The Many Causes of Threat

Photo 6.1
The Golden-eyed Leaf Frog Agalychnis annae (Endangered) was once a common species in the mountains of Costa Rica. In the late 1980s, its populations crashed and it disappeared from almost all of its range, and now it survives only in heavily disturbed and polluted habitats in the suburbs of San José.
Photo: © Michael and Patricia Fogden.

6.1 Introduction

The influence of human activities on wild species has grown at an unprecedented rate. Although some species respond positively to anthropogenic pressures, the great majority show only limited tolerance of increasingly widespread and rapid changes to ecosystems worldwide. The major humaninduced impacts on biodiversity are: habitat destruction and fragmentation; invasive alien species; over-utilization; disease; pollution and contaminants; incidental mortality; and climate change.

In the 2004 IUCN Red List of Threatened SpeciesTM, data on threats to species have been collated comprehensively for all amphibians and all threatened birds, and also for 78% of threatened mammals, and so the analyses presented here are restricted to these three groups. However, because birds, mammals and amphibians are not fully representative of species as a whole, some case studies to illustrate important threats in some other taxonomic groups are also included.

Analyses of the data on threats to bird, mammal and amphibian species evaluated for the 2004 IUCN Red List (for methods, see Appendix 2f) show that the most pervasive threat that they face is habitat destruction and degradation (see Figure 6.1) driven by agricultural and forestry activities. Over-exploitation, invasive alien species, pollution and disease are other important threats, but birds, mammals and amphibians differ in terms of the relative importance of these. Incidental mortality, human disturbance and persecution have so far had less impact in terms of the total numbers of species affected, but they can be serious for some susceptible groups. Climate change as a result of human activity is a major, and relatively recent threat, but its impacts on species are difficult to detect, especially since it probably operates to some extent by increasing the impact of other factors (for example disease in amphibians). In addition, the impacts and expected consequences of climate change are uncertain and often fall outside the time window used for Red List assessments. Recent work examining the potential consequences of climate change across a range of global habitats suggests that it could ultimately lead to the extinction of 15 - 37% of the species in their sample (Thomas et al. 2004). The impact of climate change is not included in the following analyses but IUCN is actively examining ways to integrate climate change impacts into the Red List assessments.

Figure 6.1
The major threats to globally threatened mammal, amphibian and bird species (definitions of high, medium and low impact for birds are given in Appendix 2f).

6.2 Habitat Destruction and Degradation

It is estimated that since historical times the world has lost c. 40% of its original 60 million km2 of forest cover through human activity (FAO 1997b). This loss continues today with c. 14.6 million hectares of forests destroyed each year, totalling a 4.2% loss of natural forest cover during the 1990s, with the rates of loss being highest in Africa and South America (FAO 2000). It is no surprise therefore, that habitat destruction is a major threat to the world's biodiversity. For many species the habitat degradation that accompanies selective resource exploitation, or that occurs in habitats next to cleared areas, can have serious negative consequences too.

Many tropical forest species, for instance, rely on pristine or near-pristine primary forest, and show low tolerance to selective logging. The problem is made worse by the fragmentation of natural habitats which results in smaller, more isolated sub-populations, with reduced possibilities for dispersal and increased risks of local and ultimately global extinction.

Photo 6.2
Deforestation in the Amazonian forests.
Photo: © Jean-Christophe Vié.

Photo 6.3
Selective logging in southeast Asia.
Photo: © Sue A. Mainka.

Photo 6.4 Wheat fields in southern Africa.
Photo: © Craig Hilton-Taylor.

Photo 6.5
Dam construction in Africa.
Photo: © Craig Hilton-Taylor.

Figure 6.2
The key drivers of habitat destruction affecting bird species (source: BirdLife International 2004b).

Habitat destruction and degradation is the major threat faced by globally threatened birds and amphibians affecting 86% and 88% of threatened species (1,045 and 1641 species respectively; see Figure 6.1), and 86% (652 species) of the 760 threatened mammals for which data are available (Figure 6.1). This is because the majority of these species occur in tropical forests, where the most serious habitat loss is taking place (Figures 5.1, 5.2 and 5.3).

It has been possible to examine some of the key drivers of habitat destruction using the bird data (see Figure 6.2). Of the 1,045 globally threatened birds affected by habitat destruction, large-scale agricultural activities (including crop farming, livestock ranching, and perennial crops such as coffee and oil palm) impact nearly half. A similar proportion is affected by smallholder or subsistence farming. Selective logging or tree-cutting and general deforestation affect some 30%, firewood collection and the harvesting of non-woody vegetation affect c. 15% and conversion to tree plantations some 10%. Overall, over 70% and 60% of globally threatened birds are impacted by agricultural and forestry activities respectively. Infrastructure development (including human settlement and industrial development) is a threat to over 30% of globally threatened birds.

Habitat loss is not restricted to deforestation, and it is noteworthy that preliminary evidence suggests that this is the most serious threat to freshwater fish, and also affects over 40% of marine species in the North American assessment (see Box 6.1). In freshwater, habitat loss includes factors such as dam construction, dredging, and canalization.

