Palaeontology
rsbl.royalsocietypublishing.org
Understanding modern extinctions in marine ecosystems: the role of palaeoecological data
Opinion piece
Matthew A. Kosnik1 and Michał Kowalewski2 1
Cite this article: Kosnik MA, Kowalewski M. 2016 Understanding modern extinctions in marine ecosystems: the role of palaeoecological data. Biol. Lett. 12: 20150951. http://dx.doi.org/10.1098/rsbl.2015.0951
Received: 13 November 2015 Accepted: 8 March 2016
Subject Areas: ecology, palaeontology, environmental science Keywords: palaeobiology, palaeoecology, conservation palaeobiology, Holocene, marine ecosystems, death assemblages
Author for correspondence: Matthew A. Kosnik e-mail: [email protected]
An invited contribution to the special feature ‘Biology of extinction: inferring events, patterns and processes’. Electronic supplementary material is available at http://dx.doi.org/10.1098/rsbl.2015.0951 or via http://rsbl.royalsocietypublishing.org.
2
Department of Biological Sciences, Macquarie University, Sydney, New South Wales 2109 Australia Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA MAK, 0000-0001-5380-7041; MK, 0000-0002-8575-4711 Because anthropogenic impacts on ecological systems pre-date the oldest scientific observations, historical documents and archaeological records, understanding modern extinctions requires additional data sources that extend further back in time. Palaeoecological records, which provide quantitative proxy records of ecosystems prior to human impact, are essential for understanding recent extinctions and future extinction risks. Here we critically review the value of the most recent fossil record in contributing to our understanding of modern extinctions and illustrate through case studies how naturally occurring death assemblages and Holocene sedimentary records provide context to the plight of marine ecosystems. While palaeoecological data are inherently restricted censuses of past communities (manipulative experiments are not possible), they yield quantitative records over temporal scales that are beyond the reach of ecology. Only by including palaeoecological data is it possible to fully assess the role of long-term anthropogenic processes in driving modern extinction risk.
1. Millennial scale context of extant ecological systems Palaeoecological data, despite their shortcomings, can provide multi-millennial ecological records required to contextualize modern extinctions [1 –5] and thus complement other types of data used to assess extinctions and extinction risks. While real-time instrumental records are the highest precision records and quantitative ecological research is best able to test mechanisms, their temporal scope is inadequate ([1], figure 1). Written records of exploitation deliver priceless insights further back in time, but they are typically qualitative [2]. Zooarchaeological data represent critical records of human harvesting activities [3]. By contrast, palaeoecology integrates biological, sedimentary and geochemical records to derive diverse quantitative data about ecological systems prior to, as well as during, human occupation and impact [4,5,7]. Palaeoecological research alone cannot completely document human-driven ecological changes because it relies primarily on restricted census data types (figure 1) and unlike written historical and midden records, palaeoecological research only correlates ecological changes with changing human activities. Ecological studies can take advantage of real-time instrument records and experimental manipulations to enable mechanistic understandings of ecological changes. Consequently, quantifying anthropogenic impacts necessitates a holistic approach—a synthesis of ecological, historical, archaeological and palaeoecological data—that provides more realistic assessments of anthropogenic changes and modern extinction risks (figure 1). Only then can we separate extinctions due to human impacts from those likely driven by natural causes. Of note, deep-time palaeobiological studies are becoming increasingly relevant for assessing current extinction risks (e.g. [8]). However, such studies represent macroevolutionary
& 2016 The Author(s) Published by the Royal Society. All rights reserved.
2 real time instrument restricted census quantitative
written records
IUCN Red List
middens
6000 10000
50000 1 × 105 2 × 105
Pleistocene
20000
Late Modern Early Modern Medieval Local Market–Classical cores / excavations
Breeding Bird Surveys
PGE / eLTER
HBR / LTER / NEON
temperature
sea level
1500 600 0 900
Late Global Early Global
death assemblages
1800
Continuous Plankton Recorder
1950 1900
Holocene
temporal extent (years BC/AD)
2000
Agricultural
Hunter–gatherer
Figure 1. The characteristics and temporal coverage for different data types in the context of human cultural development. Record types are scored as dominantly of that category (black), some of that category (grey), or typically not of that category (white). The y-axis is log-transformed even though this visually exaggerates the temporal extent of instrumental and experimental records. Anthropogenic time intervals based on Lotze et al. [6]. While real-time instrumental and experimental records are the most precise, they are the most spatially and temporally restricted. The longest direct records of physical phenomena extend back only into the ‘Early/ Late Modern’ time interval. These records include atmospheric carbon dioxide, sea level and continuous temperature records (bar width: first continuous record, global records, satellite data). Ecological experiments rarely extend beyond the ‘Late Global’ time interval. The Long-Term Ecological Research (LTER) and LTER-Europe (eLTER) programs illustrate the investment in LTER programs in the last few decades. These are expanded from Hubbard Brook (HBR) and the Park Grass Experiment (PGE), which are the longest running ecological experiments. Explicitly ecological data vary widely, but most are spatially and taxonomically restricted censuses with biases associated with the sampling methodology used. Direct observations including the Breeding Bird Survey and Continuous Plankton Recorder programs are the longest continuous ecological observations. The IUCN Red List is extended back as a finer line to reflect extinctions documented through historical data. Archaeological records from middens and historical writing are less resolved and temporally and spatially discontinuous, but extend further back in time. Palaeoecological records are temporally discontinuous, but are spatially widespread and extend back over the entire duration of human history and beyond. The width of the bars reflects the relative commonness and abundance of those data during those time periods. This plot reflects primarily western European and North American datasets, but the source code is provided as supplemental material to facilitate the creation of regional versions (see the electronic supplementary material for additional detail). (Online version in colour.) approaches fundamentally different from those discussed here. Near Recent palaeoecological records are particularly valuable as they typically contain extant, albeit locally or regionally extirpated, species in an essentially modern geographical and environmental context. While humans occupied continents and substantially impacted faunas and floras prior to Western colonization and industrialization (Medieval/Early Modern and Early/Late Modern transitions in figure 1), these represent substantial increases in anthropogenic pressures exerted on biological populations (e.g. [2,6]). Here we outline opportunities afforded by Recent palaeoecological data (i.e. surficial death assemblages
and buried Late Quaternary sedimentary records) when assessing extinction risk in the context of human cultural development. We also outline some of the challenges in using these records for assessing extinction risk.
