15 Bird conservation in tropical ecosystems: challenges and opportunities

Joseph A. Tobias1, Çağan H. Şekercioğlu2 and F. Hernan Vargas3

1Edward Grey Institute, Department of Zoology, University of Oxford, Oxford, UK 2Department of Biology, University of Utah, Salt Lake City, UT, USA 3Peregrine Fund, Boise, ID, USA “What would the world be, once bereft of wet and of wildness?” Gerard Manley Hopkins

Introduction and the extent to which it can be applied to tropical birds remains unclear. Here, we summarize the key attributes of Bird conservation is a global mission but most tropical ecosystems and implications for bird of the key battles are being played out in conservation. First, we outline threats to key the tropics. Tropical ecosystems are generally tropical environments. Then we argue that under greater pressure than their temperate tropical species often differ from their counterparts from human population growth, temperate-zone counterparts in ways that pose agricultural expansion and a host of related novel challenges for conservation. We conclude factors. They also support 87% of bird species, that sustainable conservation of tropical birds many of them highly susceptible to habitat loss and the ecosystem services they provide will be or climate change (Şekercioğlu et al. 2012). The achieved only if attention is focused not merely concern that many tropical species are therefore on current snapshots of species distributions destined for extinction has focused much effort and protected areas but on biotic processes and towards setting global conservation priorities interactions operating at larger spatial and tem- based on a minimum number of protected poral scales. To support these ideas, we consider areas, often one per species (e.g. Rodrigues (i) why and how tropical ecosystems work in et al. 2004; Ricketts et al. 2005). However, this different ways from temperate systems, (ii) the approach is founded on traditional conserva- shortcomings of standard conservation strate- tion strategies developed in the temperate zone, gies when applied to the tropics, and (iii) the

Key Topics in Conservation Biology 2, First Edition. Edited by David W. Macdonald and Katherine J. Willis. © 2013 John Wiley & Sons, Ltd. Published 2013 by John Wiley & Sons, Ltd. BIRD CONSERVATION IN TROPICAL ECOSYSTEMS 259

outstanding priorities for policy, practice and stimulate industrial drivers of tropical deforest- future research. The strategies we propose have ation, such as cattle ranches, soy farms, paper broad relevance for the management of tropical mills, oil palm plantations, and major highways diversity because birds have long been viewed and infrastructure projects, all of which have as a model system for assessing conservation expanded markedly during recent decades priorities, and act as flagships for numerous (Smith et al. 1993; Vargas et al. 2006). Biofuel conservation programmes (Tobias et al. 2005). production from food crops is expected to increase by 170% in the next 10 years (Fargione et al. 2010). Crucially, the spiralling demand for Threats to tropical environments crops and commodities is likely to drive further degradation of large areas of remaining tropical forests, regardless of whether human popula- Lowland tropical forests tions decline in rural areas (Vargas et al. 2006; DeFries et al. 2010). All projections carry with Tropical forests support vast numbers of species. them a degree of uncertainty, yet the precau- They also limit soil erosion, reduce floods, tionary principle dictates that we should prepare contribute to hydrological cycles, help to for a future in which lowland tropical forests stabilize the climate, and generally play a major are highly fragmented. role in human well-being. Nonetheless, people are currently removing tropical forests at a stupendous rate: an average of 1.2% of rainfor- Tropical mountains est area, equivalent to ~15 million hectares, is destroyed annually (Laurance 2008) (see Tropical mountains offer hope for conserva- Chapter 13). One view holds that this process tion because montane habitats often remain is self-reinforcing, and therefore likely to relatively intact, at least at higher elevations. accelerate, because deforestation opens previ- They play an essential role as refuges for ously remote regions to agriculture and devel- lowland biodiversity that may otherwise disap- opment, and increases the impact of fires and pear in response to climate warming or habitat hunting. An alternative view holds that such loss at lower elevations. They are also important forecasts are unduly pessimistic because human hubs of bird diversification and endemism populations will become increasingly urbanized, because of their isolation. However, adaptation and primary forest loss will be offset by regrowth to these higher elevation refuges is risky: of secondary forests in depopulated areas tropical montane endemics have limited (Wright & Muller-Landau 2006). Either way, capacity to shift their ranges across unsuitable the pressure on old-growth tropical forests is lowland habitats and are therefore particularly intense, and set to get much worse in future vulnerable to climate change (Şekercioğlu (Laurance 2006). et al. 2008). Moreover, this risk is faced by pre- Over the next 50 years, the human population cisely those species that are least affected by is expected to reach 9 billion, with an ever habitat loss in highly threatened lowlands greater proportion climbing the socio-economic (Pimm 2008). ladder (Laurance & Peres 2006). Demand for food is predicted to rise by 70–100% (Godfray et al. 2010), and global industrial activity may Tropical islands expand 3–6-fold over the same period (Soh et al. 2006). The scale of projected increases in Tropical regions contain 45,000 islands over a overall and per capita consumption of food, minimum size of 5 ha (Arnberger & Arnberger timber and countless other products will further 2001). Each island supports relatively few species 260 J.A. TOBIAS, Ç.H. ŞEKERCIOĞLU AND F.H. VARGAS but many of these are important in terms of rarity predicted that 13% of bird species may be and uniqueness (see Chapter 12). Birds endemic extinct or