reviews reviews reviews gulliver travels to the...

here are some laws and customs in this empire verypeculiar, and if they were not so directly contrary

to those of my own dear country, I should be tempted tosay little in their justification” (Swift 1726). In JonathanSwift’s classic tale, Gulliver’s Travels, Gulliver finds him-self in unfamiliar and extraordinary lands. What makeshis experiences so intriguing and comical are his trans-planted notions of order and society colliding with thevery different notions held by his exotic hosts. In a simi-lar way, ecological inferences derived from one geo-graphic area may not transfer smoothly to others and, infact, may impede further understanding. Such may be thecase when comparing the ecology and evolution of tropi-cal and temperate avifaunas, particularly neotropical andnorthern temperate assemblages.

Differences in life histories and behaviors betweentemperate and tropical birds have been recognized for along time (Skutch 1949). Alexander Skutch, during afamous series of debates with David Lack about the lati-tudinal gradient in avian clutch sizes (Lack 1947; Skutch1949), remarked that if most biologists had been raisedin the tropics they would ask why temperate birds layunusually large clutches, rather than asking, as did tem-perate biologists, why tropical clutches are so small.Similarly, Ricklefs (2002) noted that his time in theneotropics was pivotal in cementing the idea that manyneotropical bird lineages are distinct from NorthAmerican ones in both their evolutionary and life histo-ries. The degree to which such differences influence theconservation of bird populations in human-dominatedlandscapes remains unappreciated.

Nevertheless, two present-day commonalities existbetween tropical and temperate birds. First, species inboth realms are confronted with destruction and conver-sion of forests (Faaborg et al. 1995; Laurance et al. 2000).Areas of high endemism, such as the Atlantic rainforestsof Brazil, the northern and central Andes, and Amazonia,are particularly at risk (Balmford and Long 1994).Secondly, many species respond negatively to such distur-bances and their populations decline or disappear in frag-mented landscapes. Local extinction of species from frag-mented forests is well documented across northerntemperate areas (Whitcomb et al. 1981) as well as in theneotropics (Stouffer and Bierregaard 1995; Robinson1999, 2001). Thus, temperate and tropical birds face sim-ilar challenges. Yet the mechanisms producing theobserved declines in species richness may differ between

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REVIEWS REVIEWS REVIEWS

Gulliver travels to the fragmented tropics:geographic variation in mechanisms ofavian extinction

Jeffrey A Stratford1 and W Douglas Robinson2

Irrespective of geography, forest destruction and fragmentation lead to lower avian species richness. Theunderlying mechanisms causing local extirpations have been studied most thoroughly in northern temperatelandscapes, where higher levels of brood parasitism, nest predation, and possibly decreased food availabilityare responsible for the loss of some species. Tropical landscapes are being similarly altered, but studies ofresponses by tropical birds remain relatively scarce. Predicting how tropical birds respond to habitat loss andfragmentation should not be extended directly from the results of temperate investigations. Tropical birdspossess different evolutionary and life histories, which make them vulnerable to a different suite of threatsthan those normally considered for birds from temperate regions. These same traits, including greater physio-logical and sensory specialization, reduced dispersal capabilities, and much lower local and regional popula-tion densities, indicate that strategies for conserving bird diversity will be different in tropical landscapes thanthose for temperate regions.

Front Ecol Environ 2005; 3(2): 91–98

1Department of Biological Sciences, Auburn University, Auburn, AL;2Oak Creek Lab of Biology, Department of Fisheries and Wildlife,Oregon State University, Corvallis, OR ([email protected])

In a nutshell:• Bird diversity declines in landscapes altered by habitat loss and

fragmentation, but most studies have been done in northerntemperate areas

• Tropical birds are also declining in disturbed landscapes, but asa result of different threats

• Lower tolerance of microclimatic changes or light environ-ments in fragmented habitats and lower dispersal abilities arefactors generally not considered for temperate birds

• Preservation of tropical diversity will improve if these traits areconsidered during reserve design

“T

Geography of bird extinctions JA Stratford and WD Robinson

the two regions. Conservation strategies applied in tem-perate North America may therefore be less effective inthe neotropics.

