Does hunting threaten timber regeneration in selectively logged tropical forests?

Cooper Rosin

1 Hunting and land use change modify native herbivore abundances and cause cascading effects in natural ecosystems. The outcomes for vegetation depend on changes to specific plant-animal interactions, such as seed dispersal or predation, or physical disturbances. 2 We experimentally manipulated terrestrial wildlife populations in a primary low-land forest in Malaysia over an 18-year period (1996-2014) to understand how artificially high or low animal densities affect tree and liana regeneration. Our study site retains a diverse wildlife community and artificially high densities of native wild pigs (Sus scrofa) that are sustained by crop raiding in distant oil palm plantations. We used fencing that excluded terrestrial animals >1 kg to experimentally simulate conditions similar to those in defaunated forests. These two treatments-abnormally high pig abundances and megafauna loss from hunting-represent common outcomes in disturbed Southeast Asian forests and are characteristic of many forests globally. We focused on trees and lianas because they are the two dominant woody life-forms in tropical forests and crucial determinants of forest structure and function. 3 We found that liana sapling abundances (30-100 cm height) increased by 86% in unfenced control plots with wildlife but were stable in exclosures. In contrast, tree abundances did not change in unfenced control plots but increased by 83% in ex-closures without wildlife. Evidence of scaring on surviving stems suggested that these inverted outcomes were driven by selective use of tree saplings for wild pig nests. Lianas may also have greater tolerance to wildlife disturbances like nest building. By the end of the study, lianas comprised 38% of all saplings in unfenced controls but just 14% in exclosures. 4 Synthesis and applications. We conclude that artificially abundant wildlife, such as crop-raiding wild pigs, may shift tropical forest understories towards lianas while defaunation may shift it towards trees. These results highlight that ecological cascades from hunting or land use change can alter plant functional types and reshape to long-term patterns of forest succession and change. Managing unnatural wild boar populations may be required to conserve native plant communities in both their native and exotic ranges.

We introduce a special section that addresses the bushmeat or wild meat crisis, its direct impact on game species, and its indirect impact on plants in tropical forests.Introducimos una sección especial que trata la crisis de la carne de animales salvajes, su impacto directo sobre las especies cazadas y su impacto indirecto sobre las plantas en los bosques tropicales.

It has been suggested that the disturbance caused by logging of tropical forests impairs timber tree regen-eration, whilst foresters view logging as a means to stimulate both the growth of the residual trees and the germination and establishment of new recruits. Whilst substantial increases in tree seedlings after logging have been shown, there have been no direct tests of whether this initial enhancement is maintained. We tested if the initial response to logging in a tropical forest in Ghana resulted in increases in seedling recruitment relative to unlogged parts of the same forest and whether subsequent seedling mortality was greater in areas disturbed by logging. We also compared seedling composition, density, species diversity and height 7 y after logging to see if disturbed areas differed from unlogged areas. Timber tree species seedling recruits were assessed after logging in 160 sample plots randomly located on skid trails, felling gaps and in unlogged parts of the same forest. Recruits were named, tagged, mapped, counted and heights measured on five occasions spanning 7 y after logging had ceased. Seedling recruitment was initially enhanced by logging disturbance, principally by Pioneer species, but after 1 y Non-Pioneers dominated the recruits. Mortality of recruits was initially greater in unlogged areas but declined over the 7 y of the study converging on that of disturbed areas to an annualised rate of 0.2. The resultant densities of surviving recruits declined after the initial increase, especially amongst Pioneers. After 7 y, Pioneers were least abundant. Species diversity was initially enhanced by logging disturbance but declined on skid trails after 3 y. In unlogged forest, diversity of recruits increased steadily, and converged on disturbed samples by 7 y. Species composition of recruits initially differed between unlogged and logged samples, but showed convergence after 3 y. The initial effects of disturbance were, however, still detectable at 7 y. The results confirm the initial enhancement of timber tree recruitment after logging disturbance which suffered no greater mortality than unlogged areas. Within 7 y of logging, however, most measures of seedling dynamics were similar in logged and unlogged forest presumably due to canopy closure. Whilst most of the tallest trees at 7 y were Pioneer timber species, Non-Pioneers were numerically dominant. We conclude that appropriately controlled logging does not impair timber tree regeneration. The benefits appear to be securing the establishment and fast growth of Pioneer timber species whose regeneration might be less successful in unlogged forest.