consigned to extinction within 100 to islands often have relatively small geographi- years, most of them due to tropical deforesta- cal ranges, having diverged from continental tion and hunting. Given the scale of potential ancestors through isolation. This isolation has impact, the time is ripe for a more detailed often resulted in the evolution of flightlessness, assessment of the ecological processes underly- fearlessness and loss of immunity, rendering ing decline and extinction in tropical birds. island birds poorly adapted to novel anthropo- genic pressures, including habitat change and the introduction of alien predators and pathogens Demography and life-history (Milberg & Tyrberg 1993). Because of these issues, the arrival of humans on islands in the Tropical birds differ from their temperate-zone tropical Pacific led to the disappearance of at least counterparts in numerous ways but three 2000 insular bird species (Steadman 1995). It is factors have a disproportionate impact on the no surprise, therefore, that 88% of bird extinc- survival of populations. First, a far larger pro- tions since 1600 occurred on islands, mainly in portion of tropical species are highly sedentary, the tropics (Butchart et al. 2006). presumably as a result of climatic (and thus Today, island birds are coming under increas- resource) stability. For example, year-round ing pressure from human exploitation and territories are defended by only nine (4.5%) of invasive species (see Chapter XX [Cross-ref 193 North American forest bird species, whereas invasives chapter]). For example, it is thought the same figure rises to 379 (51%) of 739 that various species of rat (Rattus) have been Amazonian bird species (Salisbury et al. 2012). introduced, accidentally or otherwise, to 90% Second, tropical species have lower reproductive of the world’s islands (Jones et al. 2008; Oppel output. They tend to lay only two-egg clutches, et al. 2010). Other threats vary case by case. whereas temperate birds lay 4–13 eggs per The popularity of some tropical islands as places clutch (Jetz et al. 2008). Third, their ranges to live or visit makes them susceptible to rapid are often patchy and population densities low coastal development, overfishing or disease. On (Donlan et al. 2007). At one locality in St Lucia, for example, roughly 40% of habitat Amazonian Peru, for example, 106 (35%) of occupied by the white-breasted thrasher 329 resident species occurred at densities of <1 (Ramphocinclus brachyurus), an endangered spe- pair/100 ha, with a median abundance (i.e. cies with a global population of roughly 1200 average population density) across all species of individuals, is slated for potential tourist devel- 2.5 pairs/100 ha (Terborgh et al. 1990). This opment (Young et al. 2010). Likewise, Bataille contrasts with the last remaining primeval et al. (2009) provide evidence that tourism European forests, where the median abundance drives the ongoing introduction of avian malaria of >50 forest bird species is much higher, at vectors (e.g. Culex quinquefasciatus) from main- 10–30 pairs/100 ha (Wesołowski et al. 2006). land Ecuador to the Galapagos Islands, trans- Indeed, median abundance of European forest ported by cruise boats and aeroplanes. birds often exceeds the maximum estimated population density in Amazonia (Cercomacra cin- erascens at 20 pairs/100 ha), providing a striking New insights into threats facing illustration of the relative rarity of tropical birds. tropical avifaunas This combination of low dispersal, low reproductive output and low population density suggests that tropical birds are more sensitive to The litany of threats outlined above is broadly habitat fragmentation or disturbance, and less familiar but its ultimate impact on birds remains able to recover after population bottlenecks debatable. BirdLife International (2000) (Stratford & Robinson 2005; Soh et al. 2006). BIRD CONSERVATION IN TROPICAL ECOSYSTEMS 261

Most importantly, it implies that a far greater to tropical sedentary bird species, they have area of intact habitat is required to protect generally been neglected in comparison to viable populations. Judging only by the popula- northern hemisphere migratory species that tion densities reported above, an area 4–12 have laws and conventions dedicated to them times higher on average per species may be (e.g. Neotropical Migratory Bird Conservation required. However, the added constraints of Act in the USA). For example, between 1990 low dispersal and low reproductive output, as and 2007, international agencies provided the well as significant numbers of extreme low- island of Hispaniola (i.e. the Dominican density species, suggest that diverse tropical Republic and Haiti) with more than $1.3 mil- bird communities can only be conserved in lion for migratory bird research, compared with much larger areas. only $300,000 for the study of resident birds, including several rare endemics (Latta & Faaborg 2009). Dispersal and migration Although year-round territorial systems make up the largest component of tropical avi- The term ‘sedentary’ fails to convey the extreme faunas, a different set of risks is faced by many dispersal limitation of insectivorous birds in frugivores and nectarivores. Telemetry studies tropical forests, many of which are unable or show that these birds are typically mobile unwilling to cross relatively minor gaps such as because they track patchy food resources. roads (Stratford & Robinson 2005; Laurance Unlike temperate-zone birds, however, they are et al. 2009). In experimental tests, 50% of often unable to cross degraded landscapes. rainforest understorey species struggled to cross Classic examples include elevational migration 100 m gaps (Moore et al. 2008), and compara- in white-ruffed manakins (Corapipo altera) tive studies suggest that thousands of tropical (Boyle 2008) and unpredictably complex bird species face this problem (Stratford & annual movements over hundreds of kilome- Robinson 2005; Salisbury et al. 2012). This tres in the three-wattled bellbird (Procnias tri- contrasts sharply with the situation in temperate- carunculata) (Powell & Bjork 2004). In effect, zone habitats where gap