Multiple threats imperil freshwater biodiversity in the Anthropocene

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Magazine different stressors will therefore be critical for our understanding of the ecological consequences of noise pollution and to come up with efficient measures for potential mitigation. We better treat noise pollution, like global warming, as an integral part of the global threat of human-induced climate change. Where can I find out more? Basner, M., Babisch, W., Davis, A., Brink, M., Clark, C., Janssen, S., and Stansfeld, S. (2014). Auditory and non-auditory effects of noise on health. Lancet 383, 1325–1332. Brumm, H., and Slabbekoorn, H. (2005). Acoustic communication in noise. Adv. Stud. Behav. 35, 151–209. Francis, C.D., and Barber, J.R. (2013). A framework for understanding noise impacts on wildlife: An urgent conservation priority. Front. Ecol. Environ. 11, 305–313. Hawkins, A.D., Pembroke, A.E., and Popper, A.N. (2015). Information gaps in understanding the effects of noise on fishes and invertebrates. Rev. Fish Biol. Fish. 25, 39–64. Kunc, H.P., McLaughlin, K.E., and Schmidt, R. (2016). Aquatic noise pollution: Implications for individuals, populations, and ecosystems. Proc. R. Soc. Lond. B 283, 20160839. Ladich, F. (2008). Sound communication in fishes and the influence of ambient and anthropogenic noise. Bioacoustics 17, 35–37. Radford, A.N., Kerridge, E., and Simpson, S.D. (2014). Acoustic communication in a noisy world: can fish compete with anthropogenic noise? Behav. Ecol. 25, 1022–1030. Shannon, G., McKenna, M.F., Angeloni, L.M., Crooks, K.R., Fristrup, K.M., Brown, E., Warner, K.A., Nelson, M.D., White, C., and Briggs, J. (2016). A synthesis of two decades of research documenting the effects of noise on wildlife. Biol. Rev. 91, 982–1005. Slabbekoorn, H. (2004). Singing in the wild: the ecology of birdsong. In Nature’s Music The Science of Birdsong, P. Marler and H. Slabbekoorn, eds. (San Diego: Academic Press/Elsevier), pp. 178–205. Slabbekoorn, H. (2013). Songs of the city: Noisedependent spectral plasticity in the acoustic phenotype of urban birds. Anim. Behav. 85, 1089–1099. Slabbekoorn, H., Bouton, N., van Opzeeland, I., Coers, A., ten Cate, C., and Popper, A.N. (2010). A noisy spring: The impact of globally rising underwater sound levels on fish. Trends Ecol. Evol. 25, 419–427. Slabbekoorn, H., Dooling, R., Popper, A.N. and Fay, R.R. eds. (2018). Effects of anthropogenic noise on animals. In Springer Handbook of Auditory Research. (New York, USA: SpringerVerlag), pp. 309. Slabbekoorn, H., and Ripmeester, E.A.P. (2008). Birdsong and anthropogenic noise: implications and applications for conservation. Mol. Ecol. 17, 72–83. Wiley, R.H. (2017). How noise determines the evolution of communication. Anim. Behav. 124, 307–313. World Health Organization (2011). Burden of disease from environmental noise. Quantification of healthy life years lost in Europe. Available at www.euro.who.int/en/health-topics/ environment-and-health/noise/publications.

Institute of Biology, Leiden University, Sylviusweg 72, 2333BE, Leiden, The Netherlands. E-mail: [email protected]

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Multiple threats imperil freshwater biodiversity in the Anthropocene David Dudgeon Appropriation of fresh water to meet human needs is growing, and competition among users will intensify in a warmer and more crowded world. This essay explains why freshwater ecosystems are global hotspots of biological richness, despite a panoply of interacting threats that jeopardize biodiversity. The combined effects of these threats will soon become detrimental to humans since provision of ecosystem services, such as protein from capture fisheries, can only be sustained if waters remain healthy. Climate change poses an insidious existential threat to freshwater biodiversity in the Anthropocene, but immediate risks from dams, habitat degradation and pollution could well be far greater. In a warmer and increasingly humandominated planet, many Earth-system processes are dominated by human activities [1,2], and a pandemic array of physical and biological alterations to freshwater ecosystems are associated with rapid shifts in water use [3,4]. Water is an irreplaceable resource for people and biodiversity, and consumption or contamination of water by one group of human users makes it unavailable or unfit for others. For instance, abstraction of river water for irrigation reduces the downstream supply to the detriment of those who make a living from fishing. If it remained in the river channel, the same water might generate hydropower, flush wastes downstream, permit navigation, or sustain biodiversity. Because uses by humans and non-humans often conflict, and interests among human stakeholders differ also, fresh water is the common resource par excellence. In this essay, I describe the principal threats to fresh waters, and outline how these might intensify during the Anthropocene. I also explain why fresh waters are hotspots of global species richness, and the features that enhance the susceptibility of that biodiversity to burgeoning anthropogenic threat. Together, these features have driven recent declines in species and populations that need to be halted or reversed. Conservation action is most likely to be effective where it can be demonstrated that freshwater biodiversity enhances provision of ecosystem services for humans. Irrespective of this, I argue that immediate steps to constrain dam building and control pollution will