Forest Ecology and Management 331 (2014) 153–164 Contents lists available at ScienceDirect Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco Review Does hunting threaten timber regeneration in selectively logged tropical forests? Cooper Rosin ⇑ Nicholas School of the Environment, Duke University, P.O. Box 90328, Durham, NC 27708, United States a r t i c l e i n f o Article history: Received 6 June 2014 Received in revised form 3 August 2014 Accepted 4 August 2014 Keywords: Herbivory Hunting Natural forest management Seed dispersal Seed predation Timber regeneration a b s t r a c t Avoiding the conversion of tropical production forests to non-forest land uses is a forestry and conservation priority, and is contingent on successful regeneration of commercially important species. The underlying ecological processes that facilitate regeneration, however, are poorly understood. Perhaps as a result, timber yields after regeneration can be lower than expected. Hunting is widespread in timber concessions, and may threaten regeneration by disrupting the various processes facilitated by wildlife. Vertebrate seed dispersers are often heavily hunted, resulting in reduced seed movement for many species and a shift in community composition to favor those plants dispersed by small animals and abiotic means. Timber species with large seeds and fleshy fruit are at particular risk for dispersal and recruitment failure. Hunting also alters granivore communities, resulting in increased predation on species favored by insects and small rodents, and changing the spatial template of seed predation, with detrimental effects on many timber species. Large vertebrate herbivores decline with hunting pressure, resulting in the modification of plant competitive interactions. This is disadvantageous to several traits that are common among timber trees, including relatively slow growth and high wood density. A lack of appreciation for – and management of – these interactions could threaten forest biodiversity, limit future timber production, and increase the likelihood of forest conversion for other land uses. In this review, I highlight the plant-animal interactions that could influence timber regeneration in tropical forests, as well as how these processes might be expected to change under hunting pressure. The review concludes with recommendations for management and future research priorities. ! 2014 Elsevier B.V. All rights reserved. Contents 1. 2. 3. 4. 5. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Seed dispersal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Seed predation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Herbivory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Management considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Future research priorities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Introduction Timber production represents a major land use for tropical forests worldwide, encompassing 403 million hectares (Blaser et al., ⇑ Tel.: +1 (608) 772 2667. E-mail address: cooper.rosin@duke.edu http://dx.doi.org/10.1016/j.foreco.2014.08.001 0378-1127/! 2014 Elsevier B.V. All rights reserved. 153 154 156 158 159 159 160 161 161 2011) – roughly half the area of the contiguous United States. Though logging can have various detrimental impacts on tropical forests (eg Johns, 1988; Bawa and Seidler, 1998; Fimbel et al., 2001), there is mounting evidence that timber concessions are not without environmental merit, potentially meeting both forestry and conservation goals (Johns, 1985, 1997; Putz et al., 2000; Meijaard et al., 2005; Clark et al., 2009; Berry et al., 2010). 154 C. Rosin / Forest Ecology and Management 331 (2014) 153–164 Selectively logged forests under responsible management represent a valuable ‘‘middle way’’ between deforestation and absolute protection (Putz et al., 2012, but see also Rice et al., 1997). Avoiding the conversion of production forest to non-forest land uses is thus critical, and relies on continued regeneration of commercially important species. Most selective timber systems with sustained yields (Putz et al., 2012) use one form or another of natural forest management (see reviews by Baur (1964) and Buschbacher (1990), but see also Bawa and Seidler, 1998). These management schemes rely to varying degrees on the natural regeneration of target timber species, often with simple silvicultural treatments. Reproduction under close-tonatural forest conditions – for eventual harvest in future cutting cycles – is less labor intensive and expensive than other methods, and is thus a favored forestry scheme across much of the tropics (Weetman and Vyse, 1990; Goméz-Pompa and Burley, 1991). Recent evidence shows that the post-harvest regeneration of timber species can be lower than expected (Fredericksen and Mostacedo, 2000), highlighting the need to understand the ecological requirements of these tree species and identify the causes of regeneration failure. Plant-animal interactions are increasingly recognized as critical to maintaining tropical forest integrity and composition, particularly the processes of seed dispersal (eg Terborgh et al., 2008), seed predation (eg Asquith et al., 1997), and herbivory (eg Clark et al., 2012). These processes may play a role in timber regeneration, given the extensive interactions between timber species and tropical forest wildlife (see Tables 1 and 2). Disruptions to plant-animal interactions can have consequences both for biodiversity and forest carbon production (Wright, 2003; Brodie and Gibbs, 2009; Jansen et al., 2010; Poulsen