aversion is rare. these movements compound the challenges of Amongst European woodland birds, for example, designing effective protected area networks even the wren (Troglodytes troglodytes) is able to because isolated reserves will fail to provide cross broad (>100 m) gaps in habitat, as long as sufficient coverage for many species. low vegetation is present. Unsurprisingly, limited mobility is an overlooked determinant of extinction risk in birds. Two- Physiological constraints thirds of the planet’s bird species are sedentary, and preferences and 74% of sedentary species live exclusively in the tropics. Of sedentary species, 26% are glob- Most tropical birds experience lower climatic vari- ally threatened or near threatened with extinc- ability than do their temperate-zone counterparts, tion, compared to 10% of migratory species both within and between years (Ghalambor (Şekercioğlu 2007). Projections of land bird et al. 2006). They are therefore thought to have extinctions expected from the combined effects lower thermal plasticity (Stratford & Robinson of climate change and habitat loss also indicate 2005). The evidence from a geographical study of that sedentary bird species are approximately rufous-collared sparrows (Zonotrichia capensis) sup- five times more likely to go extinct by 2100 ports the hypothesis that populations in stable than migratory birds (Şekercioğlu et al. 2008). environments are less able to adapt to novel envi- This partly reflects the disadvantages of a ronmental conditions (Cavieres & Sabat 2008). sedentary lifestyle when it comes to tracking Moreover, there are good reasons to expect tropi- moving climate optima. Despite the greater risks cal birds to be relatively intolerant of temperature 262 J.A. TOBIAS, Ç.H. ŞEKERCIOĞLU AND F.H. VARGAS fluctuation: in particular, they have lower basal the disappearance of frugivores can have serious metabolic rates (BMR; Wiersma et al. 2007; consequences for forest regeneration, even McNab 2009), whereas species with higher BMRs when the drivers of habitat loss and degradation are more adaptable to climate change (Bernardo are controlled. et al. 2007). In general, therefore, tropical birds are likely to be constrained by narrower environmen- tal niches, reduced tolerance of thermal stress and The impact of bird declines on habitat change (Janzen 1967; Stratford & Robinson ecosystem function and services 2005; Şekercioğlu et al. 2012).

Ecosystem services are ‘the set of ecosystem Biotic interactions functions that are useful to humans’ (Kremen 2005). In general, increased biodiversity in a In terms of genetic diversity, 80% of the tree of particular environment is thought to increase life could be retained even when approxi- ecosystem efficiency and productivity, and mately 95% of species are lost (Nee & May decrease susceptibility to perturbation. Birds 1997); the only problem is that the resulting play a role as ‘mobile link’ animals connecting ecosystems would not work! Healthy ecosys- habitats and ecosystems through their move- tems depend on associations between hosts ments (Lundberg & Moberg 2003), and provid- and parasites, predators and prey, seeds and ing services such as pollination, seed dispersal, seed dispersers, and so on. These networks are nutrient deposition, pest control and scaveng- the lifeblood of biodiversity. They are particu- ing (Şekercioğlu 2006; Wenny et al. 2011). larly important in tropical ecosystems because Thus, the ongoing decline in bird species is co-evolutionary associations tend to increase in likely to have far-reaching ecological conse- abundance towards the equator (Schemske quences, from the spread of disease and loss of et al. 2009). In effect, the complex architecture agricultural pest control to the extinction of of food webs and other biotic interactions in plants dependent on avian pollinators and seed tropical ecosystems increases the likelihood of dispersers (Şekercioğlu et al. 2004). cascading co-extinctions, and cautions against In the tropics, large frugivorous birds are a simplistic view of phylogenetic diversity (PD) particularly threatened by hunting and habitat as a means to prioritize conservation action fragmentation, which can have significant (see Chapter 1). consequences for shade-tolerant, late succes- Tropical birds offer good examples of finely sional tree species with large seeds (e.g. tuned interactions, as they have more special- Lauraceae, Burseraceae, Sapotaceae). For ized dietary niches than their temperate-zone example, in the East Usambara mountains of counterparts (Belmaker et al. 2012). The most Tanzania, the endemic tree Leptonychia usamba- clear-cut cases are nectarivores. For example, rensis (Sterculiaceae) is dependent on avian some species of hummingbird with highly spe- seed dispersers such as greenbuls (Andropadus cialized bills (e.g. sword-billed hummingbird, spp.), most of which are rare or absent in small white-tipped sicklebill, etc.) can only forage on, forest fragments (Cordeiro & Howe 2003). This and pollinate, very few species of flowering results in lower seed removal, shorter dispersal plants. Thus, the survival of specialist nectariv- distance, greater seedling aggregation under ores and their associated foodplants is tightly the parent trees, and reduced recruitment in interwoven via co-evolutionary adaptations. fragments than in continuous forest (Cordeiro Similarly, frugivorous birds dictate the fate of & Howe 2003). Similarly, previous studies have forests. Many tropical trees produce large, shown that overhunting of large frugivores lipid-rich fruits adapted for animal dispersal, so (e.g. guans, toucans, hornbills) has a detrimental BIRD CONSERVATION IN TROPICAL ECOSYSTEMS 263 impact on recruitment of bird-dispersed trees What are the implications for in humid forests of Amazonia (Terborgh et al. biodiversity conservation? 