2. Recent palaeoecological records (a) Naturally occurring shell assemblages sampled from surface sediment Surficial accumulations of biomineralized skeletal material, or death assemblages, represent globally available historical
Biol. Lett. 12: 20150951
atmospheric CO2
2015
rsbl.royalsocietypublishing.org
data type
manipulative experiments
Sediment cores are increasingly recognized as valuable archives of past ecosystems. For example, cores were used effectively to document the role of fisheries in the decline of Tasmanian molluscan communities. The threefold decline in diversity and fourfold decline in abundance of molluscs observed in cores closely mirrored fishery activities in space and time, while actively harvested species declined relatively more abruptly [15]. While fishing and direct exploitation are linked to the decline of Tasmanian molluscs [15], introduced species have played an equally important role in reshaping these coastal marine systems, with 83% of live molluscan biomass collected in 1997– 1999 belonging to introduced taxa [16]. While harvesting rarely drives marine species to extinction, the indirect impacts of fishing, introduced species, and other anthropogenic impacts have the potential to drive species locally if not regionally extinct [16]. To the extent that marine protected areas (MPAs) can represent control sites, most Tasmanian MPAs have existed for fewer than 20 years
3. Key challenges (a) Preservation and sampling Palaeoecological data are subject to taphonomic biases associated with fossilization. Most obviously, organisms with robust skeletons typically yield more fossil remains than those without. However, taphonomy is just a special case of sampling bias. All data-gathering techniques have biases, and some taxa may be over/under represented by different sampling/observation techniques (e.g. [21,22]). As with ecological sampling, a species’ absence may reflect its true absence during the sampling period or the failure of a particular sampling methodology to sample it. A variety of commonly used methods can control for such sampling effects, and taphonomic processes are increasingly well understood (see [5,7,21,23] and references therein).
(b) Chronology and time-averaging While Holocene sediments enclosing fossils can be dated using a number of methods, using sedimentary dates implicitly assumes that fossils and sediments are coeval. Even when this is the case for the median fossil age, sediment derived ages cannot estimate the variance around the median age, termed time-averaging, which quantifies the time over which the fossils accumulated (e.g. [23,24]). Time-averaging can be quantified by numerical dating of individual fossils. Advances in amino acid racemization, carbon-14 and uranium–thorium disequilibrium dating have significantly reduced the costs, making it possible to date hundreds rather than a handful of specimens (see [7,18,23,24] and references therein). Estimates of time-averaging are critical when comparing palaeological to ecological data, so the differences in the timespan of sampling and temporal resolution of resulting data can both be assessed. For example, the above-mentioned River Colorado delta study [9] quantified time-averaging and corrected palaeoecological estimates of productivity to allow direct comparisons with ecological surveys of the modern fauna.
3
Biol. Lett. 12: 20150951
(b) Cores, excavations and buried palaeoecological remains
and the oldest temperate MPA has been active for just 40 years [16,17]. While the global increase in MPAs is laudable, it is important to recognize that indirect effects appear on decadal or longer timescales and that MPAs are not immune from anthropogenic impact [17,18]. Biomineralized remains from sediment cores are the only long-term data source for most MPAs. Population collapses are not always a result of human activities. Fish scales, used to reconstruct a 1700-year history of sardine abundance off the California coast, documented nine major collapses and recoveries, demonstrating that sardine population crashes occurred naturally prior to the start of the fishery, and indicated an average recovery time of approximately 30 years [19]. Cores can provide a much longer temporal perspective than surficial shell assemblages (figure 1). Core data demonstrated that benthic communities of the northern Adriatic changed notably in the most recent centuries despite persevering virtually unchanged during the previous 125 000 years [20]. This exemplifies the value of palaeoecological core data in demonstrating differential responses of marine communities, which may be resilient to naturally occurring major climate perturbations, but vulnerable to recent human impacts.