Here, we briefly review currently accepted hypotheses forbird extirpations as a result of forest fragmentation. We alsoidentify several hypotheses that should be considered andstudied in detail for neotropical birds. Our goal is not to pro-vide an exhaustive review of the hypotheses proposed toexplain declines or local extinctions of birds, but rather tohighlight the salient differences in responses to environmen-tal change by tropical and temperate birds. We focus largelyon comparing results from northern temperate areas withthose from tropical ones. Further study is needed to under-stand the degree to which factors operating in northern tem-perate landscapes also operate in southern temperate areas.

� Northern temperate extinction mechanisms

Brood parasitism

Of the primary factors responsible for population declines inthe temperate zone, brood parasitism (the laying of eggs innests of other bird species and subsequent abandonment ofoffspring to be raised by foster parents) by cowbirds hasreceived perhaps the most attention, at least in eastern andmidwestern North America (Smith et al. 2000). Brown-headed cowbirds (Molothrus ater) increase in abundance indisturbed landscapes, particularly fragmented forests in anagricultural matrix (Robinson et al. 1995). High levels ofcowbird parasitism can cause population declines, whichincreases the risk of local extirpations (Hoover 2003), andeven extinctions for a few extremely vulnerable species,such as Kirtland’s warbler (Dendroica kirtlandii) (Kepler et al.1996).

In contrast, brood parasitismappears to be a minor risk to forestbirds in most mainland neotropicallandscapes. Although two generalistbrood parasites, shiny (M bonariensis)and bronzed cowbirds (M aeneus),occur in Central and South Ameri-can landscapes, current levels ofbrood parasitism in fragmentedforests are generally low (Figure 1).The risks of brood parasitism can begreater in more subtropical land-scapes, such as Mexico, Argentina,and the West Indies, where cowbirdstend to be more numerous, and havecaused major declines in somespecies, such as the yellow-shoulderedblackbird (Agelaius xanthomus)(Wiley et al. 1991). Furthermore,where brood parasites do occur regu-larly in equatorial areas, they tend toparasitize only a few specific hostspecies with whom they may be

tightly coevolved, such as the giant cowbird (Scaphiduraoryzivora) and its hosts, oropendolas and caciques (Payne1997). Thus, one of the primary threats to forest birds livingin temperate fragments is currently of little or no conse-quence to most tropical species. How neotropical cowbirddistributions might change as landscapes become deforestedhas not, to our knowledge, been evaluated.

Nest predation

Reproductive failure in forest fragments may also becaused by abnormally elevated nest predation (Robinsonet al. 1995). Some edge-loving nest predators, such asskunks, raccoons, and snakes, are more abundant inhuman-altered landscapes (Chalfoun et al. 2002). Nestsin forest fragments may be easier for predators to detect,especially those located along edges, where predatoractivity is greater (Chalfoun et al. 2002). Other charac-teristics of the habitat remnant, such as vegetation struc-ture or food supply, may nevertheless remain attractive tobirds. In such instances, forest birds may be common, butfail at reproduction because of brood parasitism or nestpredation, a situation sometimes referred to as an ecolog-ical trap (Misenhelter and Rotenberry 2000).

Nest predation has yet to be studied rigorously in tropi-cal landscapes, fragmented or not, largely because of thedifficulty of finding sufficient numbers of nests of compar-atively rare species (Robinson et al. 2000). Extinctions ofbirds from Barro Colorado Island, Panama, a former hill-top of lowland rainforest isolated during flooding of thePanama Canal, have been explained by elevated levels ofnest predation (Terborgh 1974). The island, at 1562 ha,is too small to maintain populations of top carnivores,such as big cats and raptors, which may have allowed

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Figure 1. A pasture with cattle surrounding a forest fragment in central Brazil. In NorthAmerican landscapes, songbirds breeding in the remnant forest would suffer from highbrood parasitism, but in many neotropical landscapes proliferation of brood parasiticcowbirds is not yet a problem.