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enhance the resilience of freshwater ecosystems, and need to take place in conjunction with attempts to reduce the medium-term impacts of climate change. Principal threats to the freshwater commons Fresh waters are especially susceptible to changes arising from ‘the tragedy of the commons’. Scant consideration is given to the need to conserve aquatic biodiversity or preserve ecosystems when conflicting human interests are at stake. In most cases, only the fresh water that remains after human needs have been satisfied is available to sustain ecosystems. Nature often receives an inadequate share, such that flows of some major rivers (the Colorado, Indus, Ganges and Yellow Rivers) cease before reaching the coast. The over-abstracted Syr and Amu Darya no longer flow to their destination, resulting in the calamitous drying of the Aral Sea — perhaps the world’s worst environmental disaster. On a larger scale, climate change is an example of human misuse of the global atmospheric commons, reflecting the unwillingness of individual states (and particular stakeholders) to limit carbon emissions. Globally, the treatment of fresh waters as a commons has resulted in reduced human water security and widespread threats to biodiversity (e.g. [4]). The nature and intensity of factors degrading particular waters vary substantially. For instance, in countries where urbanization is proceeding rapidly (such as India and China), much riverine habitat is

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Magazine destroyed by mining sand for use in concrete. Nonetheless, an overall classification of threats is possible, resulting in six categories (Figure 1); each has multiple consequences, not all of which can be listed here. A fuller review of five of these threats (apart from climate change) is given elsewhere [5], and thus only key or recent citations are provided here. Flow regulation, dams and water abstraction Dam construction markedly alters flow conditions to which biota are adapted, and a riverine section above the dam is replaced by a reservoir. Movement of animals is obstructed, especially migratory species, and material (organic carbon, sediments and nutrients) is entrained. Reservoirs retain over 10,000 km3 of water, five times the standing volume of the Earth’s rivers, reducing sediment flux to the oceans by over 25% [3]; 48% of river volume is moderately to severely impacted by flow regulation, or fragmentation, or both [6]; and only 37% of rivers longer than 1,000 kilometres remain free-flowing [7]. Water abstracted for irrigation and other human needs leads to reduced downstream flows (even dewatering). These are often accompanied by downstream channelization and constraints imposed by levees and concretized banks. Dams are also the source of water transfers between drainage basins, changing conditions in donor and recipient rivers, permitting exchanges between formerly isolated biotas [8]. Pollution Pollution occurs in a host of forms, reflecting its multiple origins, with consequences that can be ubiquitous (the syndrome of eutrophication) and — as in the case of the ‘cocktail’ of contaminants and pollutants affecting an individual site — unique to a particular location. Non-chemical alteration of waters falls into this category, such as warming (thermal pollution) caused by cooling-water discharge from power stations. Pollution can arise from ‘end-of-thepipe’ point sources — for instance, discharge from a factory or a mining operation — or more diffuse run-off from agricultural land, and may be

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Figure 1. A conceptual diagram of global threats to freshwater ecosystems. The total planetary operating space is equivalent to the climate-change ellipse, and individual freshwater bodies can be positioned within this space according to the combination of threat categories that they experience. Overexploitation occupies the centre of the space because this is the earliest and sometimes the only threat to freshwater biodiversity in remote or sparsely populated localities. Most fresh waters are located within spaces where three or more threat categories overlap.