rsbl.royalsocietypublishing.org
records of marine communities. These death assemblages yield demographic and ecological data somewhat analogous to human graveyards, including a comparable suite of biases. Naturally occurring death assemblages typically contain skeletal material produced over decadal to millennial timescales [7]. The composition of a death assemblage reflects the live community that produced it and provides strong evidence of species occurrence and abundance [5,7]. When death assemblages and living assemblages disagree, the cause is often attributed to recent anthropogenic change in the living community [5,7], although this requires the death assemblage to pre-date the change in the living community [7]. This is because death assemblages are evolving records of biological productivity and will eventually reflect an altered community state. Despite their potential biases, surficial skeletal assemblages represent an accessible record of past communities. Because shell assemblages archive the pre-impact communities, they can be used to directly assess population declines and the efficacy of restoration efforts. The ecosystems of the Colorado River delta, which deteriorated drastically following construction of numerous dams, offer an apt example. Surveys and numerical dating of shell accumulations indicated clams were at least 20 times more abundant and remarkably stable over the last millennium, prior to human alteration of the river flow [9]. These data also demonstrate that restoration efforts have not returned the local benthic productivity to its pre-industrial levels. Geochemical and palaeoecological data also indicate that growth rates and trophic structure of shelly invertebrates have changed [10,11]. Similarly, isotopic indicators from fish otoliths [12] suggested that the pre-industrial river flow helped commercially important fish species to more rapidly attain large body size. Oxygen isotopes from pre-dam shells have been used to provide quantitative estimates of the water flow levels required to restore natural salinity levels in the delta [13]. Shell assemblages have also be used to strengthen litigation against industry, as exemplified by taphonomic and trace elements data from freshwater mussel shells, which provided direct evidence linking mussel extirpation to mercury pollution rather than other causes (e.g. [14]).
To make meaningful contributions to policy and scientific understanding, conservation scientists must be able to move beyond simple observations of decline. The IUCN Red List is dominated by charismatic terrestrial organisms [25] because scientists have more data for those organisms. While the number of documented marine extinctions pales in comparison with terrestrial extinctions, this is in part an artefact of a lack of quantitative data on marine invertebrate abundances, ranges, habitats, dispersal and population dynamics [26]. While most palaeobiological/historical studies document
Ethics. No experiments involving animals were conducted during the course of this research. Authors’ contributions. Both authors contributed substantially to the conception and design of the article. Both authors made important contributions to drafting and revising the article. Both authors approve the final version of the article for publication. Both authors agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. Competing interests. The authors have no competing interests. Funding. We received no funding for this study. Acknowledgements. We thank M. Gillings for constructive feedback on figure 1. We also gratefully acknowledge K. Wilson and four anonymous reviewers whose suggestions improved considerably the clarity and quality of this contribution.
References 1.
2.
3.
4.
5.
6.
7.
8.
Willis KJ, Arau´jo MB, Bennett KD, Figueroa-Rangel BL, Froyd CA, Myers N. 2007 How can a knowledge of the past help to conserve the future? Biodiversity conservation and the relevance of long-term ecological studies. Phil. Trans. R. Soc. B 362, 175–186. (doi:10.1098/rstb.2006.1977) Lotze HK et al. 2006 Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312, 1806 –1809. (doi:10.1126/science. 1128035) Rick TC, Kirch PV, Erlandson JM, Fitzpatrick SM. 2013 Archeology, deep history, and the human transformation of island ecosystems. Anthropocene 4, 33 –45. (doi:10.1016/j.ancene.2013.08.002) Dietl GP, Kidwell SM, Brenner M, Burney DA, Flessa KW, Jackson ST, Koch PL. 2015 Conservation paleobiology: leveraging knowledge of the past to inform conservation and restoration. Annu. Rev. Earth Planet Sci. 43, 79 –103. (doi:10.1146/ annurev-earth-040610-133349) Kidwell SM. 2015 Biology in the Anthropocene: challenges and insights from young fossil records. Proc. Natl Acad. Sci. USA 112, 4922– 4929. (doi:10. 1073/pnas.1403660112) Lotze HK, Coll M, Dunne J. 2011 Historical changes in marine resources, food-web structure and ecosystem functioning in the Adriatic Sea, Mediterranean. Ecosystems 14, 198 –222. (doi:10. 1007/s10021-010-9404-8) Kidwell SM. 2013 Time-averaging and fidelity of modern death assemblages: building a taphonomic foundation for conservation palaeobiology. Palaeontology 56, 487–522. (doi:10.1111/pala.12042) Finnegan S et al. 2015 Paleontological baselines for evaluating extinction risk in the modern oceans.
9.
10.
11.
12.
13.
14.
Science 348, 567 –570. (doi:10.1126/science. aaa6635) Kowalewski M, Serrano GEA, Flessa FW. 2000 Dead delta’s former productivity: two trillion shells at the mouth of the Colorado River. Geology 28, 1059– 1062. (doi:10.1130/0091-7613(2000)28 ,1059:DDFPTT.2.0.CO;2) Cintra-Buenrostro CE, Flessa KW, Avila-Serrano GE. 2005 Who cares about a vanishing clam? Trophic importance of Mulinia coloradoensis inferred from predatory damage. Palaios 20, 296–302. (doi:10. 2110/palo.2004.p04-21) Schone BR, Flessa KW, Dettman DL, Goodwin DH. 2003 Upstream dams and downstream clams: growth rates of bivalve mollusks unveil impact of river management on estuarine ecosystems (Colorado River Delta, Me´xico). Estuar. Coast. Shelf Sci. 58, 715–726. (doi:10.1016/S02727714(03)00175-6) Rowell K, Flessa KW, Dettman DL, Roman MJ, Gerber LR, Findley LT. 2008 Diverting the Colorado River leads to a dramatic life history shift in an endangered marine fish. Biol. Conserv. 141, 1138 –1148. (doi:10.1016/j.biocon.2008.02.013) Cintra-Buenrostro CE, Flessa KW, Dettman DL. 2012 Restoration flows for the Colorado River estuary, Me´xico: estimates from oxygen isotopes in the bivalve mollusk Mulinia coloradoensis (Mactridae: Bivalvia). Wetl. Ecol. Manag. 20, 313–327. (doi:10. 1007/s11273-012-9255-5) Brown ME, Kowalewski M, Neves RJ, Cherry DS, Schreiber ME. 2005 Freshwater mussel shells as environmental chronicles: geochemical and taphonomic signatures of mercury-related extirpations in the North Fork Holston River,
15.