Box 6.1 Threats to Fishes

Over-exploitation has been implicated as the leading threat to the world's marine fishes (Reynolds et al. 2002; Dulvy et al. 2003; Hutchings and Reynolds 2004). The IUCN Red List's coverage is too sparse and patchy to provide a comprehensive survey of threats. However, a fairly complete assessment of the status of North American marine fishes carried out by the American Fisheries Society (Musick et al. 2000b) suggests that 55% of the 82 fishes considered to be threatened with extinction have suffered from over-exploitation (see Figure Box 6.1.1 below). These species were assessed using different criteria from those used by the IUCN, but this is unlikely to affect the conclusion that overexploitation is the main problem. Those species that are most susceptible often suffer from a combination of high value and catchability (e.g., forming spawning aggregations), as well as low intrinsic rates of population turnover associated with late maturity (Reynolds et al. 2002; Dulvy et al. 2003). Thus, large groupers, croakers, sharks, and skates are of particular concern. It remains to be seen whether habitat destruction could eventually supplant over-exploitation as the main threat globally, given the recent widespread degradation of coral reefs, exacerbated by climate change, and development pressures on coastal habitats.

For freshwater fishes, there is strong evidence that habitat loss is more important than over-exploitation as a cause of threat (see Figure below). In this respect, freshwater fishes are similar to birds and mammals. These data are based on very conservative estimates of the number of species that are extinct, or probably extinct, globally (Harrison and Stiassny 1999). As with marine species, IUCN assessments of freshwater fishes are too sparse for confident predictions about true percentages that are under threat. However, preliminary analyses suggest that for the 20 countries for which assessments are most complete in the Red List, 17% of freshwater fish species are threatened. This estimate is comparable to the 20% figure suggested by Leidy and Moyle (1998). Unlike the case for marine fishes, freshwater species are also facing additional growing threats from introductions of alien species. Anadromous fishes, which migrate between marine and freshwaters, feature especially prominently on threatened lists, especially those that are large-bodied and late-maturing. They are usually valuable to fisheries and susceptible when passing through bottlenecks (which are often blocked by dams). The world's sturgeon species combine the worst of all of these features, and most are Endangered or Critically Endangered.

Photo 6.6
The Shark Ray or Bowmouth Guitarfish Rhina ancylostoma (Vulnerable) is a widely distributed Indo-west Pacific inshore species taken by multiple artisanal and commercial fisheries throughout its range both as a target species and as bycatch. Flesh is sold for human consumption in Asia and the fins from large animals fetch exceptionally high prices.
Photo: © Jeremy Stafford-Deitsch.

Figure Box 6.1
The relative importance of different threatening processes facing North American marine fishes (taken from Musick et al. 2000b), and having caused extinctions among freshwater fishes globally (taken from Harrison and Stiassny 1999). The data are expressed as percentages of species in each sample affected by a particular threat (sample size is 82 species for North American marine fishes, and 164 species for extinct or probably extinct freshwater fishes). In the freshwater graph, individual species have often been coded against more than one threat.

Based on information provided by John D. Reynolds and Nicholas B. Goodwin

6.3 Over-exploitation

Humans have harvested and traded species since time immemorial: for food, medicine, fuel, material use (especially timber), and for cultural, scientific and leisure (i.e., sport) activities. This use of nature is fundamental to the economies and cultures of many nations (e.g., Mainka and Trivedi 2002). For example, wild meat is not only a vital source of protein, but also generates valuable income for rural populations. However, expanding markets and increasing demand, combined with improved access and techniques for capture, and increased ease of transportation and techniques of preservation, are causing the exploitation of many species beyond sustainable levels.

Over-exploitation has been identified as a major threat faced by globally threatened birds and amphibians affecting 30% and 6% of threatened species respectively (see Figure 6.1) and 33% of the 760 threatened mammals for which data are available (Figure 6.1).

Threatened mammal species appear to be more impacted by over-exploitation than either birds or amphibians, and it is likely that when the mammals are fully coded for their threats, over-exploitation will prove to affect an even higher percentage of species than is indicated on Figure 6.1. Data in the 2004 Red List indicate that 250 species of threatened mammals are subject to over-exploitation, and larger mammals, especially ungulates and carnivores, are particularly targeted. Mammals are used extensively in the wild meat trade, notably in tropical Africa and in southeast Asia (Bakarr et al. 2001; Robinson and Bennett 2000). Some mammal species are also harvested for medicinal use, especially in eastern Asia.

In all, 345 globally threatened birds are threatened by over-exploitation for human use, primarily through hunting for food (262 species) and trapping for the cage-bird trade (117 species). The species that are targeted are often large and conspicuous, such as cranes and storks. Some families are particularly affected, with more than 10% of their species threatened by over-exploitation. Many species are at risk in some cases, including 52 species of parrots and 44 species each of pigeons and pheasants. Other families, notably waterfowl, birds of prey and rails, are also heavily hunted, although smaller proportions are affected overall. Nearly all countries and territories of the world (212, 89%) harbour bird species that are threatened by overexploitation, but this threat appears to be particularly prevalent in Asia.