JA Stratford and WD Robinson Geography of bird extinctions

numbers of medium-sized mammaliannest predators to increase unchecked.Studies using artificial bird nests sug-gested that predation was greater onBarro Colorado Island than nearbymainland sites (Sieving 1992).However, the accuracy with whichartificial nests measure predation ofreal bird nests is questionable (Mooreand Robinson 2004). Furthermore,mammalian nest predators appear notto be abundant on Barro Coloradocompared with nearby mainland for-est where big cats and eagles areextant (Wright et al. 1994). Finally,video evidence of predators attackingunderstory bird nests on the islandindicated that 80% of attacks were bysnakes, not mammals (Figure 2;Robinson et al. in press).

Despite such concerns, can resultsfrom Barro Colorado be generalizedto other tropical landscapes? Becausethey are surrounded by water and aretherefore relatively protected frominvasions that threaten fragments surrounded by agricul-tural and suburban habitats (such as spread of edge-lovingnest predators), islands are good models for understandingecosystem disintegration (Leigh et al. 2002). Yet, mostfragments occur in areas where access by species from sur-rounding habitats is much easier. As discussed above, birdsin temperate regions suffer because of this. In tropicallandscapes, however, many of which are inhabited bysmall farmers, ease of access is also greater for humans,who commonly persecute snakes and larger mammals(Redford 1992). In a sense, then, top-down control of nestpredators could be greater in tropical fragmented land-scapes, allowing bird populations greater opportunity tobreed successfully. Apart from various artificial nest stud-ies, no other data from tropical landscapes allow an evalu-ation of the effects of fragmentation on predation risk.

Prey abundance

Forest fragmentation has been associated with decreasedprey abundance for near-ground or ground-foraging insec-tivorous birds (Burke and Nol 1998). Declines in foodavailability may be a consequence of microclimaticchanges such as increased temperature and decreasedhumidity near fragment edges (Williams-Linera 1990;Saunders et al. 1999). In the neotropics, arthropod popu-lation responses to fragmentation are complex and poorlyunderstood. As might be expected, the effects of habitatfragmentation differ across arthropod taxa and throughtime as the edge changes in structure (Didham 1997).Rainforest fragmentation does alter the composition ofarthropod communities, but the applicability of the

reduced prey abundance hypothesis is currently in doubtbecause many species of potential arthropod prey canbecome more abundant after fragmentation (Didham1997). Indeed, in Costa Rica, Sekercioglu et al. (2002)did not find any differences in prey biomass betweenforested and fragmented sites.

� Suggested additional mechanisms for neotropicalbird extinctions

Nest predation, brood parasitism, and prey abundance arethe three hypotheses commonly proposed to explain localextinctions in temperate and neotropical landscapes(Figure 3). Yet there is either no data to support thesehypotheses in the tropics, or the evidence suggests thatfragmentation has the opposite effect there. How, then,can we explain why neotropical birds in forest fragmentsbecome extinct? Instead of explanations that focus onbiotic interactions, we suggest that the evolutionary his-tories of neotropical birds have resulted in physiologiesand behaviors that make them less tolerant of environ-mental variation.

Physiological constraints

Microclimatic changes in fragments may affect birdsdirectly if altered temperature and humidity levels in for-est remnants expose them to evapotranspiration ratesthat cause physiological stress. The idea of greater habitatspecialization in the tropics is an old one (Janzen 1967;Karr and Freemark 1983), but has received less attentionthan it deserves (Marra and Remsen 1997). It is under-

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Figure 2. A neotropical bird-eating snake (Pseustes poecilinota) consumes a greattinamou (Tinamus major) egg in central Panama. Snakes are important predators in thelowland tropics and middle temperate latitudes, but are relatively uncommon or absent infar northern temperate areas.


standable that ornithologists studying birds in temperateregions tend to look elsewhere for useful hypotheses.Many of these species are probably more tolerant, giventhe wide range of conditions they encounter during a cal-endar year; migratory species, for example, must endurehighly variable climatic conditions as they journey thou-sands of kilometers. Non-migratory species must survive

temperatures varying from winter to summer by an orderof magnitude more than a resident rainforest specieswould experience in its entire lifetime, and more thansome tropical species’ ancestors might have experiencedin thousands of generations. Unlike species from temper-ate areas, many neotropical species may be much lessphysiologically tolerant of climatic variation, particularlyif those species inhabit the relatively stable understoriesof closed-canopy mature forest.