16.
17.
18.
19.
20.
Virginia. Environ. Sci. Technol. 39, 1455– 1462. (doi:10.1021/es048573p) Edgar GJ, Samson CR. 2004 Catastrophic decline in mollusc diversity in eastern Tasmania and its concurrence with shellfish fisheries. Conserv. Biol. 18, 1579–1588. (doi:10.1111/j.1523-1739.2004. 00191.x) Edgar GJ, Samson CR, Barrett NS. 2005 Species extinction in the marine environment: Tasmania as a regional example of overlooked losses in biodiversity. Conserv. Biol. 19, 1294– 3000. (doi:10. 1111/j.1523-1739.2005.00159.x) Babcock RC, Shears NT, Alcala AC, Barrett NS, Edgar GJ, Lafferty KD, McClanahan TR, Russ GR. 2010 Decadal trends in marine reserves reveal differential rates of change in direct and indirect effects. Proc. Natl Acad. Sci. USA 107, 18 256 –18 261. (doi:10. 1073/pnas.0908012107) Roff G, Clark TR, Reymond CE, Zhao J-x, Feng Y, McCook LJ, Done TJ, Pandolfi JM. 2013 Palaeoecological evidence of a historical collapse of corals at Pelorus Island, inshore Great Barrier Reef, following European settlement. Proc. R. Soc. B 280 20122100. (doi:10.1098/rspb.2012.2100) Baumgartner TR, Soutar A, Ferreira-Bartrina V. 1992 Reconstruction of the history of Pacific sardine and northern anchovy populations over the past two millennia from sediments of the Santa Barbara Basin, California. CalCOFI Rep. 33, 24– 40. Kowalewski M, Wittmer JM, Dexter TA, Amorosi A, Scarponi D. 2015 Differential responses of marine communities to natural and anthropogenic changes. Proc. R. Soc. B 282, 20142990. (doi:10.1098/rspb. 2014.2990)
4
Biol. Lett. 12: 20150951
4. Conclusion
population declines and extinctions at local and regional scales, these local and regional declines have a profound impact on communities and will have important implications for their extinction risk. Palaeoecological data inform us about past biospheres and are thus suited for generating testable mechanistic hypotheses regarding ecosystem changes, extinction threats and extinctions.
rsbl.royalsocietypublishing.org
Fossil assemblages with highly precise chronologies and low amounts of time-averaging are most analogous to ecological samples. However, a highly time-averaged assemblage is valuable precisely because it provides long-term (often millennial scale) estimates of the relative importance of species in local communities. The essential chronological requirement is to place data in the temporal context of human impacts: does the assemblage pre-date or post-date the onset of substantial anthropogenic change?
Prog. Ser. 198, 249–260. (doi:10.3354/ meps198249) 23. Kosnik MA, Hua Q, Kaufman DS, Wu¨st RA. 2009 Taphonomic bias and time-averaging in tropical molluscan death assemblages: differential shell halflives in Great Barrier Reef sediment. Paleobiology 34, 565–586. (doi:10.1666/0094-8373-35.4.565) 24. Kosnik MA, Hua Q, Kaufman DS, Zawadzki A. 2015 Sediment accumulation, stratigraphic order, and the extent of time-averaging in lagoonal sediments: a
comparison of 210Pb and 14C/amino acid racemization chronologies. Coral Reefs 34, 215–229. (doi:10.1007/s00338-014-1234-2) 25. The IUCN Red List of Threatened Species. Version 2015-3. www.iucnredlist.org (accessed 2 November 2015). 26. Re´gnier C, Fontaine B, Bouchet P. 2009 Not knowing, not recording, not listing: numerous unnoticed mollusk extinctions. Conserv. Biol. 23, 1214–1221. (doi:10.1111/j.1523-1739.2009.01245.x)
5
rsbl.royalsocietypublishing.org
21. Solo´rzano Kraemer MM, Kraemer AS, Stebner F, Bickel DJ, Rust J. 2015 Entrapment bias of arthropods in Miocene amber revealed by trapping experiments in a tropical forest in Chiapas, Mexico. PLoS ONE 10, e0118820. (doi:10.1371/journal.pone. 0118820) 22. Willis TJ, MIllar RB, Babcock RC. 2000 Detection of spatial variability in relative density of fishes: comparison of visual census, angling, and baited underwater video. Mar. Ecol.