There are 133 threatened amphibian species known to be utilized by humans, mainly for the pet trade (84 species), food (79 species) and medicine (31 species). Although utilization of a species is not necessarily a major threat to the species' survival, for 104 amphibians it is. Most amphibians threatened by exploitation for food and medicine are found in Asia, and many of the species in the pet trade are found in South America and Madagascar. In Asia, exploitation for food is mainly directed towards the larger-bodied species of the family Ranidae, as well as, for example, the Chinese Giant Salamander Andrias davidianus that is listed as Critically Endangered. The species in the pet trade are usually salamanders and the colourful small frogs, in particular of the genera Dendrobates, Epipedobates and Mantella.

For some groups of species, and in some ecosystems, over-exploitation is a particularly serious threat. Examples include the turtles and tortoises in eastern and southeastern Asia, where almost all species are in serious decline as a result of harvesting for human consumption and medicine, mainly in China (see Box 2.2). Many of these species have deteriorated in Red List status over the last decade. Since 1996, the number of Critically Endangered turtle species has increased from 10 to 25, and the number of Endangered turtle species from 28 to 47. This near doubling of the number of seriously threatened turtle species in less than ten years is almost entirely due to over-utilization.

The evidence so far available suggests that overexploitation is the most serious threat to marine fish species (see Box 6.1). Extensive over-utilization of other marine species has been well documented for groups such as marine turtles, whales and marine invertebrates.

Photo 6.7
There is still an active and lucrative market for animal furs and skins in some Asian countries.
Photo: © Sue A. Mainka.

Photo 6.8
Parrots and a cracid trapped and killed in South America for the wild meat trade.
Photo: © Jean-Christophe Vié.

Photo 6.9
This species of crocodile newt, Tylototriton shanjing (Near Threatened) is known from central, western and southern Yunnan, China. Although still very common in parts of its range, over-harvesting for use in traditional Chinese medicine is becoming a serious threat. It is also becoming popular in the international pet trade.
Photo: © Henk Wallays.

Photos 6.10 and 6.11 (top to bottom)
Turtle shells and dried seahorses are both used extensively in traditional medicine and large quantities are offered for sale in Asian markets.
Photo: © Sue A. Mainka.

Photo 6.12
The invasive alien Black Rat Rattus rattus (Least Concern) has a marked impact on the native faunas of island states. The rat here is taking a New Zealand Fantail Rhipidura fulginosa (Least Concern) chick. Although the Fantail is very widespread, the rat could have a marked impact if introduced to all islands within the bird's range.
Photo: © David Mudge.

6.4 Invasive Alien Species

Humans have been transporting animals and plants from one part of the world to another for thousands of years, sometimes deliberately (e.g., livestock released by sailors onto islands as a source of food) and sometimes accidentally (e.g., rats escaping from boats). In most cases, such introductions are unsuccessful, but when they do become established as an invasive alien species (defined by IUCN (2000) as “an alien species which becomes established in natural or semi-natural ecosystems or habitat, is an agent of change, and threatens native biological diversity”), the consequences can be catastrophic. Invasives can affect native species directly by eating them, competing with them, and introducing pathogens or parasites that sicken or kill them or, indirectly, by destroying or degrading their habitat. Invasives have been identified as a major threat faced by globally threatened birds and amphibians affecting 30% and 11% of threatened species (326 and 212 species respectively; see Figure 6.1) and 8% of the 760 threatened mammals for which data are available (Figure 6.1).

Island species are particularly susceptible to invasives because of their isolated evolutionary history, with 67% of oceanic-island globally threatened birds affected directly or indirectly by invasive species, compared to 17% on continental islands and just 8% on continents (see Figure 6.3). This susceptibility is spectacularly illustrated by the demise of Polynesian Partulid snails (see Box 6.2). The much lower percentages of threatened mammals and amphibians affected by invasives than birds are probably a reflection of the limited abilities of these groups to colonize oceanic islands.

Figure 6.3 The percentage of globally threatened birds affected by invasives, comparing islands and continents.

Box 6.2 The Demise of Polynesian Partulid Snail

Since the 1970s, French Polynesia has seen one of the most dramatic examples of extinction caused by an invasive species. Seventy-two percent of the Partula snail species native to the Society Islands have gone extinct as a result of the introduction of the predatory Wolf Snail Euglandina rosea (T. Coote pers. comm.). The Wolf Snail was originally introduced to Tahiti in 1975 as a biological control agent with the aim of halting the spread of the Giant African Snail Achatina fulica. However, E. rosea instead developed a taste for the smaller partulid snails (genera Partula and Samoana) and their rapid decline began. The invasive Wolf Snail was not confined to Tahiti. It spread rapidly, at a rate of approximately 1.5 km2 per year (T. Coote pers. comm.). By 1977 it had reached Moorea and by 1992 it was present on all six Society Islands.