Evaluations of this hypothesis are lacking, because ofthe rarity of measurements of metabolic rates, particularlywith respect to ranges of thermal tolerance in neotropicalbirds. However, some indirect evidence is available.Resident insectivorous birds in Panama move to sites withhigher humidity during the heat of dry season days (Karrand Freemark 1983). Two common understory speciesnear Manaus, Brazil, exhibit slower feather growth rates inforest fragments compared to the feather growth rates ofbirds in continuous forest (Stratford and Stouffer 2001).In the Afrotropics, feather asymmetries of birds capturedin small fragments were more severe than those of birdsbirds in larger fragments, suggesting developmental prob-lems in the birds from small fragments (Lens et al. 2002).

Phylogenetically controlled comparisons of temperateand tropical bird physiological tolerances are needed. Ifthe metabolic constraint hypothesis is valid, many tropi-cal species should have narrower thermoneutral zones andbe less tolerant of small changes in temperature andhumidity. Predicting the size of those small changes couldbe accomplished by measuring annual ranges of tempera-tures and humidities experienced in the interior of unfrag-

mented forests (Figure 4). We also predictthat the fraction of bird communities dis-appearing in fragmented landscapes will benegatively correlated with the degree ofannual and daily climatic variation. Forexample, bird communities in more sea-sonal tropical environments, such as sea-sonally dry forests, some deserts, and higheraltitude habitats, should be more tolerantto fragmentation, whereas relatively asea-sonal lowland forest bird communities arelikely to contain a greater proportion offragmentation-sensitive species.

Bird species whose habitat use isrestricted to the most unvarying micro-habitats, such as the floor of old-growthforests, should be more sensitive to habitatfragmentation than birds inhabiting forestmicrohabitats with wider climatic fluctua-tions, such as canopy- and edge-dwellingspecies (Figure 4). Species distributiondata are consistent with this prediction,revealing that gap specialists and edge-lov-ing species (eg many types of humming-birds) are tolerant of fragmentation(Stouffer and Bierregaard 1995). In addi-

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Figure 3. Some specialized foragers, such as this bicoloredantbird (Gymnopithys leucaspis) in Panama, gather all theirfood by catching arthropods fleeing from raiding swarms ofpredatory army ants. When the ants disappear from forestfragments, the birds do too.

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K S

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Figure 4. Magnitude of daily temperature fluctuations within continuous forestincreases from the ground to the canopy and from the forest interior towards theforest edge and into grassland or pasture surrounding fragments (Didham andLawton 1999, and unpublished data). We hypothesize that species using the leastvariable microhabitats will be the most likely to disappear from landscapes lackingsuch relatively stable microclimatic refugia.


tion, the area available to a sensitive understory speciesshould be lower than the actual physical size of the frag-ments. Since edges are often exposed to sun and dryingwinds, they will tend to experience more microclimaticvariation than interior sites, which are protected fromsuch forces. Sensitive species would, therefore, drop out offragments earlier than would be predicted based solely onhabitat patch area. The role of physiological tolerances ormetabolic constraints as mechanistic explanations fortropical bird extinctions is ripe for further evaluation.

Visual constraints

Just as deforestation and forest fragmentation may pre-sent abiotic conditions that stress thermoregulatoryprocesses, visual constraints may also limit habitat use(Canaday 1996). We know that some neotropical birds,such as manakins and cotingas, are highly sensitive to thelight environments they select for sexual displays (Endlerand Théry 1996). Likewise, many other species may besensitive to changes in light levels. In mature tropical for-est, less than 5% of the light striking the canopy pene-trates to the ground (Shuttleworth et al. 1984). Birdspecies foraging exclusively in the lower understory or onthe ground of evergreen tropical forests must therefore seewell in low-light conditions. To do so, some species mayhave unusually large eyes to enhance light gathering orhave internal structural modifications that otherwiseenhance visual acuity in poorly lit situations.

