and regions of the tropics (Chown, 2012).
Invertebrates contribute disproportionately to the biodiversity of tropical regions, where they play significant roles in multi-trophic processes and ecosystem functions (Ewers et al., 2015). The desiccation tolerance of invertebrates (ability to withstand body water loss) depends on the body water content, which influences water loss dynamics (Thorat and Nath, 2018). Desiccation resistance (ability to reduce water loss) is rather related to body size and integumental permeability (Dias et al., 2013, Pallarés et al., 2017). Compared to their temperate counterparts, the invertebrates found in tropical rainforests are expected to have low tolerance-resistance to desiccation because they thrive in relatively stable conditions of habitat humidity or hydrology (Gibbs and Matzkin, 2001, Hoffmann et al., 2003). Yet, traits underpinning sensitivity to drought among coexisting species and the consequences at community level remain poorly documented, notably in freshwaters where responses to drying stress play a primary role in the distribution of species at multiple spatial scales (Datry et al., 2014, Pallarés et al., 2016). Theory about local adaptation suggests that tolerance and resistance traits could allow species to withstand modest to average drought intensities at the active stage (Lake, 2011). Nevertheless, once drought intensifies, reconfigurations of communities could occur if co-existing species were to respond asynchronously to desiccation stress. These assumptions remain however untested, first because we lack established relationships between species’ desiccation tolerance-resistance traits and survival to drought in tropical rainforests (see review in Thorat and Nath, 2018), and second because we don’t know which trait combinations are selected (or counter-selected) along a gradient of increasing drought intensity in these ecosystems.
Assembling data on trait variation among coexisting species in rivers, lakes or wetlands is however challenging, because of their very high taxonomic diversity. Natural microcosms that host smaller numbers of co-evolved species in contained habitats form relevant alternatives to test ecological hypotheses (Kitching, 2000, Srivastava et al., 2004). Here, we focused on the aquatic invertebrates inhabiting tank bromeliads, a discrete ecosystem that is commonly found across a wide array of Neotropical environments. Bromeliads are flowering plants represented by 3403 species native to the Neotropics (Ulloa et al., 2017). The leaves of tank-forming bromeliads are arranged in rosettes that trap water, forming “freshwater islands” in a terrestrial matrix. Tank bromeliads collect rainwater and detritus, providing a habitat for aquatic organisms ranging from bacteria to macroinvertebrates. Detailed descriptions of the bromeliad macroinvertebrate fauna and functional traits can be found in Frank and Lounibos, 2009, Céréghino et al., 2018.
To the best of our knowledge, there is nothing in the published literature about time to death of freshwater invertebrate species submitted to standardized drying stress in tropical ecosystems, so we don’t know whether upscaling species’ lethal times at community level allows to anticipate shifts in community structure under future climate scenarios. Growth rates measured under controlled hydrology have been used as a proxy to sensitivity to drought of Neotropical aquatic insects (Amundrud and Srivastava, 2015). Although this approach allows to rank species by sensitivity, it does not tell us how long species can withstand absence of water, what traits predict time to death, and what drought intensity coexisting invertebrates can survive within the range of current to predicted climate scenarios. This study was designed to address these issues. Our experiments took place in French Guiana, the epicentre of bromeliad radiation and a hotspot of biodiversity for bromeliad invertebrates. First, we established species-specific sensitivity to drought as the median lethal time (LT50) of experimental populations under controlled conditions of residual moisture in the laboratory. We examined which morphological and anatomical attributes forming desiccation tolerance and resistance traits (e.g., water content, cuticle content, body length, etc.) predict LT50. Second, in order to test whether species-specific LT50s measured in the laboratory predict community response to drought in nature, we used rainshelters placed above tank bromeliads to emulate drought scenarios ranging from ambient conditions to IPCC scenarios and extreme events in a field experiment, and we recorded the response of functional community composition to these treatments. We upscaled LT50 (this study) as well as ecological traits that describe the life history strategies of species (after Céréghino et al., 2018) at community level, to explore co-variation between drought intensity and traits constrained by the abundance of invertebrate species. We therefore asked: what traits indicate sensitivity to drought in Neotropical aquatic invertebrates, and specifically, does desiccation resistance of species measured under standardized laboratory conditions predict aquatic community response to drought in nature?