The greatest loss of Partulid diversity occurred on the island of Raiatea. In a twelve-year period following the introduction of E. rosea in 1986, all 33 native Partula species disappeared in the wild (T. Coote pers. comm.). Just four of Raiatea's Partula species remain alive in captivity. It is possible that the only species in the genus Samoana (S. attenuata) has also disappeared.

The success of ex situ conservation efforts is vital if the last surviving individuals of species that are Extinct in the Wild are to be maintained. Fifteen Partula and possibly one Samoana species are currently Extinct in the Wild. The International Partulid Conservation Programme (IPCP) was established in 1994, and today 22 Partulid taxa (19 species and three subspecies) are maintained and bred in fifteen collaborating zoos worldwide. In addition the IPCP and their local collaborators perform and support studies on the population dynamics of native and alien species in the wild, and investigate methods for the in situ conservation of partulid snails.

The in situ conservation effort has enabled the development of predator proof Partulid reserves (initially on Moorea and most recently on Tahiti) aimed at protecting surviving wild Partulid populations and providing a mechanism by which the Extinct in the Wild species might be reintroduced (Coote et al. 2004). These reserves have informed the development of similar reserves on Hawaii to protect threatened Achatinelline tree snail species from the same invasive predator threat. The IPCP is currently assisting the French Polynesian Government develop a conservation strategy for the region's endemic molluscs and their associated habitats (P. Pearce-Kelly pers. comm.).

Unfortunately there is no immediate possibility of completely eradicating E. rosea from the many Polynesian islands it has now invaded, but the above conservation effort, together with possible future developments of species-specific control methods provide hope that the remaining Partulid species might yet have a viable future.

Based on information provided by Trevor Coote, Paul Pearce-Kelly and Mary Seddon, IUCN/SSC Mollusc Specialist Group

Photos 6.13 and 6.14
The Partulid reserve on the island of Moorea, Tahiti. Inset is Partula saturalis strigosa (Extinct in the Wild), which can possibly be reintroduced into such a reserve in the future.
Photo: © Dave Clarke.

6.5 Disease

Diseases can cause chronic population declines, dramatic die-offs or reductions in the reproductive success and survival of individual species. Some diseases now appear to be spreading to populations previously unaffected, including to species already seriously threatened by other factors. Invasive diseases have already been implicated in the extinction of some species. Overall, diseases (both native and invasive) affect some 5% of globally threatened birds (67 species). For threatened mammals, only 26 species (3% of the 760 species for which data are available) are impacted by disease (Figure 6.1). However, it is the amphibians that are particularly affected by disease with some 17% of threatened species potentially impacted (317 species; see Figure 6.1).

Amphibian species have been recorded as declining since the early 1970s but initially conservationists assumed that factors such as habitat loss were to blame. By 1988 these declines had become much more serious: for example, at one site in Costa Rica, 40% of the amphibian fauna disappeared over a short period in the late 1980s (Pounds et al. 1997). Reports of declines and extinctions accelerated during the 1990s but it wasn't until 1996 that 0he cause was linked to an emerging, highly pathogenic disease, following a study that looked at the pattern of disappearances of 14 species of frogs endemic to Australia's east coast (Laurance et al. 1996). In 1998 a previously unknown chytrid fungus, named Batrachochytrium dendrobatidis, was identified as the agent (Berger et al. 1998; Longcore et al. 1999), and this has now been implicated in many reported amphibian declines.

Three aspects of the biology of B. dendrobatidis help to explain the observed patterns of amphibian decline. First, this chytrid will grow in culture only in cool temperatures. This may explain why montane species are more likely to decline than lowland species and why the disease expresses itself in the winter in Arizona, United States (Bradley et al. 2002). Second, B. dendrobatidis appears to occur only in aquatic habitats, which would explain why amphibians that spend at least part of their life cycle near streams are more likely to decline. Third, chytrids attack the keratinized beak of tadpoles, explaining why tadpoles in affected areas can be missing their beaks. Examination of museum specimens of frogs shows that chytrids were present in the United States as early as 1974 and in Australia as early as 1978 (Carey et al. 1999; Pounds and Puschendorf 2004), dates that are close to the times that declines were first noted. More recently, studies in Africa have shown the presence of chytrids dating as far back as the 1930s, suggesting an African origin of B. dendrobatidis (Weldon et al. in press).

Photo 6.15
The decline of the harlequin toad, Atelopus varius (Critically Endangered), in Costa Rica and Panama has been dramatic. It has disappeared from suitable habitats, and the cause of its decline might be the fungal disease, chytridiomycosis, the incidence of which might be related to extreme climatic events, in particular drought.
Photo: © Rober Puschendorf.

Photo 6.16
Torrent Tree Frog Litoria nannotis (Endangered) endemic to the wet tropics of north Queensland, Australia is undergoing rapid decline, even in protected areas, possibly due to the incidence of the fungal disease chytridiomycosis.
Photo: © Ross Alford.