2008) and India (Sethi & Howe 2009). In effect, widespread losses of avian frugivores may result in the domination of short-lived pioneer Armed with this information about tropical trees, with long-term effects cascading through environments and their native species, we can plant communities (Şekercioğlu et al. 2004; explore the implications for conservation Terborgh et al. 2008). They also mean that the strategies. The following sections deal with potential for long-distance dispersal is declining major threats to biodiversity at a global scale, for many plant species at precisely the time highlighting the type and scale of impact they when flexible range shifts are becoming more may have on tropical ecosystems. important because of land use and climate change. Meanwhile, the susceptibility of insectivo- rous birds to habitat degradation and fragmen- Habitat fragmentation tation may cause a different set of problems. Insectivores often control invertebrate popula- Millions of hectares of tropical forests exist tions and play a significant role in limiting foli- in fragments and many thousands of new age damage in tropical forests (van Bael et al. fragments are created every year (Sodhi et al. 2010) and plantations (Greenberg et al. 2000; 2011). These exist in a variable matrix of Kellermann et al. 2008; van Bael et al. 2008; land uses, and consequently the loss of avian Mooney et al. 2010). This form of control of diversity is highly site dependent (Sodhi et al. insect herbivores can be economically impor- 2011). Nevertheless, some patterns have tant in agricultural regions. For example, bird- emerged. Understorey insectivores, for instance, mediated predation of the coffee berry borer tend to be particularly sensitive to fragmentation (Hypothenemus hampei) in Jamaican coffee plan- (Peh et al. 2005; Barlow et al. 2006; Yong et al. tations saves farmers $310/ha per year (Johnson 2011). This may be because other dietary guilds, et al. 2010). including frugivores, granivores and nectariv- Finally, tropical scavengers such as vultures ores, are often dispersive, non-territorial and provide one of the most important yet under- naturally adapted to exploit patchy resources, appreciated ecosystem services. Avian scaven- and therefore better equipped to cross gaps gers worldwide comprise the most threatened and travel through degraded landscapes. This avian functional group, with about 40% of the process is highlighted by studies in Amazonia species being threatened or near threatened showing that fragments are primarily inhabited with extinction (Şekercioğlu et al. 2004). by bird species with good dispersal abilities or Because of the loss of decomposition services high tolerance of the non-forest matrix (Lees & provided by vultures, increased disease trans- Peres 2008). A key latitudinal difference linked mission and consequent health spending are to dispersal ability involves the likelihood of likely. Markandya et al. (2008) suggested that recolonization after local extinction. This is the spiralling Indian dog population, which illustrated by the fact that temperate bird species increased by 7.25 million between 1992 and dropping out from forest fragment avifaunas 2003, could be caused by the 90–99% declines often recolonize within a few years if source in vultures. Partly based on the associated surge populations are found nearby, whereas tropical of ~48,000 additional rabies deaths, they esti- species rarely return to the community unless mated that the health costs attributable to vul- the habitat linking the fragment to the source ture declines were US$ 18 billion (Markandya population actually recovers (see Stratford & et al. 2008). Robinson 2005). 264 J.A. TOBIAS, Ç.H. ŞEKERCIOĞLU AND F.H. VARGAS

Another issue influencing the survival of bird contrast, the melting of polar ice caps attracts populations is elevated predation in forest much more media attention despite affecting fragments. For example, in the Eastern Arc a relatively small number of bird species, most mountains of Tanzania, seven common under- of which have large global ranges. storey bird species, e.g. forest batis (Batis mixta), Previous studies indicate that tropical organisms suffered 2–200 times lower rates of nest suc- are as likely as temperate organisms to track cess in fragments versus continuous forest moving climates (Pounds et al. 1999; Colwell (Newmark & Stanley 2011). Similar reductions et al. 2008). Although the full impact of this in reproductive success appear to be widespread process under global warming is difficult to in forest fragments, and at least partly linked to predict, it is likely to force many bird species higher densities of nest predators, including uphill in the montane tropics, reducing their rodents, raccoons, mongooses and snakes, as ranges, sometimes entirely (Shoo et al. 2005; well as greater visibility of nests to hawks and Şekercioğlu et al. 2008; Wormworth & Şekercioğlu other arboreal predators (Chalfoun et al. 2002). 2011; Şekercioğlu et al. 2012). For example, the Importantly, the density and diversity of nest potential habitat of the golden bowerbird predators are typically far higher in tropical (Prionodura newtonia), a montane forest species than temperate regions, again suggesting that endemic to Australia, would be reduced by fragmentation has a greater negative impact on 98% if temperatures rose by 3 °C (Hilbert et al. tropical birds (Stratford & Robinson 2005). 2004). Likewise, a 4 °C increase would result in almost complete removal of the Pantepui vegetation of Venezuela (Nogue et al. 2009), Climate change presumably with devastating effects on 30–40 endemic bird species, e.g. rose-collared piha Most studies of the impacts of climate change (Lipaugus streptophorus). on biodiversity have focused on boreal or This so-called ‘escalator to extinction’ may be temperate regions, perhaps because it is often exacerbated by competitive interactions, a assumed that the threat of warming increases problem particularly relevant to tropical birds towards the poles. However, the tropics are a because of strong interspecific territoriality far more likely setting for climate-mediated between elevational replacement species mass extinctions, for three main reasons. First, (Jankowski et al. 2010). Finally, warming could the direct impact of global warming will be expose montane birds to an array of new path- severe in tropical mountains, where high- ogens, predators and competitors that migrate elevation climates will shrink or