Biol. Lett. 12: 20150951
rsbl.royalsocietypublishing.org
Understanding modern extinctions in marine ecosystems: the role of palaeoecological data
Opinion piece
Matthew A. Kosnik1 and Michał Kowalewski2 1
Cite this article: Kosnik MA, Kowalewski M. 2016 Understanding modern extinctions in marine ecosystems: the role of palaeoecological data. Biol. Lett. 12: 20150951. http://dx.doi.org/10.1098/rsbl.2015.0951
Received: 13 November 2015 Accepted: 8 March 2016
Subject Areas: ecology, palaeontology, environmental science Keywords: palaeobiology, palaeoecology, conservation palaeobiology, Holocene, marine ecosystems, death assemblages
Author for correspondence: Matthew A. Kosnik e-mail: [email protected]
An invited contribution to the special feature ‘Biology of extinction: inferring events, patterns and processes’. Electronic supplementary material is available at http://dx.doi.org/10.1098/rsbl.2015.0951 or via http://rsbl.royalsocietypublishing.org.
2
Department of Biological Sciences, Macquarie University, Sydney, New South Wales 2109 Australia Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA MAK, 0000-0001-5380-7041; MK, 0000-0002-8575-4711 Because anthropogenic impacts on ecological systems pre-date the oldest scientific observations, historical documents and archaeological records, understanding modern extinctions requires additional data sources that extend further back in time. Palaeoecological records, which provide quantitative proxy records of ecosystems prior to human impact, are essential for understanding recent extinctions and future extinction risks. Here we critically review the value of the most recent fossil record in contributing to our understanding of modern extinctions and illustrate through case studies how naturally occurring death assemblages and Holocene sedimentary records provide context to the plight of marine ecosystems. While palaeoecological data are inherently restricted censuses of past communities (manipulative experiments are not possible), they yield quantitative records over temporal scales that are beyond the reach of ecology. Only by including palaeoecological data is it possible to fully assess the role of long-term anthropogenic processes in driving modern extinction risk.
1. Millennial scale context of extant ecological systems Palaeoecological data, despite their shortcomings, can provide multi-millennial ecological records required to contextualize modern extinctions [1 –5] and thus complement other types of data used to assess extinctions and extinction risks. While real-time instrumental records are the highest precision records and quantitative ecological research is best able to test mechanisms, their temporal scope is inadequate ([1], figure 1). Written records of exploitation deliver priceless insights further back in time, but they are typically qualitative [2]. Zooarchaeological data represent critical records of human harvesting activities [3]. By contrast, palaeoecology integrates biological, sedimentary and geochemical records to derive diverse quantitative data about ecological systems prior to, as well as during, human occupation and impact [4,5,7]. Palaeoecological research alone cannot completely document human-driven ecological changes because it relies primarily on restricted census data types (figure 1) and unlike written historical and midden records, palaeoecological research only correlates ecological changes with changing human activities. Ecological studies can take advantage of real-time instrument records and experimental manipulations to enable mechanistic understandings of ecological changes. Consequently, quantifying anthropogenic impacts necessitates a holistic approach—a synthesis of ecological, historical, archaeological and palaeoecological data—that provides more realistic assessments of anthropogenic changes and modern extinction risks (figure 1). Only then can we separate extinctions due to human impacts from those likely driven by natural causes. Of note, deep-time palaeobiological studies are becoming increasingly relevant for assessing current extinction risks (e.g. [8]). However, such studies represent macroevolutionary
& 2016 The Author(s) Published by the Royal Society. All rights reserved.
2 real time instrument restricted census quantitative
written records
IUCN Red List
middens
6000 10000
50000 1 × 105 2 × 105
Pleistocene
20000
Late Modern Early Modern Medieval Local Market–Classical cores / excavations
Breeding Bird Surveys
PGE / eLTER
HBR / LTER / NEON
temperature
sea level
1500 600 0 900
Late Global Early Global
death assemblages
1800
Continuous Plankton Recorder
1950 1900
Holocene
temporal extent (years BC/AD)
2000
Agricultural
Hunter–gatherer
Figure 1. The characteristics and temporal coverage for different data types in the context of human cultural development. Record types are scored as dominantly of that category (black), some of that category (grey), or typically not of that category (white). The y-axis is log-transformed even though this visually exaggerates the temporal extent of instrumental and experimental records. Anthropogenic time intervals based on Lotze et al. [6]. While real-time instrumental and experimental records are the most precise, they are the most spatially and temporally restricted. The longest direct records of physical phenomena extend back only into the ‘Early/ Late Modern’ time interval. These records include atmospheric carbon dioxide, sea level and continuous temperature records (bar width: first continuous record, global records, satellite data). Ecological experiments rarely extend beyond the ‘Late Global’ time interval. The Long-Term Ecological Research (LTER) and LTER-Europe (eLTER) programs illustrate the investment in LTER programs in the last few decades. These are expanded from Hubbard Brook (HBR) and the Park Grass Experiment (PGE), which are the longest running ecological experiments. Explicitly ecological data vary widely, but most are spatially and taxonomically restricted censuses with biases associated with the sampling methodology used. Direct observations including the Breeding Bird Survey and Continuous Plankton Recorder programs are the longest continuous ecological observations. The IUCN Red List is extended back as a finer line to reflect extinctions documented through historical data. Archaeological records from middens and historical writing are less resolved and temporally and spatially discontinuous, but extend further back in time. Palaeoecological records are temporally discontinuous, but are spatially widespread and extend back over the entire duration of human history and beyond. The width of the bars reflects the relative commonness and abundance of those data during those time periods. This plot reflects primarily western European and North American datasets, but the source code is provided as supplemental material to facilitate the creation of regional versions (see the electronic supplementary material for additional detail). (Online version in colour.) approaches fundamentally different from those discussed here. Near Recent palaeoecological records are particularly valuable as they typically contain extant, albeit locally or regionally extirpated, species in an essentially modern geographical and environmental context. While humans occupied continents and substantially impacted faunas and floras prior to Western colonization and industrialization (Medieval/Early Modern and Early/Late Modern transitions in figure 1), these represent substantial increases in anthropogenic pressures exerted on biological populations (e.g. [2,6]). Here we outline opportunities afforded by Recent palaeoecological data (i.e. surficial death assemblages
and buried Late Quaternary sedimentary records) when assessing extinction risk in the context of human cultural development. We also outline some of the challenges in using these records for assessing extinction risk.