organic or inorganic compounds, or a mixture thereof, consisting of livestock waste and sewage (including pharmaceuticals), factory discharges, landfill seepage, oily run-off from roads and impermeable surfaces, agrochemicals (fertilizers or pesticides), macro- and microplastics, and so on (e.g. [9,10]). The effects of pollutants can be direct or indirect, lethal or sub-lethal, and their interactions may cause unexpected consequences. Pollution burdens can be expected to increase in the foreseeable future as a result of increasing wastewater discharge due to urbanization and intensification of livestock farming [11]. Land-use change in drainage basins Total or partial removal of natural vegetation increases run-off leading to soil erosion and sedimentation of lakes and rivers. Replacement of natural vegetation by plants with different

water requirements also changes surface and subsurface run-off, inputs of allochthonous organic matter (e.g. leaf litter and woody debris), and the degree of shading and, hence, water temperatures. Run-off from agricultural land is higher and faster than from naturally vegetated land, and may contain agrochemicals and excessive nutrients. Urbanization has particularly strong impacts, because impermeable surfaces greatly increase the magnitude and rates of contaminantrich surface run-off. Overexploitation of biological resources Over-fishing initially affects large or long-lived, late-maturing species, resulting in ‘fishing down’ the food chain and subsequent exploitation of small, rapidly maturing species [12]. Destructive fishing practices, using poisons, electricity and fine-meshed nets, are adopted as larger species

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Magazine become increasingly scarce. Frogs are also exploited for food, while birds that nest colonially are vulnerable to collection of eggs or nestlings. Other valued goods include crocodile hides and body parts of turtles used in traditional Chinese medicine; increasing scarcity of target species drives up their price and stimulates further exploitation. Alien (introduced or non-native) invasive species Impacts of alien invasive species depend on the identity of the invader and characteristics of the receiving community [13]: carnivores are especially problematic if native prey lack appropriate anti-predator adaptations. Competition for food or space may occur, especially if invaders make habitat conditions less suitable for native species. Alien species can introduce diseases to recipient communities or may themselves be pathogens. Hybridization poses a threat if there is a close evolutionary relationship between alien and native species. Global climate change Anthropogenic climate change represents a profound and insidious threat to freshwater biodiversity. Impacts will arise from rising temperatures, but changes in flow and inundation patterns due to shifts in rainfall, medium-term effects such as glacial melt, and an increased frequency of extreme events [14] will be relatively important in fresh waters because life cycles are often closely linked to hydrology. The ‘fingerprint’ of global climate change is already clear [15]: 23 out of 31 measured freshwater ecological processes show evidence of being altered. If water bodies become too warm for riverine species, and they cannot adapt, dispersal to cooler habitat (at higher altitudes, or further north) will be necessary, subject to limitations imposed by topography, habitat availability upstream, the presence of dams, and so on. Compensatory movements will be especially difficult for isolated lacustrine species that cannot disperse overland or through river networks. The extent of displacement needed to adjust to the upper range of warming predicted for the next century appears R962

insurmountable for most freshwater animals [16]. Interactions among threats The six threat categories are not independent (as conceptualized in Figure 1). For example, warmer temperatures can increase contaminant toxicity [17], while greater water abstraction by humans and climate change will reduce the capacity of rivers to dilute pollutants [11]. Flow regulation and pollution transform habitat conditions in ways that favour invasive species, which are generally more tolerant than natives and may be facilitated by climate change [13]. The ongoing global epidemic of dam construction [18] will lead to a 40% increase in reservoir storage by 2030, with direct impacts on riverine biodiversity; reservoirs also serve as ‘stepping stones’ for the spread of invasive species [19]. Dams have eliminated salmon runs in northwest Europe as well as along the west and (especially) east coasts of the United States [20]; the impacts were especially severe when combined with a targeted fishery. Other migratory species have been affected also, including those that move between rivers and coastal waters (shad, alewife, sturgeon, eels and river prawns), as well as potamodromous fishes that undertake breeding migrations within the Mekong and Amazon [21]. Exacerbation of Anthropocene threats to freshwater biodiversity The importance of the six threat categories for humans and biodiversity arises from a specific attribute of fresh water, especially water in rivers: its absolute scarcity. Liquid fresh water covers less than 1% of the Earth’s surface, constituting only 0.03% of the total volume of all water. Most of it resides in lakes (mainly Lake Baikal). The amount in rivers is a mere 0.0002% (or 0.006% of all fresh water): a standing volume of 2,120 km3 [22], which is the main water source used by humans. Human water withdrawal is slightly over 50% of the accessible surface water supply or ‘available run-off’ of approximately 12,500 km3 per year [3]. This percentage figure is sensitive to assumptions about how much water is accessible (rivers in far

