Using the Fossil Record to Understand Extinction Risk and Inform Marine Conservation in a Changing World.

Understanding the long-term effects of ongoing global environmental change on marine ecosystems requires a cross-disciplinary approach. Deep-time and recent fossil records can contribute by identifying traits and environmental conditions associated with elevated extinction risk during analogous events in the geologic past and by providing baseline data that can be used to assess historical change and set management and restoration targets and benchmarks. Here, we review the ecological and environmental information available in the marine fossil record and discuss how these archives can be used to inform current extinction risk assessments as well as marine conservation strategies and decision-making at global to local scales. As we consider future research directions in deep-time and conservationpaleobiology, we emphasize the need for coproduced research that unites researchers, conservation practitioners, and policymakers with the communities for whom the impacts of climate and global change are most imminent.

Views from the dock: Warming waters, adaptation, and the future of Maine's lobster fishery.

The ability of resource-dependent communities to adapt to climate change depends in part on their perceptions and prioritization of specific climate-related threats. In the Maine lobster fishery, which is highly vulnerable to warming water associated with climate change, we found a strong majority (84%) of fishers viewed warming water as a threat, but rank its impacts lower than other drivers of change (e.g., pollution). Two-thirds believed they will be personally affected by warming waters, but only half had plans to adapt. Those with adaptation plans demonstrated fundamentally different views of human agency in this system, observing greater anthropogenic threats, but also a greater ability to control the fishery through their own actions on the water and fisheries management processes. Lack of adaptation planning was linked to the view that warming waters result from natural cycles, and the expectation that technological advancements will help buffer the industry from warming waters.

Challenges to natural and human communities from surprising ocean temperatures.

The community of species, human institutions, and human activities at a given location have been shaped by historical conditions (both mean and variability) at that location. Anthropogenic climate change is now adding strong trends on top of existing natural variability. These trends elevate the frequency of "surprises"-conditions that are unexpected based on recent history. Here, we show that the frequency of surprising ocean temperatures has increased even faster than expected based on recent temperature trends. Using a simple model of human adaptation, we show that these surprises will increasingly challenge natural modes of adaptation that rely on historical experience. We also show that warming rates are likely to shift natural communities toward generalist species, reducing their productivity and diversity. Our work demonstrates increasing benefits for individuals and institutions from betting that trends will continue, but this strategy represents a radical shift that will be difficult for many to make.

The historical development of complex global trafficking networks for marine wildlife.

The complexity of trade networks is a major challenge to controlling wildlife trafficking and illegal, unreported, and unregulated (IUU) fishing. These networks may not be modern inventions, but have developed over centuries, from integrated global markets that preceded modern regulatory policies. To understand these linkages, we curated 150 years of tortoiseshell transactions and derived biologically informed harvest models to estimate the trade in critically endangered hawksbill sea turtles (Eretmochelys imbricata). We find that trade networks concentrated in Southeast Asia harvested 9 million turtles, over six times previous estimates. These networks spread from within the Pacific, to the Indian and Atlantic basins, and became markedly more complex after 1950. Our results further indicate that the magnitude and extent of the coastally restricted hawksbill exploitation parallel current patterns of IUU fishing. Policies to combat these interlinked illegal practices should assimilate the important role of small-scale, coastal fisheries in these increasingly complex global networks.

Ghost reefs: Nautical charts document large spatial scale of coral reef loss over 240 years.

Massive declines in population abundances of marine animals have been documented over century-long time scales. However, analogous loss of spatial extent of habitat-forming organisms is less well known because georeferenced data are rare over long time scales, particularly in subtidal, tropical marine regions. We use high-resolution historical nautical charts to quantify changes to benthic structure over 240 years in the Florida Keys, finding an overall loss of 52% (SE, 6.4%) of the area of the seafloor occupied by corals. We find a strong spatial dimension to this decline; the spatial extent of coral in Florida Bay and nearshore declined by 87.5% (SE, 7.2%) and 68.8% (SE, 7.5%), respectively, whereas that of offshore areas of coral remained largely intact. These estimates add to finer-scale loss in live coral cover exceeding 90% in some locations in recent decades. The near-complete elimination of the spatial coverage of nearshore coral represents an underappreciated spatial component of the shifting baseline syndrome, with important lessons for other species and ecosystems. That is, modern surveys are typically designed to assess change only within the species' known, extant range. For species ranging from corals to sea turtles, this approach may overlook spatial loss over longer time frames, resulting in both overly optimistic views of their current conservation status and underestimates of their restoration potential.