Although amphibians have been far more heavily impacted by disease than any group so far studied, it can also be important in other groups of species. Diseases such as canine distemper and rabies can have a major impact on large carnivores. For example, approximately 80% of the Web Valley population of the Endangered Ethiopian Wolf Canis simensis died in a rabies outbreak in 2003 (S. Williams in litt.), and the African Lion Panthera leo population in the Serengeti National Park was heavily impacted by canine distemper in 1994 (Roelke-Parker et al. 1996). Disease has also been a factor in the extinction of three bird and one plant species over the last 20 years (see Tables 3.2 and 3.3). There is concern that, as a result of increasingly widespread and serious environmental changes, newly emerging diseases will become a much more serious threat to species (Daszak et al. 2001).

Photo 6.17
The accidental introduction of mosquitoes Culex quinqufasciatus, bringing with them avian malaria Plasmodium relictum and avian pox Poxvirus avium, has had devastating consequences on Hawaiian birds. An Apapane Himatione sanguinea (Least Concern) and mosquito are shown here.
Photo: © Jack Jeffrey Photography.

Photo 6.18
Canine distemper impacted the African Lion Panthera leo (Vulnerable) population in the Serengeti National Park, Tanzania.
Photo: © Troy Inman.

Photo 6.19
The once abundant White-rumped Vulture Gyps bengalensis (Critically Endangered) has declined dramatically in South Asia due to the toxic effects of a veterinary drug, Diclofenac.
Photo: © Guy Shorrock / RSPB Images.

6.6 Pollution and Contaminants

Pollution directly affects species through mortality and sublethal effects such as reduced fertility. Pollution can also have strong indirect effects by degrading habitats or reducing food supplies. Overall, pollution affects some 12% and 29% of globally threatened bird and amphibian species (187 and 529 species respectively; see Figure 6.1) and 4% (28 species) of the 760 threatened mammals for which data are available (Figure 6.1). The much higher percentage of threatened amphibians impacted by pollution than birds or mammals is probably a reflection of the larger number of species that are dependent on aquatic ecosystems.

Perhaps the most dramatic recent example of the potentially devastating effects of pollution on wild species relates to vultures (Oaks et al. 2004; Schultz et al. 2004). In South Asia, vultures in the genus Gyps have declined by more than 95% in recent years owing to the toxic effects of a veterinary drug, Diclofenac, which is consumed when the birds feed on carcasses of animals treated with the drug.

Diclofenac is widely used in human medicine globally, but was introduced to the veterinary market on the Indian subcontinent during the early 1990s. Vultures have traditionally disposed of carcasses in cities, villages and the countryside, reducing the risk of disease and helping with sanitation. With the vultures gone, carcasses are likely to take much longer to be stripped, increasing the risk to human health. Feral dogs are filling the scavenging void, and their growing numbers also increase health and safety risks, as they are carriers of rabies. There is now an urgent need to control the veterinary use of the drug, and to establish captive breeding populations of the three vulture species concerned.

6.7 Incidental Mortality

For a few threatened species, incidental mortality can be the greatest threat. For example, the growth of longline fishing around the world is an increasing threat to many marine species. Albatrosses, for example, are coming into increasing contact with commercial fishing fleets, leading to the death through bycatch of thousands of individuals. All 21 species are now evaluated as globally threatened or Near Threatened, largely because of interactions with fisheries. It will take many years for these long-lived, slow-breeding species to recover from serious declines; assuming that such declines can actually be halted. Other groups of seabirds, such as penguins and petrels, are also heavily impacted by this threat. Overall, 83 species of threatened birds (7%) and 44 species of threatened mammals (6% of the species for which data are available) are affected by incidental mortality. For amphibians, this is a minor threat.

Photo 6.20
Black-browed Albatross Thalassarche melanophrys (Endangered) caught on a baited longline.
Photo: © Fabio Olmos.

Incidental mortality has also caused major declines in other marine species, examples include six species of sawfish (Pristis spp. – four species Endangered and two Critically Endangered), the Leatherback Turtle (Dermochelys coriacea – Critically Endangered), the Vaquita (Phocoena sinus – Critically Endangered), and Hector's Dolphin (Cephalorhynchus hectori – Endangered).

6.8 Climate Change

The Earth is undergoing profound changes to its climate. There is now little doubt that this results from human activities, mainly the burning of fossil fuels. Climatic changes have occurred throughout Earth's history. However, these recent changes are different because they are taking place faster and are unlikely to be reversed by natural processes. As yet few species have been identified as being threatened on the IUCN Red List specifically owing to climate change. However, there are many examples of the effects of climate change on species from around the world, which taken together, provide compelling evidence that climate change will be catastrophic for many species. Climate change may alter species' distribution, abundance, phenology (the timing of events such as migration or breeding), morphology (size and shape), and genetic composition.