disappear upslope (Bradshaw et al. 2009; Wright et al. (Ohlemüller et al. 2008). Second, species 2009). For these reasons, tropical high- elevation inhabiting extensive lowlands may find it dif- specialists could be among the most endangered ficult to cope with further warming or to species on earth if global temperatures rise migrate towards cooler refuges (Wright et al. (Williams et al. 2003; Ricketts et al. 2005; 2009). And third, the sheer diversity of tropi- Şekercioğlu et al. 2008). cal lineages means that these threats will Birds of tropical lowlands face a different affect large numbers of bird species. set of problems. Current projections suggest Specifically, if a warming climate threatens that, by 2100, 75% of modern lowland tropi- taxa restricted to tropical highlands (≥500 m cal forests will experience mean annual tem- asl), this would amount to approximately peratures warmer than the warmest forests 10% of the world’s ~10,000 bird species, known today, i.e. >28 °C (Wright et al. 2009). including the majority of those currently This represents an increase of 2–4 °C from considered to be safeguarded from land use present-day temperatures, well below the change (Pimm 2008; Harris et al. 2011). In upper realistic bound of 6.4 °C (IPCC 2007). BIRD CONSERVATION IN TROPICAL ECOSYSTEMS 265

Thus, lowland species may be ill suited to further warming because they are already Pathogens and disease close to their tolerance limits (Weathers 1997; Diversity, virulence and abundance of pathogens Colwell et al. 2008; Wright et al. 2009). In are all higher in the tropics. Moreover, since conjunction, latitudinal range shifts to cooler many pathogens are sensitive to temperature, environments are unlikely because there is rainfall and humidity, climate warming has the virtually no latitudinal temperature gradient potential to increase pathogen development and in the tropics (Colwell et al. 2008). In other survival rates, disease transmission and host words, the escape route to cooler climates is susceptibility (Harvell et al. 2002; Garamszegi closed to many lowland tropical species, 2011). This is coupled with the problem of range particularly those living far from the nearest shifts through introductions, invasions and topographical relief, e.g. central Amazonia climate-related expansions and contractions of (Loarie et al. 2009; Wright et al. 2009). This distributions. Such processes can lead to parasites contrasts with the situation at higher lati- becoming pathogenic when established in novel tudes, where latitudinal climatic gradients are environments or in contact with susceptible a permanent feature. new hosts. The results for birds can be devastat- Tropical islands are likely to fare little better. ing. In Hawaii, for example, more than half of Many rare island endemics are restricted to the the native avifauna became extinct due to avian montane zone where the extent of suitable malaria and other introduced pathogens habitat could recede dramatically in response to (LaPointe et al. 2010). Upward shifts in mosquito warming (Fordham & Brook 2010). Moreover, distribution predicted from continued global climatic fluctuations can seriously threaten bird warming will further reduce the refuge habitat populations. For example, El Niño conditions, available, with serious implications for some of characterized by high sea temperature and the surviving Hawaiian endemics: a predicted rainfall in the Equatorial Pacific, are associated 2 °C rise will probably eliminate all remaining with disrupted oceanic food webs. Specifically, disease-free forested refugia in Hawaii in the they tend to switch off the Cromwell current, next century (Benning et al. 2002). Montane thereby reducing fish stocks and causing popu- avifaunas throughout the tropics could be simi- lation crashes in Galapagos penguins (Spheniscus larly threatened by changes in the distribution mendiculus), an endangered species with a of hosts and vectors caused by land use and population of around 1500 individuals (Vargas climate change (Harvell et al. 2002). et al. 2006, 2007). They also promote vector- borne diseases (Gilbert & Brindle 2009; Kolivras 2010). El Niños are natural cyclical phenomena but the frequency of severe events has increased Invasive species sevenfold over the last century; moreover, global warming is predicted to drive further Invasive plants, predators and pathogens are increases in their frequency and intensity present on islands worldwide but they are (Timmermann et al. 1999). Although these more likely to cause catastrophic declines in changes may have severe consequences for the tropics. This is partly because tropical island birds and ecosystems, they are overshad- islands support many endemic species with owed by the threat of warming to atolls and tiny ranges and populations, and also because other low-lying oceanic islands. Here, extreme they provide suitable environments for inva- climatic perturbations and sea-level rises may sive species to thrive. Introductions can have have a catastrophic impact on human welfare major negative impacts on tropical birds, par- and livelihoods, as well as wildlife (Barnett & ticularly on island endemics that have evolved Adger 2003). without predation pressure. For example, the 266 J.A. TOBIAS, Ç.H. ŞEKERCIOĞLU AND F.H. VARGAS predatory brown tree snake (Boiga irregularis) landscapes (Gillies et al. 2011). Thus, those was introduced to the island of Guam shortly species forced to disperse polewards or uphill by after World War II, causing the extirpation or climate change may now find that human serious decline of 17 of the island’s 18 native settlements and agricultural areas stand in the bird species (Wiles et al. 2003). Most island way (Şekercioğlu et al. 2008). Unfortunately, extinctions have been caused by similar events, this outcome is likely to be extremely common with feral cats and rats being the most damag- because mid-elevations are among the most ing culprits (see Chapter XX [XREF INVASIVES densely populated and heavily cultivated lands CHAPTER]). Invasive plants and pathogens can in the tropics. People preferentially settle this also have strongly deleterious impacts. The red