Collateral damage to marine and terrestrial ecosystems from Yankee whaling in the 19th century.

Yankee whalers of the 19th century had major impacts on populations of large whales, but these leviathans were not the only taxa targeted. Here, we describe the "collateral damage," the opportunistic or targeted taking of nongreat whale species by the American whaling industry. Using data from 5,064 records from 79 whaling logs occurring between 1840 and 1901, we show that Yankee whalers captured 5,255 animals across three large ocean basins from 32 different taxonomic categories, including a wide range of marine and terrestrial species. The taxa with the greatest number of individuals captured were walruses (Odobenus rosmarus), ducks (family Anatidae), and cod (Gadus sp.). By biomass, the most captured species were walruses, grampus (a poorly defined group within Odontoceti), and seals (family Otariidae). The whalers captured over 2.4 million kg of nongreat whale meat equaling approximately 34 kg of meat per ship per day at sea. The species and areas targeted shifted over time in response to overexploitation of whale populations, with likely intensive local impacts on terrestrial species associated with multiyear whaling camps. Our results show that the ecosystem impacts of whaling reverberated on both marine and coastal environments.

Rethinking Trade-Driven Extinction Risk in Marine and Terrestrial Megafauna.

Large animals hunted for the high value of their parts (e.g., elephant ivory and shark fins) are at risk of extinction due to both intensive international trade pressure and intrinsic biological sensitivity. However, the relative role of trade, particularly in non-perishable products, and biological factors in driving extinction risk is not well understood [1-4]. Here we identify a taxonomically diverse group of >100 marine and terrestrial megafauna targeted for international luxury markets; estimate their value across three points of sale; test relationships among extinction risk, high value, and body size; and quantify the effects of two mitigating factors: poaching fines and geographic range size. We find that body size is the principal driver of risk for lower value species, but that this biological pattern is eliminated above a value threshold, meaning that the most valuable species face a high extinction risk regardless of size. For example, once mean product values exceed US$12,557 kg(-1), body size no longer drives risk. Total value scales with size for marine animals more strongly than for terrestrial animals, incentivizing the hunting of large marine individuals and species. Poaching fines currently have little effect on extinction risk; fines would need to be increased 10- to 100-fold to be effective. Large geographic ranges reduce risk for terrestrial, but not marine, species, whose ranges are ten times greater. Our results underscore both the evolutionary and ecosystem consequences of targeting large marine animals and the need to geographically scale up and prioritize conservation of high-value marine species to avoid extinction.

Historical reconstruction reveals recovery in Hawaiian coral reefs.

Coral reef ecosystems are declining worldwide, yet regional differences in the trajectories, timing and extent of degradation highlight the need for in-depth regional case studies to understand the factors that contribute to either ecosystem sustainability or decline. We reconstructed social-ecological interactions in Hawaiian coral reef environments over 700 years using detailed datasets on ecological conditions, proximate anthropogenic stressor regimes and social change. Here we report previously undetected recovery periods in Hawaiian coral reefs, including a historical recovery in the MHI (~AD 1400-1820) and an ongoing recovery in the NWHI (~AD 1950-2009+). These recovery periods appear to be attributed to a complex set of changes in underlying social systems, which served to release reefs from direct anthropogenic stressor regimes. Recovery at the ecosystem level is associated with reductions in stressors over long time periods (decades+) and large spatial scales (>10(3) km(2)). Our results challenge conventional assumptions and reported findings that human impacts to ecosystems are cumulative and lead only to long-term trajectories of environmental decline. In contrast, recovery periods reveal that human societies have interacted sustainably with coral reef environments over long time periods, and that degraded ecosystems may still retain the adaptive capacity and resilience to recover from human impacts.

Large-scale absence of sharks on reefs in the greater-Caribbean: a footprint of human pressures.