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northern latitudes are mostly untapped) or available for capture (typically, floodwaters are not), and to the magnitude of total global annual run-off (~40,000 km3). From 1950 to 1998, percapita water availability declined from 16,000 to 6,700 m3 per year, and will be ~5,000 m3 per year by 2025. However, only 31% of global run-off is spatially and temporally accessible to society, so per-capita availability by 2025 would be nearer 1,500 m3 per year [3]. The Earth’s human population will reach 9 billion by 2050 or thereabouts, so planetary boundaries for sustainable water use may well be overstepped [23], as is presently occurring at local scales [2]. Competition for water is always highly asymmetric: as human requirements for water increase, the water remaining for nature declines, but water available for people is not contingent upon the amount needed to sustain aquatic biodiversity. An inexorable driver of competition will be water needed to grow food. Population increases, combined with changing diets, will raise food demand by 50% by 2030 and 70% by 2050 [24]. To make this additional agricultural production possible, water withdrawals for irrigation will need to increase. Only 15% of global croplands are irrigated, but they yield half of the saleable crops. Given that the extent of arable land is finite, bringing a greater proportion under irrigation may be the most expedient approach to feeding the 2 billion additional people expected by 2050, and improving the nutritional status of the many presently undernourished. Agriculture already accounts for around 70% of water withdrawals, but will face competition from domestic and industrial sectors. Even if there is a substantial increase in the efficiency of irrigation (improvements are being made), the amount of water remaining for nature will diminish. Shifts towards diets incorporating more animal protein will exacerbate the reduction because several times as much water is needed to support a standard American diet than one of equivalent calories comprising vegetables. Foodsecurity needs could result in water consumption increasing by up to 50% over the next 20 years [23]; some estimates are even higher [24]. Water demand is rising at almost twice the

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rate of population growth and, by 2025, half the global population will be living in water-stressed areas [25] with high (>40%) to very high (>80%) ratios of withdrawal to supply. Burgeoning populations, urbanization, and economic expansion will place ever-greater demands on freshwater ecosystems, especially rivers. Additional challenges will arise from the necessity to improve access to water and sanitation. In 2015, 71% of the global population used a safely managed drinking-water service — contamination-free and located on the premises — and 89% had access to a basic service within a 30-minute round trip. However, 844 million people did not, including 159 million dependent on surface water [25]. Since 1990, the proportion of people benefitting from improved sanitation rose from 54% to 68%, but 2.3 billion people lack toilets or latrines; inadequate wastewater management pollutes drinking water, causing 361,000 child deaths annually [26]. Furthermore, intensification of urbanization and livestock rearing have been projected to increase the number of people afflicted by organic pollution (BOD >5 mg/l) from 1.1 billion in 2000 to 2.5 billion in 2050, with developing countries affected disproportionately [11]. The impacts of global warming on freshwater biodiversity in the Anthropocene will be amplified by human responses to climatic uncertainty and a world in which ‘stationarity is dead’ [14]. Adaptation to water shortages and floods that threaten human welfare and property will encourage water engineering to mitigate these problems. New dams, levees, and diversions expected to enhance water security will alter flow and inundation patterns in ways that do not augur well for biodiversity. For instance, a host of water-transfer megaprojects is under construction or planned [8]; upon realization, they could move 1,923 km3 of water annually over a total distance more than twice the Earth’s circumference. Continuing impetus to install hydropower facilities along rivers to decarbonize economies will have limited benefit. The most optimistic forecasts expand the contribution of hydropower to global energy production from 16% in 2011 to only 18% by 2040, due to the concurrent rise in energy

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Figure 2. The WWF Living Planet Index [28] consists of population trend data for a collective ‘basket’ of vertebrates in the freshwater, marine and terrestrial realms. There have been remarkable decreases among freshwater species. Declines are relative to a benchmark value of 100 in 1970, and steepened between 2012 and 2014, reflecting reductions in populations censused four years earlier. The 2016 value of 19 for freshwater populations (based on 2012 counts) has confidence limits ranging from 11 to 32; limits for the value of 62 for terrestrial populations range from 49 to 79 ([33]; recalculated and redrawn from [31]).

demand [18]. Dam construction will intensify the direct impacts of climate change because they limit the natural resilience of riverine ecosystems: for instance, by restricting the ability of fishes to make compensatory movements to cooler conditions [27]. A related problem is that hard-path adaptation to climate change may be permitted to circumvent environmental reviews and regulations because of the urgency of project implementation. Freshwater biodiversity is now in peril Fresh water is not just a scarce resource; freshwater ecosystems are also biodiversity hotspots. Freshwater species make up 9.5% of known animal species on Earth, including around one third of vertebrates [5,28]. The latter is mainly fishes, but also comprises the entire global complement of crocodilians, virtually all amphibians, and most turtles. And, despite the much greater area and total production of marine environments, species richness of bony fishes (Actinopterygii) in the seas (14,736) and fresh waters

