SPECIAL FEATURE: PERSPECTIVE Biology in the Anthropocene: Challenges and insights from young fossil records Susan M. Kidwell1 Department of the Geophysical Sciences, University of Chicago, Chicago, IL 60637 Edited by Neil H. Shubin, University of Chicago, Chicago, IL, and approved February 6, 2015 (received for review July 6, 2014) With overwhelming evidence of change in habitats, biologists today must assume that few, if any, study areas are natural and that biological variability is superimposed on trends rather than stationary means. Paleobiological data from the youngest sedimentary record, including death assemblages actively accumulating on modern land surfaces and seabeds, provide unique information on the status of present-day species, communities, and biomes over the last few decades to millennia and on their responses to natural and anthropogenic environmental change. Key advances have established the accuracy and resolving power of paleobiological information derived from naturally preserved remains and of proxy evidence for environmental conditions and sample age so that fossil data can both implicate and exonerate human stressors as the drivers of biotic change and permit the effects of multiple stressors to be disentangled. Legacy effects from Industrial and even pre-Industrial anthropogenic extirpations, introductions, (de)nutrification, and habitat conversion commonly emerge as the primary factors underlying the present-day status of populations and communities; within the last 2 million years, climate change has rarely been sufficient to drive major extinction pulses absent other human pressures, which are now manifold. Young fossil records also provide rigorous access to the baseline composition and dynamics of modern-day biota under pre-Industrial conditions, where insights include the millennial-scale persistence of community structures, the dominant role of physical environmental conditions rather than biotic interactions in determining community composition and disassembly, and the existence of naturally alternating states. biodiversity | ecology | conservation | paleobiology | paleoecology The Anthropocene is an informal term that is “anthromes” (15). The human footprint in shifting baselines syndrome,seeref.31)(Fig.1). gaining wide currency for the present epoch marine settings has been more difficult to These realizations also suggest (iii)thatmany of Earth’shistory,whenhumansdominatea evaluate because these areas are further from analytical subjects—species and populations, majority of natural processes globally (1, 2). direct observation, but seasonal hypoxia communities and habitats, landscapes and The biological effects of climate change re- linked to the runoff of cultural nutrients gradients, ecosystems and nutrient cycles— ceive the greatest attention (3–6): secular occurs in all oceans and at more than 400 may well be in disequilibrial states, a funda- warming, ocean acidification, and novel pre- sites globally, having doubled each decade mental challenge to experimentation, modeling, cipitation patterns are now pervasive (7, 8) since the 1960s (26), and 32–57% of the and prediction. Ecologists and conservation (Fig. 1). However, many other human pres- world’s fisheries are assessed as overex- biologists increasingly recognize that unex- — sures most particularly nutrification, habitat ploited or collapsed, with the remainder pected relationships and outcomes often conversion, and the overexploitation and in- fully exploited (14). Both terrestrial and emerge as study durations exceed a decade, — troduction of species also intensified with marine biologists now speak of a historically that directional change in climate and other “ ” the expansion of human populations and cumulative Anthropocene defaunation, environmental factors can compromise ex- technology during the Industrial Revolution a concept that includes many kinds of eco- perimental controls, and that most field “ – and the post-World War II Great Accelera- logical disruption (e.g., refs. 27 30). More experiments incorporate legacy effects, such ” tion (2,4,17,18)andareequallyrelevantto biological changes are almost certainly as species depletion or habitat change, that conservation and restoration efforts, as well locked into place, much as additional de- are only later appreciated (e.g., refs. 32–34). as to basic ecological research. These pres- cades of warming are inevitable from cur- ThethesisofthisPerspectiveisnotsimply sures, moreover, started much earlier during rent levels of atmospheric CO2. that historical data of many types are needed, preceding centuries to millennia at regional For biologists now fully embedded in the but that (i) the power of young fossil records Anthropocene, the disconcerting working