Modelling studies show that the ranges occupied by many species will become unsuitable for them as the climate changes. The climate space that is suitable for particular species may shift in latitude or altitude, contract or even disappear. Many species will probably not be able to keep up with their changing climate space. As species move at different rates, the community structure of ecosystems will also become disrupted. Both local and global extinctions are likely. One recent global study estimated that 15–37% of regionally endemic species could be committed to extinction by 2050 (Thomas et al. 2004), while another study in Queensland, northern Australia, shows that the number of extinctions will increase rapidly if temperatures rise by more than c. 2°C (Williams et al. 2003). Some groups of species will be particularly hard hit, for example the Proteaceae, a plant family with many endemic species in South Africa (see Box 6.3).

Extreme weather events, most likely a result of climate change, have been shown to correlate with amphibian declines in a few areas. In three tropical regions (highland Costa Rica, Andean Ecuador, and montane Puerto Rico), the requisite combination of amphibian population and climate data are available for analysis. In the highland Costa Rica site, 20 species of frogs and toads, including the Golden Toad Bufo periglenes, declined or disappeared abruptly in 1988, with subsequent abrupt declines of survivors in 1994 and 1998. Each of these decline events occurred during unusually dry periods when typical periods of cloud-borne mist failed to occur (Pounds et al. 1999). Andean Ecuador was home to the spectacular Jambato Toad Atelopus ignescens, which abruptly disappeared from 47 sites from where it was known in the 1980s, just after the two driest years recorded during the period 1962 – 1998 (Ron et al. 2003). Similarly, dry weather is correlated with the disappearance of three species and the decline of six species of frogs from the genus Eleutherodactylus in Puerto Rico (Burrowes et al. 2004). It is now considered likely that there is an interaction between the chytrid fungus linked to amphibian declines (see Disease in 6.5 above) and extreme climatic events (droughts) (Ron et al. 2003; Burrowes et al. 2004).

The timescale over which climate change is likely to lead to extinctions of some species is probably longer than the 100-year period that is most commonly used in the IUCN Red List. IUCN is working on developing new methods to identify species and habitats that are susceptible to climate change through a recently constituted task force.

6.9 Other Threats

The remaining threats, such as human disturbance, natural disasters, changes in native species dynamics, and persecution generally affect relatively small numbers of threatened birds, mammals and amphibians (Figure 6.1). However, some of these can have important impacts on particular groups of species. A notable example among mammals, are large carnivores, for which persecution is often the most serious threat.

Box 6.3 Extinction Risk from Future Land-Use and Climate Change – the Proteaceae in the Cape Floristic Region of South Africa

In South Africa's Cape Floristic Region, agriculture, invasive alien plants and urbanization have severely impacted many endemic plants and animals. This is reflected in some 1,400 plant species listed in the national Red List at present (Hilton-Taylor 1996). In the future, climate change is expected to be an additional major threat to biodiversity in this unique region at the southern tip of Africa (Midgley et al. 2002, 2003). The Proteaceae are one of the three characteristic plant families in the fynbos (the major vegetation type in the Cape Floristic Region), and they have been extensively mapped and studied through the Protea Atlas Project at South Africa's National Botanical Institute (now the South African National Biodiversity Institute).

Using spatially explicit predictions of future threats to biodiversity, Bomhard (2004) has investigated the potential impacts of future land-use and climate change on the extinction risk of the Proteaceae. He calculated a future Red List status for 229 Proteaceae species endemic to the Cape Floristic Region for the year 2020, and compared it to their currently proposed Red List status. For this study, different land-use and climate change scenarios were developed for 2020. Two of these scenarios considered only the impacts of future habitat transformation (i.e., the spread of agriculture, invasive alien plants and urbanization), providing a worst-case and best-case scenario of future land-use conditions in the region. Two other scenarios, identical in their consideration of land-use change, included the impacts of rapid anthropogenic climate change.

From the present to 2020, up to 54 of the 229 Proteaceae species could be uplisted by up to three threat categories, and the proportion of threatened species could rise by up to 6% under the overall worst-case scenario (see Figures Box 6.3.1 and Box 6.3.2 below). With increasing threat levels, the number of Least Concern species decreases from 75 at present to 53 under the overall worstcase scenario, whereas the number of Critically Endangered and Extinct species increases, particularly under the climate change scenarios. For example, the number of Critically Endangered species increases from three at present to six with high habitat transformation and 12 with climate change and high habitat transformation. There are no extinctions predicted due to land-use change according to these simulations, but four of the study species could become extinct due to climate change.

Photo: © Nick Helme.

Photo: © Nigel Forshaw.

Photos 6.21 and 6.22 The Redelinghuys Pincushion Leucospermum arenarium (Endangered) and the Malmesbury Conebush Leucadendron thymifolium (Endangered) are both examples of the protea family that are likely to be impacted by climate change in the future.

Figure Box 6.3.1
Red List status of all study species under current conditions; low and high future habitat transformation excluding climate change (LT - CC, HT - CC); and low and high future habitat transformation including climate change (LT + CC, HT + CC).