(15,149) is similar [29]. That almost 10% of global animal biodiversity is associated with habitats occupying <1% of the Earth’s surface accentuates the threat posed by growing human water demands in the Anthropocene. One aggravating factor is that rivers and almost all lakes are landscape receivers within drainage basins. Any increases in soil erosion, nutrient and contaminant loadings that accompany land-use change are transported downhill into valley bottoms and hence rivers. Rivers are also downstream transmitters of material received from their basins, and impacts do not remain local. The hierarchical architecture of rivers and their tributaries facilitates this transmission, increasing the vulnerability of biodiversity throughout the network and in receiving lakes. Paradoxically, this longitudinal connectivity is essential to freshwater ecosystem health, since the migrations of fishes and transport of materials depend upon it. Dams hinder these processes, ‘smooth out’ flow variability and limit the floodplain inundation to which the riverine biota is adapted

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Figure 3. The last known female specimen of the critically endangered Yangtze soft-shelled turtle, which died in April 2019. Repeated attempts at artificial insemination in China using sperm from a captive male had failed. The remaining global population of this species consists of three males, two of them in Vietnam. Photograph by kind permission of Gerald Kuchling, Turtle Survival Alliance.

and upon which their life cycles depend. The increased frequency of extreme events (floods and droughts) under climate change will also have consequences mediated through their effects on life-cycle events. A further complicating factor is that the habitats of most freshwater species are aquatic ‘islands’ set within a terrestrial matrix. Fish typically are unable to move between rivers since they cannot tolerate salinity sufficiently well to migrate along the coast nor can they travel overland and surmount terrestrial barriers. Amphibiotic animals, such as frogs and aquatic insects with terrestrial adults, enjoy more scope for overland dispersal. However, many are habitat specialists, and their ability to traverse terrestrial landscapes is limited. Because faunal exchange among water bodies is restricted, there is a considerable degree of local endemism (high -diversity) and species often have small geographic ranges, resulting in high species turnover (-diversity) among basins and accounting for the richness (in per unitarea terms) of freshwater fishes [29]. An important conservation implication is that river basins (especially those R964

in latitudes unaffected by recent glaciation) are not fully ‘substitutable’ in biodiversity terms [30]; thus, protection of one river or lake does not conserve a representative portion of the regional species total (-diversity). Thus, loss of a species from one water body could represent global extinction. The next great extinction? Freshwater biodiversity is in a state of global crisis with freshwater species generally far more imperiled than their terrestrial counterparts [5,31]. Inadequate knowledge of tropical freshwater biodiversity [28] could mean the extent of the threat is even greater. Population trend data [32,33] show that declines in freshwater species (3.9% annually since 1970) are consistently greater than those on land (1.1%; Figure 2), and the IUCN Red List (www.redlist.org) reveals that 22.5% (almost 6,000 out of 26,400 species assessed) of them are threatened. A similar proportion is classified as ‘data deficient’ (DD), indicating that data on distribution and abundance are insufficient for conservation assessment. As for frogs, 30% are at risk but another 26% are DD. The DD

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classification in the Red List is qualified by the remark that species with a circumscribed range that have not been recorded for some time may deserve threatened status; many might well be gravely endangered [34]. Human activities have already transgressed planetary boundaries for terrestrial and marine biodiversity, with species losses at least one to two orders of magnitude in excess of background extinction rates recorded from the fossil record [23]. If this is so, we have certainly far exceeded whatever reductions would have been sustainable for freshwater biodiversity. In intensively developed regions, especially those where human water requirements have been secured by investment in river engineering and water treatment, over one third of the species in major animal groups are threatened, including 38% of the fish species in Europe and 39% in North America. Other notable examples of species declines [5,31] are large river fishes worldwide and Asian freshwater turtles, as well as extinction of the Yangtze River dolphin (Lipotes vexillifer). In April 2019, the demise of the last known female Yangtze soft-shelled turtle (Rafetus swinhoei: Figure 3) received wide media coverage. The extent of the declines and losses of freshwater biodiversity that have been documented is probably a reliable indicator of the extent to which current practices are unsustainable [5]. There has been a ‘great thinning’ (sensu [35]) in abundance of freshwater animals, a ‘great shrinking’ in body size as large species are overexploited, and a ‘great mixing’ of biotas as freshwater invasions proceed, so that the label Homogenocene (sensu [13]) may be just as appropriate as Anthropocene for the current epoch. Irrespective of this, trajectories of human population growth, water use and consequential environmental alterations will continue to rise steeply in the foreseeable future (the ‘great acceleration’: sensu [1]), putting freshwater biodiversity at evergreater risk. What is needed? What can be done to alleviate the tragedy of the freshwater commons? Or avert further damage and species declines? An obvious starting point is the necessity to raise awareness — from citizens