scales, both on land and in coastal seas, and to contribute critical data has been trans- have been accompanied by biological-stress assumptionsmustbethat(i)anyareaor formed in the last few decades by three syndromes (19), such as decreased body size, biota under study today is not fully natural, revolutions in the earth sciences and (ii)paleo- population size, trophic levels, and diversity, given current human stresses and legacies of biologic analysis of records from the last as well as functional and complete extinction past stress, and (ii) interannual to -decadal few centuries and millennia is already chal- of species (14, 20–24). These nonclimate fac- variability is probably superimposed upon a lenging our understanding of ecological dy- tors are now as global as climate change trend rather than a stationary mean. These namics and contributing to conservation, (Fig. 1). realizations underscore the arbitrary nature Today, even lakes in remote, high-altitude of most proposed ecological baselines, which restoration, and management efforts in a and -latitude settings receive atmospheric are often defined by the first scientific obser- deposition of nitrates from industrial fertil- vations (usually from the early 20th century, Author contributions: S.M.K. wrote the paper. izers(16,25),andmorethanhalfofallland at best), by the oldest digitized records (1980s The author declares no conflict of interest. area inclusive of the Arctic has been con- or younger), or by the personal experience of This article is a PNAS Direct Submission. verted to range, crop, or densely settled a scientist or manager (for discussion of the 1Email: [email protected]. 4922–4929 | PNAS | April 21, 2015 | vol. 112 | no. 16 www.pnas.org/cgi/doi/10.1073/pnas.1403660112 Downloaded by guest on October 2, 2021 Satellites, sensors PERSPECTIVE Regulatory biomonitoring andlongertimeframesthatencompasssus- Quant. ecology, fishery science -------- Biological pected natural and anthropogenic drivers. SPECIAL FEATURE: Economic reports ---------- data sources Journals, surveys ------- Fully anchored sclerochronogies Three Revolutions in the Earth Sciences Fully anchored tree-ring chronologies Paleobiological Seabed, landscape death assemblages That Have Transformed the Power of the Ancient DNA data sources Sediments with fossils (& archeological evidence) Fossil Record .... ‘Anthropo .... cene’ Pliocene Pleistocene Holocene (future) Fidelity of (Paleo)biological Information. Terrestrial ‘anthromes’ The first-order concern with all geohistorical biomes: semi-natural wild records—ice cores, tree-rings, sediment cores, Anthropogenic 250 and biological remains in both natural and N input: 2 0 archeological contexts—is their fidelity, or Non-climate collapsed + Regional over-exploited stressors: Fisheries: depletions developing fully exploited faithfulness, to the original signal. Over the 4 Phases of 1° human expansion; 2° EU exploration, 3° global past two decades, taphonomic research on ‘Sixth Exinction’: megafauna + islands colonization markets Δ Temp °C postmortem processes has dramatically in- H. sapiens 2 Technology: Neolithic Revolution Industrial Revolution Great Acceleration hunt-gather agric., settlement mech. agric. & fishing in all stresses creased the kinds of biological information that can be confidently extracted from fossil Lifespan of child born today specimens, especially from the durable tissues 8.2 -2 thataremostlikelytobepreservedunderthe Ocean pH: 8.0 more or less oxygenated conditions of soils, caves, lake floors, and seabeds (shells, bones, 7.8 pollen, and other biomineralized or refractory BCE CE 1850 1900 1950 2000 2050 2100 organic tissues). Ancient DNA (aDNA) anal- 543 21500 250 10 5 2 1 -100 -50 0 +50 +100 +150 ysis can now exploit a larger array of materials Million Yrs BP Thousand Yrs BP Years before (-) or after (+) 1950 CE and preservational settings than previously Fig. 1. Historical trends in environmental conditions and technology over the last 5 million years, culminating in the assumed, with a temporal scope to 1 Ma Anthropocene, when human activities achieved a global signature. Most biological data (Top) are from studies con- (million years ago) and full paleo-genomes ducted after World War II, and thus short-term variability has occurred in the context of trends rather than stationary now within reach (42). Diet, home range, means in climate, nutrients, and other human pressures. The deeper historical reach of paleobiological data challenge assumptions of stability and equilibrium and show that many populations, species, communities, and biomes had growth rate, and other life-history information undergone significant changes in abundance, structure, and function at regional scales well before the mid-20th are