A potential cost of such specialization is an inability touse brightly lit habitats such as large forest gaps, edges, orcanopies. Although such constraints will probably not leaddirectly to higher extinction risk, they could explain lowrates of recolonization after local extirpation by retardingthe progress of light-sensitive species across brightly lithabitat gaps. It is also possible thatspecies sensitive to bright light maybe unable to detect the presence ofdistant habitat patches in a land-scape. That is, their perceptual rangecould be limited compared to speciesthat forage regularly in gaps, edges,and other brighter habitats.

Given the general absence ofsuch light-limited habitats for diur-nal birds in temperate areas, thisdegree of specialization is unlikelyto be an important component ofextinction risk for these species.Particular groups of neotropicalbirds that might be more sensitiveto light conditions are the groundantbirds (Formicariidae) and someovenbirds (Sclerurus leaftossers).Tests of the light-sensitivityhypothesis should include histologi-cal comparisons of ocular structural

components and cell sensitivities between fragmenta-tion-sensitive and fragmentation-tolerant species.Comparisons could be done in a phylogenetically con-trolled manner, given the occurrence within some fami-lies (eg Thamnophilidae) of both forest-interior and gap-specialist species. Additional experiments could includehabitat choice tests in chambers where light environ-ments are manipulated and bird use of those environ-ments is quantified.

Dispersal ability

Another hypothesis that was previously dismissed as basi-cally irrelevant to temperate breeding birds is that somespecies could experience difficulties colonizing isolatedhabitat remnants. Given that birds are generally verymobile, the inability or unwillingness of neotropical birdsto traverse gaps seems surprising to many temperate-zonebiologists (Harris and Reed 2002). This attitude might bechanging, since more recent evidence suggests that somespecies from temperate regions may be more inhibitedfrom crossing gaps than others (Bélisle et al. 2000; Gobeiland Villard 2002). Considering that many temperate-zone species fly thousands of kilometers during migration,it is particularly interesting that we are discovering howsome species settle for a breeding season and then appearto restrict what types of landscapes they will movethrough (Bélisle and St. Clair 2001).

In contrast, dispersal limitation is a longstandinghypothesis among tropical ornithologists (Wallace 1853;Willis 1974; Mayr and Diamond 2001). Within the trop-ics, there may be hundreds of forest-dwelling species thatwill not move across non-forested habitats (Figure 5). Forinstance, Develey and Stouffer (2001) found that manymixed-flock species were unlikely to cross a road of only

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Figure 5. A river in central Brazil. Alfred Russell Wallace first noticed that few forestbirds fly across water in the lowland neotropics. Genetic studies have also demonstratedreduced avian gene flow across tropical rivers.


30 m in width. Consequently, when populations in iso-lated forest remnants disappear, for whatever reason, theprobability of recolonization ever reconstituting a popu-lation will be minimal, perhaps even zero, for somespecies (Robinson 1999). Such dramatic restrictions onimmigration are highly unlikely in most temperate land-scapes, perhaps because of the propensity of many speciesto exhibit long-distance movements during migrationand postnatal dispersal. Studies of genetic differentiationsupport the idea that many neotropical species are quitesedentary (Capparella 1988; Bates 2000), whereas mostspecies from northern temperate areas show little geneticdifferentiation across their geographic ranges (Lovette etal. 2003).

Long-term datasets evaluating extinction and recolo-nization phenomena are rare for any landscape. A simplecomparison between Kendeigh’s (1980) long-term sur-veys of Trelease Woods in central Illinois, USA, andlong-term data from Barro Colorado Island, Panama(Willis and Eisenman 1979; Robinson 1999), indicatesregular recolonization in the temperate fragment but notin the tropical one (Figure 6). Acquiring additionallong-term survey data from fragmented landscapes isneeded to better understand this possible latitudinal dif-ference in immigration tendencies. Experimentalapproaches are also needed to evaluate the abilities oftropical species to cross habitat gaps of various distancesand across various habitat types. For example, dispersalacross agricultural habitats such as pastures or row crops

may not be as difficult as flights acrossopen water if some species are willingto leave forest but need stoppingpoints along the way to ensure a suc-cessful journey.