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Magazine to policymakers — of the remarkable richness of freshwater biodiversity. This must be linked to information about the many threats and consequent degree of endangerment that prevails. It is, however, one thing to enlighten people about the hidden or overlooked biodiversity of inland waters, but quite another to mount persuasive arguments for their protection. A fundamental feature of the tragedy of the freshwater commons is that individuals must limit their own actions in order to maintain the communal good. In the Anthropocene world, limitations upon human activities intended to preserve biodiversity, and justifications of allocations of water for nature, will need to be extraordinarily persuasive. How, then, can progress be made? Two options seem possible, but these are not mutually exclusive, and other alternatives need not be ruled out. First, the argument for preservation of freshwater biodiversity can be made on utilitarian grounds: i.e. preservation of biodiversity is worthwhile for humans — hence we should limit our selfish degradation of the commons — because of the goods and services that more-or-less intact ecosystems offer. This argument suffers from the shortcoming that it is by no means evident that the services provided by river ecosystems (e.g. provision of clean water, flood control, and so on) require preservation of all of the species present in those systems, and it has little traction when some stakeholders gain economic benefit from projects that degrade the ecological underpinning of the freshwater commons. Nonetheless, the supply of ecosystem goods, such as the yield of protein from capture fisheries, may be enhanced by maintaining rivers in near-natural states with intact food chains [36], especially where many species are exploited. This rationale has been applied in attempts to limit dam construction along the mainstream of the lower Mekong that are likely to devastate the world’s most productive freshwater fishery [21]. Even here, where there is an unambiguous link between biodiversity and service provision, the ecosystem services are degraded to the detriment of food security for millions [37]. More generally, many people in the world

do not eat much animal protein, but what they do eat is mostly freshwater fishes. They provide the equivalent of all dietary animal protein for 158 million people, with poor and undernourished populations particularly reliant on inland subsistence fisheries [38]. However, not all rivers sustain economically valuable fisheries, or the fishery may be based on one or a few species. In such cases, managing the river for other uses (e.g. some combination of water supply, navigation and hydropower), or in a manner that favours productivity of the most desirable fishery species, may maximize net economic benefit even if it fails to bring about the best outcome for biodiversity. Some conservationists (e.g. [39]) would argue for another option: to assert that freshwater biodiversity deserves preservation, in and of itself, because of its existence value. This stance arises from an ethical or intergenerational imperative, and comprehension of the shared evolutionary history of all life on Earth. Unfortunately, it may fail to offer sufficiently strong justification for prioritizing freshwater biodiversity conservation over human needs for clean water and sanitation, nor will it serve to satisfy the expectations of growing populations who wish to enjoy improved standards of living. Moreover, freshwater animals are often non-charismatic — appearing quite similar to non-specialists — with little contemporary relevance for most people. Still, much remains to be done. Offsetting some of the effects of dams is possible if their operation is adjusted to ensure allocation of sufficient water to sustain ecosystems and biodiversity downstream. These environmental requirements must be compared with the water needed to produce goods and services for society, allowing identification of places where water conflicts will be most intense and that therefore require urgent action to address conservation and management challenges. A great deal of research on environmental flow allocations has been undertaken, and scientists have good understanding that maintaining the dynamic and variable nature of river flows is a prerequisite for protecting freshwater biodiversity