et al., 2013), though the specific effects on the regeneration of timber are largely unknown. As a result, logging companies generally lack any practical management of these processes, despite their apparent importance (Terborgh, 1995; Hammond et al., 1996; Guariguata and Pinard, 1998; Sheil and Van Heist, 2000; Putz et al., 2012). A major threat to the integrity of plant-animal interactions is the increasing impact of hunting for subsistence and the commercial wild meat trade (Redford, 1992). Hunting is widespread in tropical forests (Robinson and Bennett, 2000; Fa et al., 2002), and is further facilitated by logging through the creation of road networks and increased access to frontier forests (Wilkie et al., 2000). Hunting within concessions can be particularly intensive, as extractive industries promote immigration and timber companies rarely provide supplemental protein to their workers’ diets (Robinson et al., 1999; Auzel and Wilkie, 2000; Poulsen et al., 2009). Overall, hunting within concessions affects animal distributions more strongly than do the direct effects of logging (van Vliet and Nasi, 2008; Poulsen et al., 2011). Hunting alters ecological processes in many ways (see reviews by Wright (2003), Stoner et al. (2007), Abernethy et al. (2013) and Kurten (2013)). If these processes are important for the regeneration of timber, disruptions to them may threaten continued production and must be managed appropriately. In this review, I highlight the plant-animal interactions that could influence timber regeneration, as well as how these processes might be expected to change under hunting pressure, with a focus on seed dispersal, post-dispersal seed predation, and herbivory. I identify specific interactions between hunted wildlife and prominent timber tree species, with attention to the world’s three main regions of tropical forest. The review concludes with recommendations for management and future research priorities. 2. Seed dispersal Dispersal confers several potential reproductive advantages to the seed. Dispersed seeds may benefit from colonizing novel and uncompetitive environments, landing in sites suitable for establishment, and escaping the vicinity of the parent (Howe and Smallwood, 1982; Willson and Traveset, 2000; Muller-Landau and Hardesty, 2005). Escape through dispersal reduces the incidence of attack on seeds and seedlings by host-restricted natural enemies near the parent tree, as described by the Janzen–Connell model (Janzen, 1970; Connell, 1971). This model of distance- and density-responsive mortality mechanisms is well-supported scientifically (see reviews by Hammond and Brown (1998) and Terborgh (2012)), and dictates a major role of seed dispersal in regeneration success. Indeed, there is strong evidence that nearly all sapling recruits arise from seedlings of dispersed seeds (Howe and Miriti, 2000; Terborgh and Nuñez-Iturri, 2006; Terborgh, 2013). Any disruption to the dispersal process may have impacts on individual trees, species, and communities. In particular, hunting threatens the integrity of animal-mediated dispersal, with potential consequences for timber regeneration in forests subject to such pressures. The majority of tree species in humid tropical forests produce seeds with fleshy fruit or aril and are dispersed by animals (Howe and Smallwood, 1982; Willson et al., 1989; Jansen and Zuidema, 2001; Beaune et al., 2013). Many species producing a hard pericarp are also dispersed by vertebrates through caching and other pathways (Janzen, 1971; Forget, 1990; Jansen and Forget, 2001; Hulme, 2002; Beck, 2005). Dispersal by animals is thus widespread, and is probably as common for potential timber species as for tropical forest tree species in general (Jansen and Zuidema, 2001). Trees with vertebrate-dispersed seeds account for 72% of the 95 timber species in the Guianas (Hammond et al., 1996), and 74% of the 46 timber species in Bolivia (Jansen and Zuidema, 2001). Although this over-represents animal dispersal among the few timber species most desired by current world markets (see Table 1), proportions of animal-dispersed timber trees are expected to increase with depletion of high-value, wind-dispersed timbers and growing demand for lesser-known species (Jansen and Zuidema, 2001; Putz et al., 2001). Dispersal by animals is clearly important for many timber species (see Tables 1 and 2), though few studies have determined its specific role in regeneration success. As noted above, dispersal which increases seed distance from the parent tree may be critical for timber regeneration. Pulp removal and gut passage may also improve survival and germination of animal-dispersed seeds (Traveset, 1998; Traveset and Verdu, 2002; Levi and Peres, 2013). To assess the value of dispersal for the timber tree Virola surinamensis in Panama, Howe et al. (1985) monitored seeds and seedlings located near the parent, noting over 99% mortality by insects and mammals within 12 weeks; seeds dropped 45 m from the fruiting tree were at an advantage of up to 44-fold compared to their undispersed counterparts. Similarly, undispersed seeds and seedlings of the timber species Pycanthus angolensis and Canarium schweinfurthii in Cameroon faced substantially greater mortality by invertebrates and rodents than those that had been dispersed by primates (Mbelli, 2002). Poor natural regeneration of the Guyanese timber tree Hymenaea courbaril beneath its own canopy supports the assertion that primate dispersal is critical for recruitment, with 98% of undispersed seeds suffering mortality due to bruchid beetle attack (Hammond et al., 1992). Hammond et al. (1999) found that while dispersal of the timber tree Chlorocardium rodiei did not completely preclude natural enemy attack, it did delay predation long enough to promote germination success with increasing distance from conspecific adults, thus dispersal benefitted trees through a combination of spatial and temporal factors. Documented recruitment failure in the absence of dispersal is a concern for timber production, given that animal dispersers – and their services – are strongly impacted by hunting. Most highly desirable game animals of tropical forests are prominent seed 155 C. Rosin / Forest Ecology and Management 331 (2014) 153–164 Table 1 Ecological characteristics and plant-animal interactions of the 10 most commonly harvested timber tree species (based on volume exported in 2011 and 2012; ITTO, 2012) from the world’s three main regions of tropical forest. Note the disproportionate representation of wind dispersed species by current harvests; these species are often favored because of their long, straight boles. Scientific name Family Disperser(s) Seed predator(s) Herbivore(s) Diaspore Volume (1000 m3) Tabebuia spp. Peltogyne venosa Bignonaceae Leguminosae Wind Wind, monkeys Insectsd Insects Winged Pod 142 79 Swartzia spp. Fabaceae Insects, mammals Fleshy 68 Dicorynia guianensis Mora excelsa Leguminosae Bats, birds, rodents, monkeys Wind, gravity Saki monkeysa Beetles, ants, saki monkeys (P. paniculata)o Rodents, ants Insects, rodents, brocket deeri Rodents Insects Pod 37 Insects Pod 35 Chlorocardium rodiei Goupia glabra Eperua falcata Lauraceae Insects, rodents Insects 32 Insects, rodents Insects, rodents, peccariesr, saki monkeysa,o Insects Insects, mammalss Woody nut Fleshy Pod Peccariest, beetles Leaf miner insects Fleshy 10 Atta spp. ants Fleshy 9 Elephants; psyllids (Pseudophacopteron spp.), caterpillars, chimpanzees (flowers) Winged 1063 Winged 509 Psyllids, Anaphe venata silkworm, other insects Iroko gall fly, gorillas Winged nut Fleshy 364 Insects 202 Colobus monkeysR, insects Cottony floss Pod/ winged Pod 143 Numerous animals Winged 75 Hyblaea and Eutectona caterpillars, other arthropods Woody nut Winged 71 Neotropics Manilkara bidentata Catostemma commune Leguminosae Goupiaceae Leguminosae Sapotaceae Water, fish, rodents (secondary) Scatterhoarding rodentss Birds Explosive dehiscence, scatterhoarding rodents (secondary)r Birdsq, monkeysl i Bombacaceae Monkeys, bats, other mammals Brocket deer (C. fragrans) Aucoumea klaineana Burseraceae Wind Entandrophragma cyclindricum Triplochiton scleroxylon Chlorophora excelsa/Milicia excelsa Ceiba pentandra Meliaceae Wind Sterculiaceae Wind Moraceae Birds, bats, and squirrels Malvaceae Wind Leguminosae Wind Dysdercus cotton stainer, other insects Primates Leguminosae GorillasC, other primates Colobus monkeysR Fabaceae Wind, animals (secondary) Lamiaceae Wind Beetles Meliaceae Wind RodentsE,D antelopes, shoot borers, lepidopterous insects Wind, scatterhoarding rodents Wind, scatterhoarding rodents Wind Insects, rodents, primates, bearded pigs Insects, rodents, primates, bearded pigs Beetles Insects, rodents, primates, bearded pigs Insects 11 10 Afrotropics Cylicodiscus gabonensis Erythrophleum ivorense Pterocarpus soyauxii Tectona grandis Entandrophragma utile Rodents (Entandrophragma spp.)D Insects Insects 306 181 63 Indo-Malayan Tropics InsectsP, rodentsP, other mammals Shorea spp. Dipterocarpaceae Dipterocarpus spp. Dipterocarpaceae Tectona grandis Lamiaceae Dryobalanops spp. Dipterocarpaceae Xylia xylocarpa Leguminosae Wind, scatterhoarding rodents Explosive dehiscence Hevea brasiliensis Koompassia spp. Acacia mangium Euphorbiaceae Leguminosae Fabaceae Explosive dehiscence Wind, orangutansF Birds, ants Beetles, ants Mammals, insects Parashorea spp. Dipterocarpaceae Anisoptera spp. Dipterocarpaceae Wind, scatterhoarding rodents Wind, scatterhoarding rodents Insects, rodents, primates, bearded pigs Insects, rodents, primates, bearded pigs Beetles and other insects, snails, mammals Insects, mammals dispersers, including large primates, duikers, deer, tapirs, and other ungulates (Redford and Robinson, 1987; Feer, 1995; Fa et al., 2005; Insects, mammals Hyblaea and Eutectona caterpillars, other arthropods Insects, porcupines, other mammals Insects Winged nut Winged nut Woody nut Winged nut Woody pod Capsule Winged Coiled pod Winged nut Winged nut 4041 2700 965 810 718 172 163 152 85 81 Corlett, 2007; Peres and Palacios, 2007; Beaune et al., 2013). In general, frugivorous vertebrates suffer greater declines with 156 C. Rosin / Forest Ecology and Management 331 (2014) 153–164 hunting pressure than either granivorous or folivorous species, regardless of body size (Peres and Palacios, 2007). Animal dispersers can be partitioned into several non-overlapping ‘‘syndromes’’ based on morphological traits of the fruits they consume (Gautier-Hion et al., 1985). While there may be many potential dispersers for any one timber species (Howe and Smallwood, 1982), they can vary in their effectiveness (Schupp, 1993), and actual redundancy may be lower than anticipated based on dietary overlap (Poulsen et al., 2002). Additionally, the removal of a given disperser may change regeneration patterns by altering the tree’s seed shadow and susceptibility to predation (Janzen and Vázquez-Yanes, 1991). Large-bodied vertebrates are capable of ingesting – and dispersing, via endozoochory – a greater quantity and size range of fruit than smaller animals (Corlett, 1998; Peres and Van Roosmalen, 2002; Knogge and Heymann, 2003). Dispersal of timber trees