Section snippets
Study area
This study was carried out in French Guiana from October 2018 to April 2019, near the Petit-Saut Dam, Sinnamary (5°03043″N, 53°02046″W; elevation < 80 m a.s.l.; Fig. 1). French Guiana is an overseas region of France located on the north-eastern coast of South America. About 96% of its surface area (83.534 km2) is covered by equatorial forest. The climate is tropical moist with 3000 mm of annual precipitation, little seasonal variation in air temperature (monthly average = 20.5–33.5 °C), and a
Lethal times and underpinning traits
Survival curves were significantly and consistently different between the treatments and controls (Gehan-Wilcoxon tests, p < 0.05). A potential “tube effect” on our LT50 estimates was null or negligible, because none of the control populations reached a LT50 within the timeframe of the observations, and mortality in the controls ranged from 0% to <20% of the individuals at the end of the trials. In the drought treatments, LT50 varied from 4.18 to 19.06 days depending on the species (Fig. 2;
Discussion
We found that time to death of bromeliad invertebrates subject to drying stress is determined by desiccation-resistance traits, namely body mass and cuticle content, rather than desiccation-tolerance traits such as body water content. The LT50 of most species varied from 4 to 9 days in the laboratory, and reached 19 days in the ostracod Elpidium bromeliarum, suggesting that the conspicuous plant-held waters of Neotropical forests host drought-resistant invertebrates. Considering future climate
Conclusion
As future climate scenarios predict declines in precipitation in many regions of the world, anticipating how species will cope with drought is of utmost importance for environmental managers to support climate change adaptation. Our study supports the idea that physiology can bridge the gap between ecology and climate change (Kearney and Porter, 2009), under the basic assumption that organisms cannot survive in environments that do not allow them to maintain basic regulatory functions as well
CRediT authorship contribution statement
Régis Céréghino: Conceptualization, Methodology, Investigation, Formal analysis, Writing - original draft, Writing - review & editing, Supervision, Project administration, Funding acquisition. Léa Françoise: Investigation, Data curation, Formal analysis, Writing - original draft, Writing - review & editing. Camille Bonhomme: Investigation, Writing - review & editing. Jean-François Carrias: Conceptualization, Methodology, Investigation, Writing - review & editing, Project administration, Funding
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We acknowledge financial support for research provided by the French Agence Nationale de la Recherche (ANR) through the Resilience project (grant ANR-18-CE02-0015) and an Investissement d’Avenir grant (Labex CEBA, ref. ANR-10-LABX-25-01), by the French Centre National de la Recherche Scientifique (CNRS) through the EC2CO-Biohefect project Proseco, and by the French Fondation pour la Recherche sur la Biodiversité (FRB, CESAB programme) as part of the activities of the FunctionalWebs Working
References (64)
- et al.
Revisiting water loss in insects: a large scale view
J. Insect Physiol.
(2001) - et al.
Physical features and chitin content of eggs from the mosquito vectors Aedes aegypti, Anopheles aquasalis and Culex quinquefasciatus: Connection with distinct levels of resistance to desiccation
J. Insect Physiol.
(2015) - et al.
Water balance of Lake Tana and its sensitivity to fluctuations in rainfall, Blue Nile basin, Ethiopia
J. Hydrol.
(2006) - et al.
Rebuilding community ecology from functional traits
Trends Ecol. Evol.
(2006) - et al.
Effects of dehydration rate on physiological responses and survival after rehydration in larvae of the anhydrobiotic chironomid
J. Insect Physiol.
(2008) - et al.
Clearing and dissecting insects for internal skeletal morphological research with particular reference to bees
Revista Brasileira de Entomologia
(2016) - et al.
Trait-Based Assessments of Climate-Change Impacts on Interacting Species
Trends Ecol. Evol.
(2020) - et al.
Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates
Mar. Environ. Res.
(2012) - et al.
Are natural microcosms useful model systems for ecology?
Trends Ecol. Evol.
(2004) - et al.
Drought sensitivity predicts habitat size sensitivity in an aquatic ecosystem
Ecology
(2015)
Extreme drought pushes stream invertebrate communities over functional thresholds
Glob. Change Biol.
The Invertebrates: A Synthesis
Resistance and resilience of invertebrate communities to seasonal and supraseasonal drought in arid-land headwater streams
Freshwater Biol.
Taxonomic and biological trait differences of stream macroinvertebrate communities between mediterranean and temperate regions: Implications for future climatic scenarios
Glob. Change Biol.
Understory environments influence functional diversity in tank-bromeliad ecosystems
Freshwater Biol.
Desiccation resistance in tropical insects: causes and mechanisms underlying variability in a Panama ant community
Ecol. Evol.
Constraints on the functional trait space of aquatic invertebrates in bromeliads
Funct. Ecol.
Ants mediate the structure of phytotelm communities in an ant-garden bromeliad
Ecology
Ecological Niches: Linking Classical and Contemporary Approaches
Trait-based approaches to conservation physiology: forecasting environmental change risks from the bottom up
Phil. Trans. R. Soc. B
Drying determines the temporal dynamics of stream invertebrate structural and functional beta diversity
Ecography
Broad-scale patterns of invertebrate richness and community composition in temporary rivers: effects of flow intermittence
Ecography
Functional trait responses of aquatic macroinvertebrates to simulated drought in a Neotropical bromeliad ecosystem
Freshwater Biol.
Environmental drivers of invertebrate population dynamics in Neotropical tank bromeliads
Freshwater Biol.
Tank bromeliads sustain high secondary production in neotropical forests
Aquat. Sci.
Traits underpinning desiccation resistance explain distribution patterns of terrestrial isopods
Oecologia
Combining the fourth-corner and the RLQ methods for assessing trait responses to environmental variation
Ecology
Logging cuts the functional importance of invertebrates in tropical rainforest
Nat. Commun.
Desiccation resistance: effect of cuticular hydrocarbons and water content in Drosophila melanogaster adults
PeerJ
Insects and allies associated with bromeliads: a review
Terr. Arthrop. Rev.
Global warming-accelerated drying in the tropics
PNAS
Evolution of water balance in the genus Drosophila
The J. Exp. Biol.
Cited by (7)
Functional trait dataset of benthic macroinvertebrates in South Korean streams
2023, Scientific DataPrevious stress causes a contrasting response to cadmium toxicity in the aquatic snail Potamopyrgus antipodarum: lethal and behavioral endpoints
2023, Environmental Science and Pollution ResearchLack of congruence between fundamental and realised aridity niche in a lineage of water beetles
2022, Freshwater Biology
- 1
These two authors contributed equally.