With changing climates, some currently suitable habitats will become unsuitable, and if species cannot move to areas where future climates are suitable for them, they are eventually committed to extinction. It is predicted that the worst affected areas will be the low-lying areas on the West Coast and Southwest of the Cape Floristic Region. Such species and regions of concern can now be prioritized for monitoring and planning; eventually leading to appropriate conservation action guided by the principles of climate change integrated conservation strategies (Hannah et al. 2002a and b).

Figure Box 6.3.2
Change in Red List status (number of categories downlisted or uplisted) of all study species for the future compared to current conditions. Future scenarios are low and high habitat transformation excluding climate change (LT - CC, HT - CC), and low and high habitat transformation including climate change (LT + CC, HT + CC).

Based on information provided by Bastian Bomhard

6.10 Threatening Processes and Patterns of Extinction

The threats described so far are proximate external threats or pressures. Their impact is affected by various other factors (described below) and, as a result, substantial differences in the patterns of threat and extinction are observed both between different groups of species (e.g., birds versus amphibians) and within similar groups of species (e.g., a family or genus of birds or amphibians).

6.10.1 Spatial Variation in Threats

Human populations are growing and influencing the environment differently in different parts of the world (see Section 7). In general, species face the highest threats when people arrive or rapidly expand their activities in a particular region, and many recent extinctions have followed patterns of human exploration and settlement, especially on islands (MacPhee and Flemming 1999). For example, the earliest Pacific island migrations led to the extinction of probably thousands of species (Olson et al. 1982; Steadman 1995), and the rapid expansion of intensive agriculture in northwestern Europe led to declines in farmland bird species (Robinson and Sutherland 2002).

Current examples can be seen in the Red List information. For example, of the 435 amphibian species that qualify for a more threatened IUCN category than they did in 1980, species fall into three groupings: those experiencing heavy exploitation (55 species mainly in East and Southeast Asia); those experiencing significant habitat loss (198 species, especially in Southeast Asia, West Africa, and the Caribbean); and those experiencing declines, even where suitable habitat remains, for reasons that are not fully understood, although disease interacting with climate change is emerging as the most likely cause (189 species, mainly in South America, Mesoamerica, the Caribbean, the United States and Australia). Seven species are experiencing heavy exploitation and experiencing decline even in suitable habitat. The most important threats to amphibians therefore show significant variation geographically.

Figure 6.4
Changes in threat processes over time for birds (source: BirdLife International 2004b).

Numbers on the bars are percentages. “Rapidly declining” amphibian species are those that now qualify for listing in a more threatened IUCN Red List Category than they did in 1980. NT=Near Threatened; VU=Vulnerable; EN=Endangered; CR=Critically Endangered; CR(PE)=Critically Endangered (Possibly Extinct); EW=Extinct in the Wild; EX=Extinct.

Figure 6.5
The number of “rapidly declining” amphibian species in the IUCN Red List Categories, broken into the major types of threat they are facing, with the threat level increasing from left to right.

6.10.2 Temporal Variation in Threats

Human activities and their effects on the environment have changed over hundreds of years. This results in a temporal variation in threats. For example, at a global level overexploitation and invasive alien species were the predominant causes of extinction in historical times in birds. Over time, extinctions caused by over-exploitation have declined, and habitat loss and invasives have become the dominant causes (Figure 6.4). For amphibians, the data have been analysed in a different way by examining how the major threats that have caused 435 species to deteriorate in Red List status since 1980 (see 6.10.1 above) vary between the IUCN Red List Categories (see Figure 6.5). The percentage of species experiencing poorly understood population declines, even in suitable habitat, increases with increasing extinction risk, indicating that the factors that cause these declines (probably disease interacting with climate change) are driving species towards extinction very rapidly, compared to habitat loss and over-exploitation.

6.10.3 Intrinsic Vulnerability

Studies on a range of taxa have identified correlations between susceptibility to extinction and intrinsic biological traits (see reviews by Purvis et al. 2000b and Fisher and Owens 2004; Box 6.4). Vulnerability to local extinctions is associated with low abundance and high habitat specificity. Among larger bodied groups, such as birds and mammals, small geographic range size is also important and, when tested alongside island living, has been found to explain most of the apparent high risk faced by island endemics (Manne et al. 1999; Purvis et al. 2000b). In other taxa, especially fish and invertebrates, small ranges appear less important, perhaps because their local densities are much higher, or because the threats they face are less related to small range areas. Among the vertebrates, large body size and slow reproductive rates are closely related to one another, and a number of studies have shown one or both to significantly increase extinction risk (Gaston and Blackburn 1995; Bennett and Owens 1997). This is as predicted; slow reproductive turnover will limit the recovery of species from declines caused by any threatening process, and species with larger body sizes are favoured for exploitation by humans. In the cases where both body size and life history have been studied, life history has been shown to be more important in carnivores (Purvis et al. 2000a; Cardillo et al. 2004) and, interestingly in the extinctions of large mammals in the Late Quaternary (Cardillo and Lister 2002; Johnson 2002). In marine fishes, large body size and slow population growth rates contribute to species declines (Dulvy et al. 2003), and the most significant impact of recent fisheries activities has been to deplete the upper trophic levels of fish – the top carnivores (Pauly et al. 1998). Top predators also appear to be especially threatened in mammals (Purvis et al. 2000a; Cardillo et al. 2004).