reliant on large animals is thus unlikely to be compensated for by smaller non-game taxa, except perhaps in cases where a given species is additionally dispersed via synzoochory (as by bats). In the Guianas, for example, the seeds of most timber trees are animal-dispersed and larger than one gram – too large to be effectively dispersed by smaller animals (Hammond et al., 1996). Some trees may have one or very few critical dispersers (Howe, 1977; Hallwachs, 1986; Tutin et al., 1991; Asquith et al., 1999), and face dispersal failure when these particular species are absent. In Uganda, chimpanzees are the primary – perhaps sole – dispersers of the timber tree Cordia millennii (Plumptre et al., 1994; Bakuneeta et al., 1995; Reynolds, 2005), and in Gabon, the only known disperser for the timber tree Cola lizae is the lowland gorilla (Tutin et al., 1991). Even moderate hunting of important dispersers, as in ‘‘half-empty’’ forests (Redford and Feinsinger, 2001), may be sufficient to alter timber regeneration patterns. McConkey and Drake (2006) found that hunted flying foxes ceased to function as dispersers for three timber species (Pouteria grayana, Syzygium clusiifolium, and S. dealatum) long before they became rare. Shifts in abundance of vertebrate dispersers may have variable effects on plants. While large-bodied dispersers are reduced or extirpated with hunting, densities of small-bodied fauna can increase through compensatory mechanisms (Peres and Dolman, 2000; Rosin and Swamy, 2013). As a result, hunting reduces dispersal of large-seeded trees, while those dispersed by small animals and wind tend to increase in abundance (Wright et al., 2007; Stoner et al., 2007; Nuñez-Iturri et al., 2008; Terborgh et al., 2008; Vanthomme et al., 2010; Effiom et al., 2013; Harrison et al., 2013; Kurten, 2013). This shift in dispersal based on reproductive traits such as seed size has important consequences for timber trees specifically. When compared against the tree community as a whole, the seeds of fleshy-fruited timber species can be significantly larger than those of non-timber species (Hammond et al., 1996), and thus more negatively affected by changes to the disperser assemblage due to hunting. For one particular guild of small-seeded plants, the winddispersed lianas, hunting can promote significantly increased abundance (Wright et al., 2007), though widespread evidence is limited. Lianas are detrimental to timber trees; they induce stem deformations and other mechanical damage, slow diametric growth, and increase the likelihood of the host tree falling (Putz, 1982, 1991; Clark and Clark, 1990). Infested trees may suffer reduced seed production (Stevens, 1987; Nabe-Nielsen et al., 2009) and possible recruitment failure in adjacent gaps, given that lianas can impede the successional process (Schnitzer et al., 2000). Combined, these factors lead to poor timber regeneration when lianas are abundant (Grauel and Putz, 2004). Lianas also hinder timber harvest and complicate management, as liana-laden trees cause greater felling damage to the surrounding forest (Fox, 1968; Appanah and Putz, 1984; Johns et al., 1996) and raise costs associated with liana cutting and herbicide treatment (Putz, 1991). By benefitting lianas, hunting may thus indirectly reduce timber production and profitability. There is ample evidence both that animal-mediated dispersal is important for many timber species, and that hunting alters this process. Trees reliant on large vertebrates face dispersal failure, heightened natural enemy attack, and increased abundance of competitors such as lianas, all of which may hinder timber regeneration in forests subject to hunting pressure. 3. Seed predation Seed predation is an important ecological interaction which can regulate plant population dynamics (Janzen, 1971; Crawley, 1992; Hulme, 1998). As seed predators are abundant and diverse in tropical forests, and consume the seeds of many timber tree species (see Tables 1 and 2), it is reasonable to assume that they may impact regeneration processes, though direct evidence is limited. In particular, changes to community composition of seed predators, as can occur under hunting, may alter seed predation regimes and differentially impact tree recruitment. Large mammalian granivores such as pigs (Suidae) and peccaries (Tayassuidae) exert predation pressures that influence tree recruitment (Ghiglieri et al., 1982; Bodmer, 1991; Curran and Webb, 2000; Ickes et al., 2001; Silman et al., 2003; Beck, 2005; Beaune et al., 2012). Small mammals, particularly rodents, can be voracious seed consumers as well (Fleming, 1975; Smythe, 1986; Hulme, 1993; Blate et al., 1998), with potentially stronger seed predation pressures than larger mammals (Terborgh et al., 1993; DeMattia et al., 2004; Paine and Beck, 2007). Rodents prey on seeds even when alternative resources such as pulpy fruits are available (Adler, 1995), and can kill seedlings up to several weeks after germination, to exploit sprouts and seed reserves (DeSteven and Putz, 1984; Forget, 1997). Insects and other arthropods are also important seed predators of timber species (see below; Toy, 1988; Hammond et al., 1992), and impact seeds differently than vertebrates (Janzen, 1971; Terborgh et al., 1993; Notman and Villegas, 2005). Small rodents tend to favor seeds of small size (Blate et al., 1998; Vieira et al., 2003; Dirzo et al., 2007), exerting predation pressures unique from large mammals (DeMattia et al., 2004; Mendoza and Dirzo, 2007; Hautier et al., 2010). Agoutis and peccaries also differ in their seed preferences