2. Recent palaeoecological records (a) Naturally occurring shell assemblages sampled from surface sediment Surficial accumulations of biomineralized skeletal material, or death assemblages, represent globally available historical
Biol. Lett. 12: 20150951
atmospheric CO2
2015
rsbl.royalsocietypublishing.org
data type
manipulative experiments
Sediment cores are increasingly recognized as valuable archives of past ecosystems. For example, cores were used effectively to document the role of fisheries in the decline of Tasmanian molluscan communities. The threefold decline in diversity and fourfold decline in abundance of molluscs observed in cores closely mirrored fishery activities in space and time, while actively harvested species declined relatively more abruptly [15]. While fishing and direct exploitation are linked to the decline of Tasmanian molluscs [15], introduced species have played an equally important role in reshaping these coastal marine systems, with 83% of live molluscan biomass collected in 1997– 1999 belonging to introduced taxa [16]. While harvesting rarely drives marine species to extinction, the indirect impacts of fishing, introduced species, and other anthropogenic impacts have the potential to drive species locally if not regionally extinct [16]. To the extent that marine protected areas (MPAs) can represent control sites, most Tasmanian MPAs have existed for fewer than 20 years
3. Key challenges (a) Preservation and sampling Palaeoecological data are subject to taphonomic biases associated with fossilization. Most obviously, organisms with robust skeletons typically yield more fossil remains than those without. However, taphonomy is just a special case of sampling bias. All data-gathering techniques have biases, and some taxa may be over/under represented by different sampling/observation techniques (e.g. [21,22]). As with ecological sampling, a species’ absence may reflect its true absence during the sampling period or the failure of a particular sampling methodology to sample it. A variety of commonly used methods can control for such sampling effects, and taphonomic processes are increasingly well understood (see [5,7,21,23] and references therein).
(b) Chronology and time-averaging While Holocene sediments enclosing fossils can be dated using a number of methods, using sedimentary dates implicitly assumes that fossils and sediments are coeval. Even when this is the case for the median fossil age, sediment derived ages cannot estimate the variance around the median age, termed time-averaging, which quantifies the time over which the fossils accumulated (e.g. [23,24]). Time-averaging can be quantified by numerical dating of individual fossils. Advances in amino acid racemization, carbon-14 and uranium–thorium disequilibrium dating have significantly reduced the costs, making it possible to date hundreds rather than a handful of specimens (see [7,18,23,24] and references therein). Estimates of time-averaging are critical when comparing palaeological to ecological data, so the differences in the timespan of sampling and temporal resolution of resulting data can both be assessed. For example, the above-mentioned River Colorado delta study [9] quantified time-averaging and corrected palaeoecological estimates of productivity to allow direct comparisons with ecological surveys of the modern fauna.
3
Biol. Lett. 12: 20150951
(b) Cores, excavations and buried palaeoecological remains
and the oldest temperate MPA has been active for just 40 years [16,17]. While the global increase in MPAs is laudable, it is important to recognize that indirect effects appear on decadal or longer timescales and that MPAs are not immune from anthropogenic impact [17,18]. Biomineralized remains from sediment cores are the only long-term data source for most MPAs. Population collapses are not always a result of human activities. Fish scales, used to reconstruct a 1700-year history of sardine abundance off the California coast, documented nine major collapses and recoveries, demonstrating that sardine population crashes occurred naturally prior to the start of the fishery, and indicated an average recovery time of approximately 30 years [19]. Cores can provide a much longer temporal perspective than surficial shell assemblages (figure 1). Core data demonstrated that benthic communities of the northern Adriatic changed notably in the most recent centuries despite persevering virtually unchanged during the previous 125 000 years [20]. This exemplifies the value of palaeoecological core data in demonstrating differential responses of marine communities, which may be resilient to naturally occurring major climate perturbations, but vulnerable to recent human impacts.