BACKGROUND: In recent decades, large pelagic and coastal shark populations have declined dramatically with increased fishing; however, the status of sharks in other systems such as coral reefs remains largely unassessed despite a long history of exploitation. Here we explore the contemporary distribution and sighting frequency of sharks on reefs in the greater-Caribbean and assess the possible role of human pressures on observed patterns. METHODOLOGY/PRINCIPAL FINDINGS: We analyzed 76,340 underwater surveys carried out by trained volunteer divers between 1993 and 2008. Surveys were grouped within one km2 cells, which allowed us to determine the contemporary geographical distribution and sighting frequency of sharks. Sighting frequency was calculated as the ratio of surveys with sharks to the total number of surveys in each cell. We compared sighting frequency to the number of people in the cell vicinity and used population viability analyses to assess the effects of exploitation on population trends. Sharks, with the exception of nurse sharks occurred mainly in areas with very low human population or strong fishing regulations and marine conservation. Population viability analysis suggests that exploitation alone could explain the large-scale absence; however, this pattern is likely to be exacerbated by additional anthropogenic stressors, such as pollution and habitat degradation, that also correlate with human population. CONCLUSIONS/SIGNIFICANCE: Human pressures in coastal zones have lead to the broad-scale absence of sharks on reefs in the greater-Caribbean. Preventing further loss of sharks requires urgent management measures to curb fishing mortality and to mitigate other anthropogenic stressors to protect sites where sharks still exist. The fact that sharks still occur in some densely populated areas where strong fishing regulations are in place indicates the possibility of success and encourages the implementation of conservation measures.

Documenting loss of large trophy fish from the Florida Keys with historical photographs.

A loss of large vertebrates has occurred in aquatic and terrestrial ecosystems, but data to measure long-term population changes are sparse. Historical photographs provide visual and quantitative evidence of changes in mean individual size and species composition for groups of marine fish that have been targeted by sport fishing. I measured such trends for 13 groups of recreationally caught "trophy" reef fish with photographs taken in Key West, Florida, from 1956 to 2007. The mean fish size declined from an estimated 19.9 kg (SE 1.5) to 2.3 kg (SE 0.3), and there was a major shift in species composition. Landings from 1956 to 1960 were dominated by large groupers (Epinephelus spp.), and other large predatory fish were commonly caught, including sharks with an average length of just <2 m. In contrast, landings in 2007 were composed of small snappers (Lutjanus spp. and Ocyurus chrysurus) with an average length of 34.4 cm (SE 0.62), and the average length of sharks declined by more than 50% over 50 years. Major declines in the size of fish caught were not reflected in the price of fishing trips, so customers paid the same amount for a less-valuable product. Historical photographs provide a window into a more pristine coral reef ecosystem that existed a half a century ago and lend support to current observations that unfished reef communities are able to support large numbers of large-bodied fish.

Extinction rate, historical population structure and ecological role of the Caribbean monk seal.

The productivity and biomass of pristine coral reef ecosystems is poorly understood, particularly in the Caribbean where communities have been impacted by overfishing and multiple other stressors over centuries. Using historical data on the spatial distribution and abundance of the extinct Caribbean monk seal (Monachus tropicalis), this study reconstructs the population size, structure and ecological role of this once common predator within coral reef communities, and provides evidence that historical reefs supported biomasses of fishes and invertebrates up to six times greater than those found on typical modern Caribbean reefs. An estimated 233,000-338,000 monk seals were distributed among 13 colonies across the Caribbean. The biomass of reef fishes and invertebrates required to support historical seal populations was 732-1018 gm(-2) of reefs, which exceeds that found on any Caribbean reef today and is comparable with those measured in remote Pacific reefs. Quantitative estimates of historically dense monk seal colonies and their consumption rates on pristine reefs provide concrete data on the magnitude of decline in animal biomass on Caribbean coral reefs. Realistic reconstruction of these past ecosystems is critical to understanding the profound and long-lasting effect of human hunting on the functioning of coral reef ecosystems.

Global trajectories of the long-term decline of coral reef ecosystems.

Degradation of coral reef ecosystems began centuries ago, but there is no global summary of the magnitude of change. We compiled records, extending back thousands of years, of the status and trends of seven major guilds of carnivores, herbivores, and architectural species from 14 regions. Large animals declined before small animals and architectural species, and Atlantic reefs declined before reefs in the Red Sea and Australia, but the trajectories of decline were markedly similar worldwide. All reefs were substantially degraded long before outbreaks of coral disease and bleaching. Regardless of these new threats, reefs will not survive without immediate protection from human exploitation over large spatial scales.