elevational band because of its pleasant climate quinine tree (Cinchona pubescens), for example, and suitability for a range of important cash is causing drastic changes to the native plant crops, including coffee, tea and coca. It therefore community of the Galápagos Islands, and is seems likely that human activity is reducing destroying the breeding habitat of the Galápagos the ability of many species to track climates, rail Laterallus spilonotus (Shriver et al. 2010). with potentially disastrous effects on long-term The main line of defence against invasive spe- survival prospects. cies is eradication schemes, which are often Even discounting the problem of dispersal costly but sometimes highly effective (e.g. constraints, climate change may significantly Donlan et al. 2007). exacerbate a number of threats to tropical birds (Şekercioğlu et al. 2012). Contemporary com- munities of birds, plants, pathogens and other The central role of synergisms interacting species will be disassembled by individualistic range shifts, such that novel com- At a local scale, the fate of tropical biodiversity is munities of species will mix in the future typically shaped by a suite of factors: biotic, (Laurance & Peres 2006; Thuiller 2007). There abiotic and socio-economic (Seddon et al. 2000). will be winners and losers in these new interac- It is often the inevitable interactions and syner- tions, and the outcome across entire networks gisms between these factors that pose the greatest of species may produce unanticipated effects threat of all (Dobson et al. 2006; Brook et al. on ecosystems (Parmesan 2006). Overall, the 2008; Tylianakis et al. 2008). For example, as dramatic pace of contemporary habitat loss, habitat declines, hunting pressure often increases, combined with the synergistic effects of a twin threat responsible for an elevated future climatic change, overhunting, emerging extinction risk in tropical vertebrates (Laurance pathogens and many forms of habitat degrada- & Useche 2009). Likewise, the fragmentation of tion, could sharply increase the rate of species tropical forest increases the risk of fires, further extinctions (Tylianakis et al. 2008). reducing avian diversity (Barlow et al. 2006). The importance of synergisms in tropical ecosystems is highlighted by the issue of climate Governance, legislation change. While many species coped perfectly and economics well with wide temperature fluctuations and other stressors during their evolutionary history Many tropical nations are too poorly equipped, (Balmford 1996), none did so in a heavily financially and institutionally, to cope with the human-modified environment with numerous current rate of environmental change (Butchart additional barriers to dispersal. This is important et al. 2006). This problem is further exacer- because the inherent low dispersal ability of bated by widespread corruption (Barrett et al. many tropical bird species means that they are 2001; Lee & Jetz 2008). The triumvirate of often unable to disperse across agricultural poverty, weak institutions and corrupt officials BIRD CONSERVATION IN TROPICAL ECOSYSTEMS 267 leads to the destruction or mismanagement of climate datasets originate from the tropics, in protected areas, and the uncontrolled contrast to many thousands from Europe or exploitation of natural resources at the whim North America (Rosenzweig et al. 2008). of global markets (Smith et al. 2003). Rising prices for commodities, such as gold, can unleash a surge of tropical deforestation by Towards long-term and broad-scale making exploitation profitable in regions for- strategies for the conservation of merly too remote to be affected (Swenson et al. tropical ecosystems 2011). Biofuel crops, such as sugar cane, oil palm or soy, grow best at low latitudes, and thus escalating demands are creating an incen- Most conservation efforts and priority-setting tive for converting tropical habitats to farmland exercises focused on tropical systems have (Laurance 2006; Laurance & Peres 2006; Brook attempted to apply strategies developed in the et al. 2008). These mechanisms can now oper- temperate zone. Many rely on species as units ate rapidly and with dramatic consequences, of conservation; others emphasize metrics not least because infrastructural projects have such as phylogenetic diversity (PD), such that opened up trade routes, making the exploita- conservation may target the maximum amount tion of once remote regions economically via- of ‘evolutionary history’. However, the preced- ble. For example, the Trans-Oceanica Highway ing sections outline several reasons why these links the Brazilian soya belt of Acre and Mato approaches may fail in the tropics. Up to this Grosso with Peruvian ports, such that the point we have dwelt on the underlying problems; expanding markets of China and other the following sections focus on conservation Asian countries have direct influence on the priorities and solutions. deforestation frontiers of southern and western Amazonia (Tobias et al. 2008b). Protected areas and beyond

Knowledge Between 1994 and 2004, the extinction of 16 bird species was prevented through a combina- A final piece in the jigsaw is knowledge, or lack tion of habitat protection, control of invasive thereof. The quality of information about tropi- species and captive breeding (Butchart et al. cal birds lags far behind that available for the 2006). For example, wild populations of temperate zone in terms of taxonomy (Tobias Seychelles magpie-robin (Copsychus sechellarum) et al. 2008a), population size (Tobias & Seddon increased from approximately 15 to 136 2002; Seddon & Tobias 2007) and conservation individuals, and Mauritius kestrel (Falco puncta- status (Tobias & Brightsmith 2007). Taxonomic tus) from four to 500–800 individuals. These revisions tend to reveal that many tropical bird targeted schemes, often costing millions of species consist of more than one cryptic species, dollars per species, are clearly effective in some each with global ranges and populations smaller cases. However, they only involve <10% of than previous estimates (Lohman et al. 2010). critically endangered bird species, suggesting The scale of