rsbl.royalsocietypublishing.org
records of marine communities. These death assemblages yield demographic and ecological data somewhat analogous to human graveyards, including a comparable suite of biases. Naturally occurring death assemblages typically contain skeletal material produced over decadal to millennial timescales [7]. The composition of a death assemblage reflects the live community that produced it and provides strong evidence of species occurrence and abundance [5,7]. When death assemblages and living assemblages disagree, the cause is often attributed to recent anthropogenic change in the living community [5,7], although this requires the death assemblage to pre-date the change in the living community [7]. This is because death assemblages are evolving records of biological productivity and will eventually reflect an altered community state. Despite their potential biases, surficial skeletal assemblages represent an accessible record of past communities. Because shell assemblages archive the pre-impact communities, they can be used to directly assess population declines and the efficacy of restoration efforts. The ecosystems of the Colorado River delta, which deteriorated drastically following construction of numerous dams, offer an apt example. Surveys and numerical dating of shell accumulations indicated clams were at least 20 times more abundant and remarkably stable over the last millennium, prior to human alteration of the river flow [9]. These data also demonstrate that restoration efforts have not returned the local benthic productivity to its pre-industrial levels. Geochemical and palaeoecological data also indicate that growth rates and trophic structure of shelly invertebrates have changed [10,11]. Similarly, isotopic indicators from fish otoliths [12] suggested that the pre-industrial river flow helped commercially important fish species to more rapidly attain large body size. Oxygen isotopes from pre-dam shells have been used to provide quantitative estimates of the water flow levels required to restore natural salinity levels in the delta [13]. Shell assemblages have also be used to strengthen litigation against industry, as exemplified by taphonomic and trace elements data from freshwater mussel shells, which provided direct evidence linking mussel extirpation to mercury pollution rather than other causes (e.g. [14]).
To make meaningful contributions to policy and scientific understanding, conservation scientists must be able to move beyond simple observations of decline. The IUCN Red List is dominated by charismatic terrestrial organisms [25] because scientists have more data for those organisms. While the number of documented marine extinctions pales in comparison with terrestrial extinctions, this is in part an artefact of a lack of quantitative data on marine invertebrate abundances, ranges, habitats, dispersal and population dynamics [26]. While most palaeobiological/historical studies document
Ethics. No experiments involving animals were conducted during the course of this research. Authors’ contributions. Both authors contributed substantially to the conception and design of the article. Both authors made important contributions to drafting and revising the article. Both authors approve the final version of the article for publication. Both authors agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. Competing interests. The authors have no competing interests. Funding. We received no funding for this study. Acknowledgements. We thank M. Gillings for constructive feedback on figure 1. We also gratefully acknowledge K. Wilson and four anonymous reviewers whose suggestions improved considerably the clarity and quality of this contribution.
References 1.
2.
3.
4.
5.
6.
7.
8.
Willis KJ, Arau´jo MB, Bennett KD, Figueroa-Rangel BL, Froyd CA, Myers N. 2007 How can a knowledge of the past help to conserve the future? Biodiversity conservation and the relevance of long-term ecological studies. Phil. Trans. R. Soc. B 362, 175–186. (doi:10.1098/rstb.2006.1977) Lotze HK et al. 2006 Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312, 1806 –1809. (doi:10.1126/science. 1128035) Rick TC, Kirch PV, Erlandson JM, Fitzpatrick SM. 2013 Archeology, deep history, and the human transformation of island ecosystems. Anthropocene 4, 33 –45. (doi:10.1016/j.ancene.2013.08.002) Dietl GP, Kidwell SM, Brenner M, Burney DA, Flessa KW, Jackson ST, Koch PL. 2015 Conservation paleobiology: leveraging knowledge of the past to inform conservation and restoration. Annu. Rev. Earth Planet Sci. 43, 79 –103. (doi:10.1146/ annurev-earth-040610-133349) Kidwell SM. 2015 Biology in the Anthropocene: challenges and insights from young fossil records. Proc. Natl Acad. Sci. USA 112, 4922– 4929. (doi:10. 1073/pnas.1403660112) Lotze HK, Coll M, Dunne J. 2011 Historical changes in marine resources, food-web structure and ecosystem functioning in the Adriatic Sea, Mediterranean. Ecosystems 14, 198 –222. (doi:10. 1007/s10021-010-9404-8) Kidwell SM. 2013 Time-averaging and fidelity of modern death assemblages: building a taphonomic foundation for conservation palaeobiology. Palaeontology 56, 487–522. (doi:10.1111/pala.12042) Finnegan S et al. 2015 Paleontological baselines for evaluating extinction risk in the modern oceans.
9.
10.
11.
12.
13.
14.
Science 348, 567 –570. (doi:10.1126/science. aaa6635) Kowalewski M, Serrano GEA, Flessa FW. 2000 Dead delta’s former productivity: two trillion shells at the mouth of the Colorado River. Geology 28, 1059– 1062. (doi:10.1130/0091-7613(2000)28 ,1059:DDFPTT.2.0.CO;2) Cintra-Buenrostro CE, Flessa KW, Avila-Serrano GE. 2005 Who cares about a vanishing clam? Trophic importance of Mulinia coloradoensis inferred from predatory damage. Palaios 20, 296–302. (doi:10. 2110/palo.2004.p04-21) Schone BR, Flessa KW, Dettman DL, Goodwin DH. 2003 Upstream dams and downstream clams: growth rates of bivalve mollusks unveil impact of river management on estuarine ecosystems (Colorado River Delta, Me´xico). Estuar. Coast. Shelf Sci. 58, 715–726. (doi:10.1016/S02727714(03)00175-6) Rowell K, Flessa KW, Dettman DL, Roman MJ, Gerber LR, Findley LT. 2008 Diverting the Colorado River leads to a dramatic life history shift in an endangered marine fish. Biol. Conserv. 141, 1138 –1148. (doi:10.1016/j.biocon.2008.02.013) Cintra-Buenrostro CE, Flessa KW, Dettman DL. 2012 Restoration flows for the Colorado River estuary, Me´xico: estimates from oxygen isotopes in the bivalve mollusk Mulinia coloradoensis (Mactridae: Bivalvia). Wetl. Ecol. Manag. 20, 313–327. (doi:10. 1007/s11273-012-9255-5) Brown ME, Kowalewski M, Neves RJ, Cherry DS, Schreiber ME. 2005 Freshwater mussel shells as environmental chronicles: geochemical and taphonomic signatures of mercury-related extirpations in the North Fork Holston River,
15.
