Elsevier

Ecological Indicators

Volume 119, December 2020, 106839
Ecological Indicators

Desiccation resistance traits predict freshwater invertebrate survival and community response to drought scenarios in a Neotropical ecosystem

https://doi.org/10.1016/j.ecolind.2020.106839Get rights and content

Highlights

  • Median lethal time (LT50) is a measure of sensitivity to desiccation stress.

  • LT50 of tropical freshwater invertebrates ranged from 4.18 to 19.06 days.

  • LT50 is predicted by desiccation-resistance traits, cuticle content and dry body mass.

  • LT50 predicts community response to various drought intensities in nature.

Abstract

The intensification of dry seasons is a major threat to freshwater biodiversity in Neotropical regions. Little is known about resistance to drying stress and the underpinning traits in Neotropical freshwater species, so we don’t know whether desiccation resistance allows to anticipate shifts in biological diversity under future climate scenarios. Here, we used the aquatic invertebrates that live in the rainwater-filled leaves of tank bromeliads, to examine the extent to which desiccation resistance of species measured in the laboratory predicts community response to drought intensification in nature. We measured desiccation resistance in 17 invertebrate species (>90% of the biomass usually found in bromeliads of French Guiana) by recording the median lethal time (LT50) of experimental populations exposed to controlled conditions of residual moisture. In the field, we placed rainshelters above tank bromeliads to emulate drought scenarios ranging from the ambient norm to IPCC scenarios and extreme events, and we recorded the response of functional community structure. LT50 ranged from 4.18 to 19.06 days, and was related to cuticle content and dry body mass. Among other functional indicators that represent strategies to optimize resource use under stressful conditions (e.g., habitat use, trophic specialization), LT50 was the best predictor of community structure responses along a gradient of emulated drought intensities. Therefore, species’ LT50s measured under laboratory conditions can be used to forecast aquatic community response to drying stress in nature. Anticipating how species will cope with drought has never been more important for environmental managers to support climate change adaptation. We show that desiccation resistance in freshwater invertebrates is a key indicator of potential population size and local–global range shifts, and this could be especially true in the Neotropics where species have narrow physiological tolerances for climatic variation.

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

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    These two authors contributed equally.

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