taxonomic uncertainty in the trop- that conservation efforts and funding need to ics suggests that conservation issues need to be be greatly expanded. re-evaluated, as many analyses are sensitive to Aside from financial constraints, it is doubtful estimates of global range (e.g. Rodrigues et al. whether this fire-fighting approach is viable 2004; Vale et al. 2008). Moreover, latitudinal from the perspective of ecosystem function. bias in knowledge is not restricted to taxonomy: Small or fragmented populations will cease for example, only a tiny number of long-term to play a significant ecological role, and thus 268 J.A. TOBIAS, Ç.H. ŞEKERCIOĞLU AND F.H. VARGAS conservation strategies assuming that species Conservation priorities: too much will survive in a few isolated reserves are pattern, not enough process unlikely to result in healthy tropical ecosys- tems. Only by maintaining large, intercon- The idea that conservationists need to focus on nected populations can we avoid numerous the processes sustaining biodiversity is not new species being officially extant but functionally (Smith et al. 1993; Moritz 2002), but it has extinct (Sodhi et al. 2011). Thus, conservation proved difficult to incorporate into conservation needs to focus not only on protected areas but strategies. The approach requires us to see the broader landscape context in which reserves beyond the current pattern of extant species, are embedded. This is especially important in and to consider longer-term evolutionary the humid tropics, where the fate of avian perspectives. But what perspectives are these? diversity within protected areas is often inextri- There is a tendency to assume that by using cably linked to the surrounding agricultural molecular phylogenies to map conservation matrix (Harvey et al. 2008). priorities, we have somehow captured the Lowland and mid-elevation forests of tropical evolutionary process but a phylogeny is as Asia (Peh et al. 2005), Africa (Norris et al. 2010) much a pattern as anything else (Losos 2011). and Meso-America (Harvey et al. 2008) are Instead, the defining attributes of process-based tightly coupled agro-forestry systems, with conservation are (i) the preservation of genetic, most habitats supporting rural livelihoods. phenotypic and functional diversity below the Amazonia is inexorably going this way. A prior- species level; (ii) the maintenance of abundance ity for birds is to promote landscape configura- so that lineages continue to perform their tions that connect reserves, maintain a diverse ecological functions across their natural ranges; array of habitats and retain high structural and and (iii) the promotion of conditions necessary floristic complexity (Koh 2008; Chazdon et al. for long-term population connectivity and 2009). In particular, the preservation of forest dispersal, even under climate and land use remnants, including riparian strips, secondary change scenarios. forests and individual trees, helps birds to move The contrasts between pattern-based and between forest patches and even breed process-based conservation are striking. in human-dominated landscapes (Şekercioğlu A pattern-based approach tends to prioritize et al. 2007; Martensen et al. 2008; Dent & rare endemics, many of which are only nar- Wright 2009). rowly divergent from their closest relatives, by Promoting these features is a huge challenge, preserving small populations in isolated particularly in areas suited to mechanized agri- reserves. A process-based approach does not culture. Where possible, engagement is required target these potentially ephemeral ‘twigs’ of the to ensure that farmers are stakeholders in tree of life, and attempts instead to sustain the creating landscapes that preserve birds as well as underlying mechanisms that provide the impe- rural livelihoods (Harvey et al. 2008). One tus for adaptation and speciation. This can be successful blueprint involves Payment for achieved in different ways. One method is to Ecosystem Service schemes, such as those oper- focus attention on all genetically and pheno- ating in Costa Rica, which motivate landowners typically distinct lineages within species (Moritz to maintain forest patches and watershed 2002); another is simply to maintain the con- reserves (Sodhi et al. 2011)(see Chapter 4). These text for selection, rather than protecting pheno- measures need to be expanded where possible, types per se (Thomassen et al. 2011). A key and coupled with outreach and education initia- practical component is the maintenance of tives, to ensure that we preserve key ecosystem habitat heterogeneity and connectivity within processes as well as populations of rare species. and between reserves, particularly where this BIRD CONSERVATION IN TROPICAL ECOSYSTEMS 269 captures genetic variation across environmen- example, intensive agricultural development tal gradients (Moritz 2002). should be focused on grasslands or precleared Aldo Leopold famously observed that ‘to land, rather than forests, as this limits losses keep every cog and wheel is the first precaution in terms of both carbon balance and bird of intelligent tinkering’, meaning that all parts diversity (Danielsen et al. 2009). Island restoration. The eradication of invasive of ecosystems should be saved, even though t mammals, plants and pathogens is key to their function may be unclear. Conservationists preserving avifaunas of tropical islands. worldwide have tended to interpret ‘parts’ as t Connectivity between bird populations. This ‘species’. However, this misses the point that in can be achieved by integrating degraded, all ecosystems the essential cogs and wheels are secondary and fragmented habitats into adaptation, connection and interaction – in conservation schemes. Techniques include other words, not patterns but processes. minimizing forest fragmentation and frag- Incorporating this viewpoint into the bigger ment degradation, preventing fires, cattle picture of conservation thinking is particularly incursions and other types of disturbance, vital in the tropics. reducing the contrast between fragments and the surrounding non-forest matrix, and increasing fragment connectivity via ecologi- cal corridors, riparian