based on the presence of chemical and/or physical defenses (Kuprewicz, 2012), and specialized invertebrates such as bruchid beetles and other weevils can process seed compounds toxic to larger animals (Janzen, 1971). Given that different granivores have distinct seed preferences, changes that alter the relative abundance of these fauna may substantially alter seed predation pressures. Hunting contributes to compositional change of seed predator communities, with potentially important consequences. Pigs and peccaries are frequently hunted, as are some large rodents like agoutis and porcupines, while smaller rodents such as squirrels, rats, and mice are much less favored (Redford and Robinson, 1987; Clayton et al., 1997; Fa et al., 2005; Rao et al., 2005; Corlett, 2007). This disparity of harvest rates can shift faunal community composition, while interspecific dynamics may further enhance these changes. As with primates (described above), compensatory responses can occur when two or more species share a common resource and are differently impacted by hunting, thus small rodents may increase in abundance with hunting pressure even while total animal biomass declines (Smythe, 1987; Happold, 1995; Phillips, 1997; Wright, 2003). Observational and experimental evidence support this, with greater abundance of small and medium-sized rodents documented in sites where their predators and/or competitors are absent (Glanz, 1991; Adler and 157 C. Rosin / Forest Ecology and Management 331 (2014) 153–164 Table 2 Ecological characteristics and plant-animal interactions of less commonly harvested timber tree species from the world’s three main regions of tropical forest. Harvest rates are currently low but expected to increase as the market for lesser-known timber species increases (Jansen and Zuidema, 2001). Species selected based on frequent mention in the literature and/or future market potential. Scientific name Family Disperser(s) Seed predator(s) Herbivore(s) Diaspore Amburana spp. Araucaria angustifolia Brosimum utile Leguminosae Araucariaceae Wind Birds, rodents, and other mammalse Insects Peccaries, rodents Insects Insectsf Moraceae Carapa guianensis Cedrela spp. Meliaceae Monkeysc,l, tapirs (B. parinaroides)m, birds, peccariesn Scatterhoarding rodents Insects, deer Meliaceae Wind Brocket deer (Brosimium spp.)i, saki monkeysa,o, peccariesp Brocket deeri, saki monkeysp, rodents, peccaries Saki monkeysa Winged Fleshy nut Fleshy Woody nut Winged Cordia goeldiana Dinizia excelsa Boraginaceae Leguminosae Hymenaea courbaril Ocotea spp. Leguminosae Birds, monkeysl Wind/gravity, rodents and other mammals (secondary)g Monkeys, scatterhoarding rodents Lauraceae Numerous birds and mammals Pradosia ptychandra Swietenia spp. Sapotaceae Monkeysl Meliaceae Wind, rodents (secondary) Trattinickia spp. Virola spp. Burseraceae Myristicaceae Birdsq, monkeysl Birds, monkeysk Sapotaceae Elephants, gorillasC Bush pigs, porcupines Sapotaceae Elephants, giant pouched rats, monkeys Bush pigs, porcupines Leguminosae Birdsz Neotropics Shootborer (Hypsiplya grandella), other arthropods Brocket deeri Parrots, macaws, beetlesh Fleshy Pod Saki monkeysa, peccaries, rodents, beetlesc Small rodentsj, insects, brocket deeri, peccaries Saki monkeysa, peccaries (P. surinamensis)S, beetles Beetles, rodentsb Beetles, rodents, peccaries, brocket deeri, saki monkeysc Atta spp. ants Insects, mammals Fleshy nut Fleshy Insects, mammals Fleshy Shootborer (Hypsiplya grandella) Winged Insects, deer, tapirs Fleshy Fleshy Afrotropics Autranella congolensis Baillonella toxisperma Copaifera mildbraedii Dacryodes buettneri Diospyros crassiflora Gambeya africana Gilbertiodendron dewevrei Guarea cedrata Khaya ivorensis Lophira alata Millettia laurentii Nauclea diderrichii Staudtia spp. Testulea gabonensis Fleshy Bush pigs, antelopes, elephants Fleshy fLeshy u,v,w Burseraceae Numerous birds, squirrels, monkeys, apes Ebenaceae Birds, gorillas29, mandrillsA,y, other animals Sapotaceae GorillasC, chimpanzees, elephants, birds Explosive dehiscence, gorillas Meliaceae Meliaceae Ochnaceae Hornbills, monkeys, duikers, porcupines Wind Wind, mandrillsA Fabaceae Explosive dehiscence y Red river hogs , mandrills , rodents Red river hogs (G. lacourtiana)x, mandrillsA Red river hogsx, antelopes, elephants, rodents, primates Menemachus beetles Beetles, rodents Rodents, mandrillsA, colobus monkeysR C Leguminosae x B Elephants Fleshy Jumping plant-lice Fleshy Fleshy Forest buffaloes, bongos; elephants Psyllids, other insects Gall-forming insects, gorillasv, colobus monkeysR Caterpillars, apesw, colobus monkeysR Shoot-boring moth larvae Pod Fleshy Winged Winged Pod Fleshy Rubiaceae Birds, elephants, duikers, monkeys, gorillas Myristicaceae Luxembourgiaceae Numerous animals Wind MandrillsA Grey parrots Gorillasv Fleshy Winged Rodents RodentsH Insects Fleshy Fleshy Indo-Malayan Tropics Buchanania spp. Calophyllum spp. Anacardiaceae Guttiferae Canarium spp. Celtis spp. Dillenia spp. Burseraceae Ulmaceae Dilleniaceae Gonystylus bancanus Heritiera simplicifolia Intsia spp. Palaquium spp. Thymelaeaceae Animals Birdsq, orangutansF, gibbonsG, bats, squirrels, monkeys Birdsq, gibbonsI, sun bearsJ, monkeys, bats Birdsq, rodents OrangutansG, monkeys, elephants, pigs, squirrels, birds OrangutansF, Malayan flying foxesK, fruit bats Sterculiaceae Wind Beetles, moth larvae Leguminosae Sapotaceae Red leaf monkeysL, rodents Squirrels, other rodentsH, birds Pometia pinnata Pouteria spp. Syzygium spp. Sapindaceae Sapotaceae Myristicaceae Terminalia spp. Combretaceae Birdsq Birds, gibbonsI,M, orangutansF, civetsN, sun