Low population densities and largehome ranges

The average abundance of most forest-dwelling, neotropical species is anorder of magnitude lower than theirnorth temperate ecological counter-parts (Terborgh et al. 1990; Robinsonet al. 2000). In Amazonian Peru, 35%of species occur in densities of <1pair/100 ha and median abundance is2.5 pairs/100 ha (Terborgh et al. 1990).In other Amazonian sites, medianabundance may be even lower(Stouffer and Bierregaard 1995). Lowabundance goes hand in hand withmuch larger home ranges in the trop-ics, establishing a greater degree ofarea-sensitivity than is normally seenin bird species from northern temper-ate zones. The smallest territories ofpasserines in Amazonia are 3 to 4 ha,

whereas many breeding season territories of birds intemperate areas are less than 1 ha (Terborgh et al. 1990).When forests are fragmented, the rarity of most tropicalspecies will result in a low probability of occurrence.Likewise, large territory sizes and patchy distributionswill ensure that few individuals of most species will bepresent even in 100-ha fragments, a size that many biol-ogists studying northern temperate species would con-sider to be large. The probability of long-term persis-tence in all but fragments of hundreds to thousands ofhectares is expected to be small unless recolonizationsare frequent.

� Conclusions

The unusually specialized lives of tropical birds, relativeto temperate species, subjects them to greater risk ofextinction in altered landscapes. The most sensitivespecies are highly adapted to environments of the under-story and forest floor, where variations in humidity, tem-perature, and light are very small. Furthermore, at leastover recent evolutionary time, the continuous distribu-tion of mature forest means that year-round residentspecies rarely, if ever, had to cross non-forest habitats,resulting in morphological specializations for walkingand reduced abilities for sustained flight. Although manyof these hypotheses still require intensive evaluation byexperimental and observational studies, the pace atwhich tropical landscapes are being fragmented demands

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Figure 6. Diagrammatic representation of recolonization patterns in a temperatefragment, Trelease Woods, Illinois, US, and a tropical fragment, Barro ColoradoIsland, Panama. Stippled bars indicate years in which survey data were available.Solid bars indicate dates each species was present. Species are year-round residents, somigratory behavior does not account for recolonizations. Data from Barro Coloradoare for six year-round residents with loud, distinctive songs, which are thereforeunlikely to be missed by ornithologists if the species were present. Recolonization ofTrelease Woods after local extirpation was common, whereas none of the speciesrecolonized Barro Colorado Island.


that we move forward and designtropical reserve systems with thesespecialized lives of tropical birds inmind. We suggest the followingapproaches.

First, given the very large homeranges and the general rarity ofmost species, every effort must bemade to preserve the largest habitatremnants still extant. In manycases, this should include thepreservation of many small forestpatches in a region, followed by thereforestation of surrounding dis-turbed habitats. Some dispersal-limited species may not moveacross pastures, but will movethrough young second-growth for-est, which will facilitate passiverecolonization of smaller fragments.

Second, when protection of thematrix surrounding fragments isimpossible, corridors connectingisolated remnants are essential.Reducing the isolation of patches by reconnecting themis absolutely critical to promote dispersal in the tropics,although it may not be necessary in many temperatelandscapes (Hannon and Schmiegelow 2002).

Third, the effective area of remnants will be increasedif microclimatic variability is reduced and the light envi-ronment is carefully regulated (Figure 7). Three strate-gies will help here. One is to construct vegetative buffersaround edges of new fragments to reduce wind and lightpenetration. In many neotropical locations, the creationof buffer zones can be accomplished relatively quicklyand passively by allowing second-growth trees to growaround the margins of forest fragments. Additional con-siderations are to exclude cattle and other grazers whichdefoliate the ground and understories of forests and toexclude, or carefully limit, timber extraction, as theremoval of timber permits increased solar penetration byopening up canopies.

These approaches will also benefit conservation ofbirds in temperate regions, but many tropical birds lackthe same levels of resilience to disturbance because oftheir evolutionary and life histories. Gulliver would alsohave found the lives of tropical birds to be very peculiar.Understanding these peculiarities will lead to effectiveconservation.

� Acknowledgements

We thank the Brazilian and Panamanian natural resourceagencies for allowing us to study birds in their countries.The work was supported by the Auburn UniversityCenter for Forest Sustainability and National ScienceFoundation grants 0212587, 0408186, and 0422233.

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