strips and landscape Key measures to preserve healthy restoration. Where feasible, efforts should tropical avifaunas focus on developing and implementing community schemes and government legis- With the goal of managing tropical ecosystems lation to maintain these landscape features and preventing further declines in tropical at deforestation frontiers. birds, we propose a list of conservation and t Intact elevational and ecological gradients. research priorities. Although these are designed Even supposedly complete gradients, such as with birds in mind, similar strategies will greatly Manu National Park in Peru, are currently improve our chances of preserving a vast being truncated or interrupted by habitat degradation. One laudable government- proportion of tropical biodiversity in resilient, sponsored initiative attempts to connect functional and flexible ecosystems (Hole et al. protected areas from the western lowlands of 2009). Ecuador, over the Andes and down into eastern Amazonia, and there is an urgent need to replicate this approach elsewhere to Conservation targets safeguard elevational corridors. The logic of preserving elevational transects extends t Extensive protected areas, i.e. ‘megareserves’, to all habitat mosaics and ecotones, i.e. sustaining viable populations of birds in large gradations between core habitat types. In all areas of intact habitat (Laurance 2005; Peres cases, land-sparing efforts need to consider 2005). These areas are always richer in bird that environmental gradients may fluctuate diversity, and more important for bird con- spatially over time. servation, than land shared with agricultural t Strengthened incentives to promote the productivity (Edwards et al. 2010; Gibson sustainable economic use of bird-friendly et al. 2011; Phalan et al. 2011). habitats. This includes much greater t Improved yields of tropical crops. This is an emphasis on educating people in tropical important factor in allowing a maximum nations about the key functional roles played area of natural habitat to be spared for con- by ecosystems in flood protection, sustaina- servation purposes. ble food production and delivery of clean t Improved targeting of clearance and conver- water (Edwards et al. 2010; Şekercioğlu sion of forests for human land uses. For 2012). 270 J.A. TOBIAS, Ç.H. ŞEKERCIOĞLU AND F.H. VARGAS

questions require a focus on the biodiversity Research agenda value of plantations and other agricultural habitats, and management practices that t Promote research focused on tropical birds. maintain connectivity in natural populations Bird behaviour and ecology are fundamental (Harvey et al. 2008). to process-based conservation strategies, yet t Long-term population dynamics. The extent most work on this subject has targeted tem- to which degraded habitats serve as a ‘safety perate-zone taxa (Newmark & Stanley net’ for tropical bird populations needs 2011). detailed study. It is clear that these habitats t Dispersal. Research should clarify the ability of support a wide diversity of bird species and tropical birds to use human-modified land- are important for conservation (Edwards scapes, cross gaps and navigate corridors, as et al. 2011), yet studies that only consider these are critical aspects of avian life-history presence/absence, or even relative abundance, from the perspective of landscape manage- may provide an overly optimistic scenario if ment. The recent use of tracking technology surveys detect temporary transients or if to quantify dispersal ability and habitat use degraded habitats act as ‘ecological traps’ (Part (e.g. Gillies & St. Clair 2008; Hawes et al. 2008; et al. 2007). Thus, we need an improved Hadley & Betts 2009) should be expanded. understanding of underlying population t Understanding biotic interactions. These are dynamics in key habitats, with a focus on complex even in temperate-zone bird com- individual fitness, demography, extinction munities but in the tropics more research is lags, etc. required to understand the long-term impli- t Resolving the land-sharing versus land-sparing cations of interactions with food plants, prey debate. Retaining habitat patches in the land- and parasites. A range of modern tools, from scape reduces agricultural yield, so that agri- field experiments to phylogenies, should be cultural production needs to spread over larger used to explore the role of interactions in areas to meet demand (Edwards et al. 2010). maintaining stable tropical ecosystems. More research is required to identify optimum t Improving knowledge about range and abun- conservation strategies for balancing the trade- dance. Most tropical regions remain poorly off between larger protected areas and a more known in terms of the distribution and abun- connected landscape for birds. dance of bird species, and how these fluctu- t Climate change. Most studies have focused on ate over time. Progress requires field surveys the temperate zone, and we need to and monitoring exercises, ideally coupled know much more about the physiological with the development of automated moni- constraints, and climate-tracking potential of toring tools, e.g. song identification software. tropical birds (Stratford & Robinson 2005; t Improving knowledge about taxonomy. Wormworth & Şekercioğlu 2011). For example, Detailed phenotypic and molecular studies a global review of range shifts in response to are required to revise tropical species limits climate warming was unable to include a sin- and relationships in many avian families. gle study on tropical birds (Chen et al. 2011). t Conservation potential of agricultural landscapes, including logged and secondary forests. Most studies have looked at bird Conclusions diversity from the perspective of isolated nat- ural habitat, whereas the matrix of human land uses provides a useful framework for a When it comes to bird conservation, lessons different set of questions. What are the rela- tive impacts of different agricultural practices learnt in temperate systems cannot simply be on conservation outcomes and ecosystem transferred to the tropics. The current practice of services? 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