bearsO, fruit bats Bats, birds Monkeys, bats, birds, squirrels GibbonsI,M, hornbillsQ and other birds, civetsN, sun bearsO, small fruit bats, squirrels Birdsq, monkeysH RodentsH Fleshy Fleshy Fleshy Squirrels, other rodents Woody capsule Winged Deer, mouse deer, rats Insects Pod Fleshy Conopomorpha moths Squirrels, beetles RodentsH Insects Fleshy Fleshy Fleshy Rodents, insects Roesalia moth caterpillars Fleshy 158 C. Rosin / Forest Ecology and Management 331 (2014) 153–164 General sources: Pan-tropical: World Agroforestry Centre Database, PROTAbase, Jansen and Zuidema (2001); Neotropics: van Roosmalen (1985) and Hammond et al. (1996); Afrotropics: Doucet (2003); Indo-Malayan tropics: Soerianegara and Lemmens (1993), Lemmens et al. (1995) and Sosef et al. (1998). a Norconk and Veres (2011); b Lambert et al. (2005); c Terborgh et al. (1993); d Ribeiro et al. (1994); e Carvalho (1994); f Arnold and Fonseca (2011); g Embrapa Amazonia Oriental (2004); h Dick (2001); i Gayot et al. (2004); j Wenny (2000); k Howe et al. (1985); l Simmen and Sabatier (1996); m Henry et al. (2000); n Bodmer (1991); o van Roosmalen et al. (1988); p Altricher et al. (2001); q Snow (1981); r Forget (1989); s Hammond et al. (1999); t Beck (2005); u Sabater-Pí (1979); v Williamson et al. (1990); w Tutin and Fernandez (1993); x Beaune et al. (2012); y Astaras and Waltert (2010); z Hawthorne (1995); A Lahm (1986); B Morgan and Sanz (2007); C Doran et al. (2002); D Hall (2008); E Synnott (1975); F Galdikas (1988); G Ungar (1995); H Blate et al. (1998); I Marshall et al. (2009); J McConkey and Galetti (1999); K Hamzah et al. (2010); L Davies (1991); M Mumford (2009); N Mudappa et al. (2010); O Fredriksson et al. (2006); P Turner (1990); Q Kanwatanakid-Savini et al. (2009); R McKey et al. (1981); S Fragoso (1999). Levins, 1994; Keesing, 1998; Lambert et al., 2003; Laurance et al., 2006; Poulsen et al., 2011; Effiom et al., 2013). Logging itself modifies forest habitat in ways that additionally benefit small mammalian seed predators, such as opening canopy gaps (Struhsaker, 1997), and expanding road margins (Malcolm and Ray, 2000), increasing the density of vegetation through post-harvest regeneration. Overall these factors lead to increased rodent richness, diversity, and density in selectively logged forests (Isabirye-Basuta and Kasenene, 1987), and potentially more so in those subject to hunting pressure. Hunting may also indirectly benefit some invertebrate seed predators such as insects. Seeds that contain bruchid beetle larvae may be preferentially fed on by mammalian granivores (Silvius, 2002; Gálvez and Jansen, 2007). When hunting reduces populations of these mammals, larvae have a greater chance of surviving the seed stage to adulthood, increasing their abundance (Stoner et al., 2007). As a result, seed predation by insects dramatically increases with hunting pressure, at least on the several species of palm for which much data is available; two reviews have noted this increased predation, which ranges from 2- to 14-times higher (Kurten, 2013) and from 4- to 70-times higher (Stoner et al., 2007) in hunted vs. nonhunted sites. This change could have important consequences for timber trees, given the extent to which insects attack their seeds both pre- and post-dispersal, regardless of the dispersal mode. In Guyana, invertebrates heavily infest seed crops of the timber trees Peltogyne spp. and Aspidosperma spp. (ter Steege et al., 1996), and bruchid beetles destroyed nearly all undispersed H. courbaril seeds in one study (Hammond et al., 1992, see above). Weevils are a major predator of V. surinamensis in Panama (Howe et al., 1985), and can kill up to 90% of the seed crop of dominant dipterocarps in Malaysia (Toy, 1988). Due to differential hunting intensity and potential compensatory responses, the functional make-up of the seed predator guild may be expected to change dramatically under hunting pressure. Such shifts in faunal composition and abundance directly affect species-specific and community-wide seed predation and recruitment (DeSteven and Putz, 1984; Sork, 1987; Asquith et al., 1997; DeMattia et al., 2004; Hautier et al., 2010). Asquith et al. (1997) documented increased seed and seedling predation in forests under extreme mammal defaunation – those in which only small rodents remained of the original terrestrial mammalian granivore/herbivore community – compared to forests with a more complete fauna. Rodent density was negatively correlated with the overall density of tree seedlings in a logged Ugandan forest (Kasenene, 1980), and with the density of preferred small-seeded seedlings in a hunted Mexican forest (Dirzo et al., 2007). Increased rodent abundance may play an important role in reducing the regeneration of many timber trees (Kasenene, 1984; Struhsaker, 1997). Rodents are significant seed predators of mahogany (Aglaia sp.) in Malaysia (Becker and Wong, 1985), and true mahogany (Swietenia macrophylla) in Brazil (Grogan and Galvão, 2006; Norghauer et al., 2006). In Guyana, rodents attacked 43% of monitored seeds of the timber tree C. rodiei, as late as 566 days after implantation (Hammond et al., 1999). Abundant small rodents in hunted and logged Costa Rican forest sites removed significantly more seeds of three timber species (Dipteryx panamensis, Minquartia guianensis, and Virola koschnyi) than in a comparable site protected from hunting (Guariguata et al., 2000, 2002). In experimental plantings of the timber species Strombosia scheffleri in Uganda, 74.8% (n = 119) of seedlings died within 122 days, with 95.7% of