(e.g. [40]). This well-cited framework for development of flow standards is evidence of progress in that it challenges the resource-management paradigm directed towards control of hydrological variability, enhancing predictability for humans, plus the imperative to ‘balance’ resource protection and development [40]. Although environmental water allocations are more often planned than implemented, and the outcomes have been mixed [41], there have been some successes with modification of the operation of small dams to enhance conditions downstream. A notable environmental water allocation was implemented downstream of the Three Gorges Dam (China), intended to enhance spawning by various carp of fisheries importance. Although a complete assessment has yet to be published, monitoring before and after implementation revealed an increase in eggs and larvae [42]. Adjusting the operation of the largest dam in the world to promote carp breeding shows the scale at which regulations, stakeholder engagement, and science can be combined to bring about environmental improvements. Development and implementation of action plans for the conservation of threatened species are needed if we hope to preserve these species into the Anthropocene. Such plans should identify measures needed to protect the target species, and incorporate population and/or habitat management, as well as regular monitoring. Attention also needs to be paid to DD species and their conservation status updated so that they can either be confirmed as currently non-endangered or become the subject of a targeted action plan. Research is needed to determine which species are most vulnerable to climate change and might therefore warrant conservation intervention, such as assisted translocation [31]. At present, potential climate-change ‘losers’ cannot be identified due to the paucity of data on the thermal tolerances of many freshwater species. The argument that we should not move animals around in order to avoid causing unanticipated harm cannot be equated with adopting the ‘precautionary principle’ because climatic shifts as the world warms may leave freshwater animals

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Magazine stranded within water bodies where temperatures exceed those to which they are adapted or to which they can adjust. Under these circumstances, doing nothing could result in more harm than the potential risks associated with translocation. While climate change represents an insidious existential threat to freshwater biodiversity — one that should emphatically not be underestimated — the immediate risks from dams, landuse change and pollution could be far greater, causing fish extinctions of around 150 times higher than natural rates [43]. These findings reinforce the view that action to conserve freshwater biodiversity in the Anthropocene should prioritize amelioration of immediate threats, rather than be diverted towards measures intended to mitigate the medium-term impacts of climate change. Such prioritization would enhance ecosystem resilience and could offer hope for the preservation of freshwater biodiversity, providing a basis for optimism that we may be able to address the pervasive but more gradual effects of climate change as the Anthropocene unfolds. It will not, however, be sufficient to address only the biophysical aspects of conservation. A fully integrated approach linked to global initiatives (such as the Sustainable Development Goals) that takes account of social and economic concerns, and the necessary changes in water governance, will be needed [44]. Conclusions Fresh waters are global hotspots of biodiversity, but they are also hotspots of endangerment. The same environmental factors bringing about the initial pattern of richness are responsible for the susceptibility of that biodiversity to anthropogenic threats. The current array of threats to freshwater environments is distinctive, and, as human populations and water needs expand, threat intensity will increase. Climate change will further amplify their effects, while adaptation to a higher frequency of climatic extremes will spur pharaonic water-engineering schemes unlikely to favour biodiversity. Amelioration of proximate threats to freshwater biodiversity must be combined with broader-scale measures (emissions R966

reductions) to limit climate change. The first requires immediate action but, without the second, will have only short-term benefits for biodiversity. However, failure to relieve proximate threats will constrain the resilience of freshwater ecosystems and compromise their biotas, leaving them vulnerable to further species loss even under an optimistic scenario where Anthropocene carbon emissions have been greatly reduced. ACKNOWLEDGEMENTS I am grateful to two anonymous reviewers for their constructive reports. I also thank Lily C.Y. Ng and Jia Huan Liew. Gerald Kuchling was kind enough to allow the use of his turtle photograph. REFERENCES 1. Steffen, W., Persson, A., Deutsch, L., Zalasiewicz, J., Williams, M., Richardson, K., Crumley, C., Crutzen, P., Folke, C., Gordon, L., et al. (2011). The Anthropocene: from global change to planetary stewardship. Ambio. 40, 739–761. 2. Steffen, W., Richardson, K., Rockström, J., Cornell, S.E., Fetzer, I., Bennett, E.M., Biggs, R., Carpenter, S.R., de Vries, W., de Wit, C.A., et al. (2015). Planetary boundaries: guiding human development on a changing planet. Science 347, 1259855. 3. Vörösmarty, C.J., and Sahagian, D. (2000). Anthropogenic disturbance of the terrestrial water cycle. BioScience 50, 753–765. 4. Vörösmarty, C.J., McIntyre, P.B., Gessner, M.O., Dudgeon, D., Prusevich, A., Green, P., Glidden, S., Bunn, S.E., Sullivan, C.A., Reidy Liermann, C., et al (2010). Global threats to human water security and river biodiversity. Nature 467, 555–561. 5. Dudgeon, D., Arthington, A.H., Gessner, M.O., Kawabata, Z., Knowler, D., Lévêque, C., Naiman, R.J., Prieur-Richard, A.-H., Soto, D., Stiassny, M.L.J., et al. (2006). Freshwater biodiversity: importance, threats, status and conservation challenges. Biol. Rev. 81, 163–182. 6. Grill, G., Lehner, B., Lumsdon, A.E., MacDonald, G.K., Zarfl, C., and Reidy Liermann, C. (2015). An index-based framework for assessing patterns and trends in river fragmentation and flow regulation by global dams at multiple scales. Environ. Res. Lett. 10, 015001. 7. Grill, G., Lehner, B., Thieme, M., Geenen, B., Tickner, D., Antonelli, F., Babu, S., Borrelli, P., Cheng, L., Crochetiere, H. et al. (2019). Mapping the world’s free-flowing rivers. Nature 569, 215–221. 8. Shumilova, O., Tockner, K., Thieme, M., Koska, A., and Zarfl, C. (2018). Global water transfer megaprojects: a solution for the waterfood-energy nexus? Front. Environ. Sci. 6, 150. 9. Lebreton, L.C.M., van der Zwet, J., Damsteeg, J., Slat, B., Andrady, A., and Reisser, J. (2017). River plastic emissions to the world’s oceans. Nat. Commun. 8, 15611. 10. Burns, E.E., Carter, L.J., Kolpin, D.W., ThomasOates, J., and Boxall, A.B.A. (2018). Temporal and spatial variation in pharmaceutical concentrations in an urban river system. Water Res. 137, 72–85.