Many of these studies take quite a broad approach to examining correlations, and unsurprisingly, more detailed examinations reveal more complex patterns. For example, habitat loss might be expected to most affect those species that are ecologically specialized, whereas processes such as human persecution and introduced predators may have more of an impact on species with long generation times. This expectation is borne out for birds (Owens and Bennett 2000). In the mammalian carnivores, slow reproductive rates and low population density are more strongly correlated with high threat in species that inhabit areas of human population density (Cardillo et al. 2004).

6.10.4 Extinction Filters

The impact of threats on certain species can also be influenced by whether or not the threats are new (resulting in so-called extinction filters). There is much evidence for the existence of extinction filters, whereby prior exposure to a threat selectively removes those populations most vulnerable to it, leaving behind a community which is more resilient to similar threats in future, even if depauperate (Balmford 1996). This important concept explains much of the variation in past extinction rates and can be used to inform future predictions. For example, the impact of introduced rats on island-nesting seabirds appears less marked on islands with native rats or land crabs, as these seabirds have evolved in the presence of predators. In a similar fashion corals may be less likely to bleach in response to rising sea temperatures in areas where they have been repeatedly exposed to temperature stresses in the past (Brown et al. 2000; Podestá and Glynn 2001; West and Salm 2003).

6.10.5 Extinction Lags

The time period from the introduction of a threat to the extinction of a species can be highly variable, resulting in socalled extinction lags. The nature of the threat is obviously one important factor: some processes that increase mortality (disease, pollution) may lead to almost immediate consequences on the population, whereas the effects of overexploitation can be delayed by long generation times of the target species, and by a focus on older age classes. It is with habitat loss that the lag times will often be the longest.

Box 6.4 What is Most Important in Determining Extinction Risk?

The degree to which extinctions are due to external threats versus intrinsic characteristics has recently been investigated for some higher taxa. Among mammals about 50% of the variation in extinction risk is explained by variation in species' biological traits (Purvis et al. 2000b and c), with the remainder being attributable to human pressures and the interactions between human pressures and biological traits. Evidence that threat level is most highly correlated with human population density (Harcourt and Parks 2003) may not imply causality since human density and species richness correlate positively at continental scales (Balmford et al. 1996). However, in one study of mammalian carnivores where both human pressures and biological traits are taken into consideration it transpires that variation in human pressure does not on its own account for much variation in extinction risk. Extinction risk in the mammal order Carnivora is predicted more strongly by biology than exposure to human populations. However, biology interacts strongly with human population density to determine risk; biological traits explain 80% of variation in risk for species with high levels of exposure to human populations, compared to 45.1% for carnivores generally (Cardillo et al. 2004).

Photo 6.23
Nectophrynoides viviparus (Vulnerable) occurs in the Uluguru and Udzungwa Mountains and in the Southern Highlands of eastern and southern Tanzania. It is threatened by ongoing forest loss. It is one of very few species of frogs that gives birth to live young.
Photo: © David Moyer – Wildlife Conservation Society.

Recent evidence indicates that for vertebrates facing habitat loss and fragmentation, it may be decades to hundreds of years before species finally become extinct. Theoretically, the time from habitat loss to local extinction will be determined by the degree of fragmentation, the time since the threat took place, the spatial configuration of the fragments, as well as the biology of the species involved (Hanski and Ovaskainen 2002). In practice, estimates of the time from fragmentation to species extinction have been estimated for tropical forest bird species. Data on birds in Kenyan tropical forest fragments suggests that species loss approximates an exponential decay with a half-life of approximately 50 years for fragments of roughly 1,000 hectares. (Brooks et al. 1999). In Amazonian forest fragments less than 100 hectares in area, one half of the bird species were lost in less than 15 years, whereas fragments over 100 hectares lost species over timescales of a few decades to perhaps a century (Ferraz et al. 2003).

These time lags are important. On the one hand they mean that our estimates of current extinction may be serious underestimates of the ultimate legacy of habitat loss. For example, for African primate populations Cowlishaw (1999) estimated that over 30% of all those species that will ultimately be lost as a result of historical deforestation have still to go extinct locally. On the other hand, the lag times offer time for reversal of the trend so long as the period to habitat recovery is not longer than the time to extinction.

Key Findings

Photo 6.24
The Nubian Ibex Capra nubiana (Endangered) occurs in rocky desert areas in northeast Africa and parts of western Asia. The species faces numerous threats including direct competition with livestock for food and water, hunting, and habitat degradation.
Photo: © Jean-Christophe Vié.

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