Clustered warming tolerances and the nonlinear risks of biodiversity loss on a warming planet

Abstract

Anthropogenic climate change is projected to become a major driver of biodiversity loss, destabilizing the ecosystems on which human society depends. As the planet rapidly warms, the disruption of ecological interactions among populations, species and their environment, will likely drive positive feedback loops, accelerating the pace and magnitude of biodiversity losses. We propose that, even without invoking such amplifying feedback, biodiversity loss should increase nonlinearly with warming because of the non-uniform distribution of biodiversity. Whether these non-uniformities are the uneven distribution of populations across a species' thermal niche, or the uneven distribution of thermal niche limits among species within an ecological community, we show that in both cases, the resulting clustering in population warming tolerances drives nonlinear increases in the risk to biodiversity. We discuss how fundamental constraints on species' physiologies and geographical distributions give rise to clustered warming tolerances, and how population responses to changing climates could variously temper, delay or intensify nonlinear dynamics. We argue that nonlinear increases in risks to biodiversity should be the null expectation under warming, and highlight the empirical research needed to understand the causes, commonness and consequences of clustered warming tolerances to better predict where, when and why nonlinear biodiversity losses will occur.This article is part of the discussion meeting issue 'Bending the curve towards nature recovery: building on Georgina Mace's legacy for a biodiverse future'.

Keywords: biodiversity loss; climate change; global change; thermal limit; thermal safety margin; tipping point.

Figure 1.

The nonlinear inundation of a beach as the tide gradually rises provides an analogy for how risks to biodiversity can accelerate under steady climate warming. At time point 0 (a) B ₀ denotes the initial extent of the beach while T ₀ denotes the initial sea level. At time point 1 (b) sea levels have risen by a set amount to T ₁, but only a small area of the beach is flooded (B ₀ − B ₁). At time point 2 (c) sea levels have risen by the same amount again, but larger areas of beach have been inundated (B ₁ - B ₂ » B ₁ −B ₀). While here we use the nonlinear increase in the area at risk from the rising tide as an analogy, the exposure of biodiversity [33] and human populations [34] to rising sea levels could represent a real example of accelerating risk under climate change without invoking any feedback loops. This is because most land area, and therefore terrestrial wildlife and human populations, are concentrated at low elevations.

Figure 2.

Examples of the risk of nonlinear biodiversity responses to temperature at different scales of biological organization. Frequency distribution of (a) current sea surface temperatures across the geographical distribution of the coral Pectinia pygmaea [35], (b) critical thermal limits (maxima) of dung beetle species within a tropical forest assemblage [36], (c) leaf temperatures through time within a tropical forest tree [37], and (d) global warming levels at which biological and physical tipping elements in major Earth systems are at risk of being triggered [38]. Red lines denote the corresponding cumulative distributions, showing the nonlinear increase in the percentage of biological units exposed to temperatures beyond their thermal limits as the climate warms. Red lines are nonlinear owing to (a,c) the clustering of biological units that share the same thermal limit across a temperature gradient or (b,d) the clustering of thermal limits of biological units (and physical units in (d)). Graphs (a,b) demonstrate the nonlinear risk posed by clustered warming tolerances to a species across its geographical range and across species within an ecological community, respectively, and are the focus of this manuscript. In all cases (a–d), nonlinear risks are driven by clustered warming tolerances (i.e. the magnitude of warming before a biological unit—be that a population, a species within an assemblage, an organ within an individual, or a major Earth system—is committed to collapse). For ease of visualization, in (a,c) the temperature axis is reversed (i.e. warmer temperatures on the left) so that in all panels cumulative risk increases from left to right with warming. Tree silhouette image credit is given to T. Michael Keesey from a photo by Bernard Dupont (licence https://creativecommons.org/licenses/by-sa/3.0/).

Figure 3.

Ecological and evolutionary responses could mediate nonlinear increases in the risks of biodiversity loss. Grey lines denote the null expectation arising from clustered warming tolerances that are caused by geographical or physiological constraints. Black lines denote possible expectations for risk after including various ecological and evolutionary responses of populations to thermal exposure. Arrows indicate how risk changes. Abrupt responses can be (a) delayed (e.g. phenological plasticity delays the collapse of great tit (Parus major) populations owing to phenological plasticity [97]) or (b) advanced (e.g. in Drosophila, thermal limits for sperm are typically lower than for adults, causing risk to be underestimated if adult physiology is used to predict warming tolerances [98]). The abruptness of biodiversity responses can be (c) tempered (e.g. population thermal limits differ between sympatric mammal and bird species in the Mojave Desert owing to microhabitat use [99]) or (d) intensified (e.g. local adaptation of Daphnia magna to temperature variation across its latitudinal range causes reduced variation in warming tolerances [100]).

Figure 4.

Without local adaptation in individual upper thermal limits (a) the population warming tolerances of a species will be greatest at the cold margin of their geographical range (e.g. at high latitudes). However, if populations are locally adapted to their thermal environment (b), warming tolerances will show little variation over the geographical range of a species. These clustered warming tolerances indicate that if the climate warms at the same rate everywhere, a locally adapted species will experience a more abrupt loss of populations over time, without invoking feedback loops or synchronous extreme weather events across the range.