16.
17.
18.
19.
20.
Virginia. Environ. Sci. Technol. 39, 1455– 1462. (doi:10.1021/es048573p) Edgar GJ, Samson CR. 2004 Catastrophic decline in mollusc diversity in eastern Tasmania and its concurrence with shellfish fisheries. Conserv. Biol. 18, 1579–1588. (doi:10.1111/j.1523-1739.2004. 00191.x) Edgar GJ, Samson CR, Barrett NS. 2005 Species extinction in the marine environment: Tasmania as a regional example of overlooked losses in biodiversity. Conserv. Biol. 19, 1294– 3000. (doi:10. 1111/j.1523-1739.2005.00159.x) Babcock RC, Shears NT, Alcala AC, Barrett NS, Edgar GJ, Lafferty KD, McClanahan TR, Russ GR. 2010 Decadal trends in marine reserves reveal differential rates of change in direct and indirect effects. Proc. Natl Acad. Sci. USA 107, 18 256 –18 261. (doi:10. 1073/pnas.0908012107) Roff G, Clark TR, Reymond CE, Zhao J-x, Feng Y, McCook LJ, Done TJ, Pandolfi JM. 2013 Palaeoecological evidence of a historical collapse of corals at Pelorus Island, inshore Great Barrier Reef, following European settlement. Proc. R. Soc. B 280 20122100. (doi:10.1098/rspb.2012.2100) Baumgartner TR, Soutar A, Ferreira-Bartrina V. 1992 Reconstruction of the history of Pacific sardine and northern anchovy populations over the past two millennia from sediments of the Santa Barbara Basin, California. CalCOFI Rep. 33, 24– 40. Kowalewski M, Wittmer JM, Dexter TA, Amorosi A, Scarponi D. 2015 Differential responses of marine communities to natural and anthropogenic changes. Proc. R. Soc. B 282, 20142990. (doi:10.1098/rspb. 2014.2990)
4
Biol. Lett. 12: 20150951
4. Conclusion
population declines and extinctions at local and regional scales, these local and regional declines have a profound impact on communities and will have important implications for their extinction risk. Palaeoecological data inform us about past biospheres and are thus suited for generating testable mechanistic hypotheses regarding ecosystem changes, extinction threats and extinctions.
rsbl.royalsocietypublishing.org
Fossil assemblages with highly precise chronologies and low amounts of time-averaging are most analogous to ecological samples. However, a highly time-averaged assemblage is valuable precisely because it provides long-term (often millennial scale) estimates of the relative importance of species in local communities. The essential chronological requirement is to place data in the temporal context of human impacts: does the assemblage pre-date or post-date the onset of substantial anthropogenic change?
Prog. Ser. 198, 249–260. (doi:10.3354/ meps198249) 23. Kosnik MA, Hua Q, Kaufman DS, Wu¨st RA. 2009 Taphonomic bias and time-averaging in tropical molluscan death assemblages: differential shell halflives in Great Barrier Reef sediment. Paleobiology 34, 565–586. (doi:10.1666/0094-8373-35.4.565) 24. Kosnik MA, Hua Q, Kaufman DS, Zawadzki A. 2015 Sediment accumulation, stratigraphic order, and the extent of time-averaging in lagoonal sediments: a
comparison of 210Pb and 14C/amino acid racemization chronologies. Coral Reefs 34, 215–229. (doi:10.1007/s00338-014-1234-2) 25. The IUCN Red List of Threatened Species. Version 2015-3. www.iucnredlist.org (accessed 2 November 2015). 26. Re´gnier C, Fontaine B, Bouchet P. 2009 Not knowing, not recording, not listing: numerous unnoticed mollusk extinctions. Conserv. Biol. 23, 1214–1221. (doi:10.1111/j.1523-1739.2009.01245.x)
5
rsbl.royalsocietypublishing.org
21. Solo´rzano Kraemer MM, Kraemer AS, Stebner F, Bickel DJ, Rust J. 2015 Entrapment bias of arthropods in Miocene amber revealed by trapping experiments in a tropical forest in Chiapas, Mexico. PLoS ONE 10, e0118820. (doi:10.1371/journal.pone. 0118820) 22. Willis TJ, MIllar RB, Babcock RC. 2000 Detection of spatial variability in relative density of fishes: comparison of visual census, angling, and baited underwater video. Mar. Ecol.
Biol. Lett. 12: 20150951
