Thermal niches of planktonic foraminifera are static throughout glacial–interglacial climate change

Abiotic niche lability reduces extinction risk by allowing species to adapt to changing environmental conditions in situ. In contrast, species with static niches must keep pace with the velocity of climate change as they track suitable habitat. The rate and frequency of niche lability have been studied on human timescales (months to decades) and geological timescales (millions of years), but lability on intermediate timescales (millennia) remains largely uninvestigated. Here, we quantified abiotic niche lability at 8-ka resolution across the last 700 ka of glacial–interglacial climate fluctuations, using the exceptionally well-known fossil record of planktonic foraminifera coupled with Atmosphere–Ocean Global Climate Model reconstructions of paleoclimate. We tracked foraminiferal niches through time along the univariate axis of mean annual temperature, measured both at the sea surface and at species’ depth habitats. Species’ temperature preferences were uncoupled from the global temperature regime, undermining a hypothesis of local adaptation to changing environmental conditions. Furthermore, intraspecific niches were equally similar through time, regardless of climate change magnitude on short timescales (8 ka) and across contrasts of glacial and interglacial extremes. Evolutionary trait models fitted to time series of occupied temperature values supported widespread niche stasis above randomly wandering or directional change. Ecotype explained little variation in species-level differences in niche lability after accounting for evolutionary relatedness. Together, these results suggest that warming and ocean acidification over the next hundreds to thousands of years could redistribute and reduce populations of foraminifera and other calcifying plankton, which are primary components of marine food webs and biogeochemical cycles.

Abiotic niche dynamics determine patterns of community composition over space and regulate trajectories of diversity over time (1). Both niche lability (2, 3) and conservatism (1, 4) have been proposed to spur speciation, and abiotic niche lability has been associated with ecological invasions (5–7) and with reduced risk of extinction during times of climate change (8). Thus, a deeper understanding of species’ propensity for niche stasis versus lability could improve predictions of biodiversity restructuring in response to anthropogenic climate change (9).Stasis in species’ abiotic niches through time has been documented in empirical research, but most such studies have been limited to ecological niche modeling on decadal scales (reviewed in ref. 10) or paleoecological examination on 10⁶ to 10⁷ y scales (5, 11, 12). Since empirical rates of niche change are scarce and difficult to acquire, many studies merely assume that niche evolution occurs at a constant rate along branches of a phylogeny (2, 3, 6, 7). Niche dynamics at intermediate timescales of centuries to millennia are particularly poorly documented (10), and studies at this meso scale have been restricted to terrestrial systems (e.g., refs. 13–15) or to comparisons between the present day and the single historical time step of the Last Glacial Maximum, ∼21 ka (16–20). Quantifying the rate and relative frequency of niche change in marine species over timescales of 10² to 10⁵ years is important, however, because species will adapt or go extinct in response to anthropogenic ocean changes over this timescale (21).Here, we investigated climatic niche lability from the rich sedimentary archive of global planktonic foraminifera across the last 700 ka of glacial–interglacial cycles at 8-ka resolution. Planktonic foraminifera (Protista) construct “shells” (tests) of calcite, thereby sequestering carbon and recording an isotopic signature of past ocean conditions. Tests readily accumulate over large expanses of the seafloor. Consequently, the fossil record of foraminifera—arguably “the best fossil record on Earth” (22)—affords an exceptionally high-resolution view into past species distributions. This detailed record fuels studies of biostratigraphy, paleoclimatology, and paleoecology (20, 22–25). Moreover, the complete species diversity of planktonic foraminifera has been described for the Plio–Pleistocene, with good agreement between morphological and molecular phylogenies (22, 25–27). Although some have speculated that foraminifera competitively exclude each other (24), recent work found that planktonic foraminifera species seldom restrict each other’s distributions (28). Presumably, therefore, species occupy the full envelope of existing environmental conditions within their tolerance limits, and geographic distributions are determined almost entirely by physical ocean conditions.We developed five analyses to investigate the degree of abiotic niche lability in foraminifera. All methods examined the univariate niche axis of temperature, which is the single most important explanatory variable in regard to geographic distributions of foraminifera (20, 29–32) and is a climate-related stressor and extinction driver for diverse marine fauna across timescales (33, 34). The adaptive potential of thermal niches has been taken as a key determinant of global community structure and genetic connectance in plankton (35). Primary productivity and other environmental variables, however, may also structure abiotic niches of plankton (36). Our suite of analyses quantified whether and by how much planktonic foraminiferal niches shifted along a temperature axis. First, we correlated time series of species’ thermal optima with global temperature to determine whether species tracked suitable habitat or experienced environmental fluctuations in situ. We then quantified species’ niche dissimilarity between pairs of time bins—either tracking niches across bin boundaries or contrasting niches at climatic extremes of glacial maxima and interglacial thermal peaks. To characterize niche change we applied trait evolution models to time series of temperatures at occupied sites. Lastly, we explored variation in intraspecific niche lability among ecotypes while accounting for phylogenetic relatedness. SI Appendix, Table S1 lists the response variable and sample size for each analysis.