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Chair of Ecology & Biodiversity, School of Biological Sciences, The University of Hong Kong, Hong Kong S.A.R., China. E-mail: [email protected]

Essay

The insect apocalypse, and why it matters Dave Goulson The majority of conservation efforts and public attention are focused on large, charismatic mammals and birds such as tigers, pandas and penguins, yet the bulk of animal life, whether measured by biomass, numerical abundance or numbers of species, consists of invertebrates such as insects. Arguably, these innumerable little creatures are far more important for the functioning of ecosystems than their furry or feathered brethren, but until recently we had few long-term data on their population trends. Recent studies from Germany and Puerto Rico suggest that insects may be in a state of catastrophic population collapse: the German data describe a 76% decline in biomass over 26 years, while the Puerto Rican study estimates a decline of between 75% and 98% over 35 years. Corroborative evidence, for example from butterflies in Europe and California (which both show slightly less dramatic reductions in abundance), suggest that these declines are not isolated. The causes are much debated, but almost certainly include habitat loss, chronic exposure to pesticides, and climate change. The consequences are clear; insects are integral to every terrestrial food web, being food for numerous birds, bats, reptiles, amphibians and fish, and performing vital roles such as pollination, pest control and nutrient recycling. Terrestrial and freshwater ecosystems will collapse without insects. These studies are a warning that we may have failed to appreciate the full scale and pace of environmental degradation caused by human activities in the Anthropocene. A key feature of the Anthropocene is the accelerating decline of biodiversity. Public perception of this loss is particularly focused on extinction events, especially those of large mammals such as the northern white rhino or birds such as the passenger pigeon or dodo. Sad though these events are, the actual proportion of species that have so far gone extinct during the modern era are relatively small. Just 80 species of mammal and 182 species of bird have been lost since 1500, representing 1.5% and 1.8%, respectively, of the known species [1] (note that this time period excludes the wave of extinctions that took place in the late Pleistocene when man first spread around the world). On the face of it, these figures would seem to be at odds with the notions that we are in the midst of the ‘sixth mass extinction event’, or that biodiversity is in crisis. However, evidence has recently begun to emerge suggesting that global wildlife has been affected far more profoundly than these relatively modest figures for actual extinctions might suggest. Most species may not yet have gone extinct, but they are, on average, far less abundant than they once

were. A recent landmark paper by Bar-On et al. [2] estimated that 83% of wild mammal biomass has been lost since the rise of human civilization. The scale of human impact is also revealed by their estimate that wild mammals now comprise just 4% of mammalian biomass, with livestock comprising 60% and humans the remaining 36%. They also calculate that 70% of global avian biomass is made up of domestic poultry. Also released in 2018 was the World Wildlife Funds and Zoological Society of London’s ‘Living Planet Report’ [3], which estimates that the abundance of the world’s wild vertebrates (fish, amphibians, reptiles, mammals and birds) fell by 60% between 1970 and 2014. I was born in 1965, and in my lifetime we have moved from an age of bio-abundance to one of bio-paucity. One has to wonder what wildlife will be left by the time my teenage children reach my age. Catastrophic though declines of wild vertebrates have been, it seems that another even more dramatic change may have been quietly taking place, one that may have more profound implications for human wellbeing. The large majority of known species are invertebrates, dominated

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