mortality attributed to rodents (Lwanga, 1994). Synnott (1975) documented comparably extensive rodent predation of the timber tree Entandrophragma utile, and Hall (2008) encountered predation pressure so intense that rodents dug under or squeezed through holes in wire mesh exclosure cages to consume 100% of experimentally scattered Entandrophragma angolense seeds. It is clear that rodent predation on seeds can be a significant filter on timber tree recruitment, particularly given their increased abundance in hunted forests. The spatial aspects of seed deposition and granivore habitat preferences may also influence predation pressure on timber species. As small seed predators such as insects and rodents are generally more specialized and occupy smaller home ranges than large vertebrates, they may exert stronger Janzen–Connell type pressures (discussed above) on timber recruitment, increasing the value of seed dispersal away from parent trees. Rodents also favor the microhabitat conditions generated by young disturbed growth (Lambert and Adler, 2000), thus their seed and seedling predation can be higher in gaps than under closed canopy (Schupp, 1988; Schupp and Frost, 1989; Hammond et al., 1992). Wind-dispersed seeds – a common trait among currently harvested timber species – arrive more frequently in gaps than in the understory (Augspurger and Franson, 1988; Loiselle et al., 1996), so predation on these tree species may be especially high with increasing rodent abundance. While wind-dispersal may continue to be effective even in forests where large animal dispersers are absent (see above), increased rodent predation in gaps may depress overall recruitment. Evidence of this is limited, and merits further attention (see Future Research Priorities, below). Alteration of the granivore guild through hunting will variably release plant species from seed predation or impose greater mortality, depending on the seed species’ attractiveness to the remaining small fauna. In sum, due to the changes in seed predation intensity and selectivity of an altered granivore community, hunting may have strong indirect impacts on tree recruitment and timber regeneration dynamics. 4. Herbivory While the term ‘‘herbivory’’ sometimes encompasses both frugivory and granivory (discussed above), this section will focus on the consumption of leaf tissue; here, the term is used synonymously with folivory. Herbivores reduce leaf tissue and photosynthetic capacity, killing seedlings and harming or potentially killing saplings by uprooting and breaking stems. Herbivory is increasingly being recognized as an interaction which shapes tropical forest tree communities (Dirzo and Miranda, 1991; Marquis, 2005; Terborgh et al., 2006; Clark et al., 2012), and disruptions to this process may alter plant competitive interactions and impact timber tree recruitment. Tropical forest herbivores are abundant and highly diverse in character, from invertebrates to elephants. Given this diversity, the effects of hunting on the herbivore guild vary, mostly as a C. Rosin / Forest Ecology and Management 331 (2014) 153–164 result of differences in body size and hunter preference. The extreme size classes of herbivores generally escape hunting pressure (illegal poaching for secondary animal products, as with elephants, is an exception, eg. Maisels et al., 2013), while mid-sized herbivores are among the most heavily hunted vertebrates. Ungulate herbivores such as tapirs, deer, and bovids are highly desired game species (Redford and Robinson, 1987; Fa et al., 2005; Poulsen et al., 2009), and their populations can be severely reduced in hunted sites (Redford, 1992; Peres, 2000; Laurance et al., 2006; Corlett, 2007). The removal of terrestrial herbivores by hunting may have both direct and indirect consequences for timber tree recruitment. In general, diminished herbivory results in increased survival and densities of seedlings and saplings, but reduced diversity (Dirzo and Miranda, 1991; Terborgh and Wright, 1994; Bulinski and McArthur, 1999; Alves-Costa, 2004; Dyer et al., 2010; Harrison et al., 2013). In their pioneering study of a defaunated Mexican forest, Dirzo and Miranda (1991) observed dense seedling carpets and a complete absence of vertebrate herbivore leaf damage; lacking herbivores, the understory became an impoverished mosaic of virtual monocultures, dramatically altered in structure. How well timber species might fare in such an altered system is mostly unknown. In addition to consuming leaf tissues, terrestrial herbivores can physically damage plants through trampling, rooting, and digging. Seedling responses to this damage can differ among species (Clark and Clark, 1989), which may result in disproportionately increased survival of more vulnerable species when large animals are no longer abundant (Roldán and Simonetti, 2001). Both direct impacts of herbivores – consumption and physical damage – may thus differentially affect plant species, though again, their effects on timber tree performance are not well documented. The hunting of vertebrate herbivores may indirectly affect timber trees both by increasing invertebrate herbivory and by altering plant competitive interactions. As with small mammals (discussed above), insect herbivores can compensate with increased abundance when large vertebrates are extirpated (Dirzo, 2001). Insects exert strong and specialized herbivore pressures (Coley and Barone, 1996; Massey et al., 2005) and are widely regarded as significant timber pests (Gray, 1972; Nair, 2007). Hunting may thus indirectly lead to added timber losses by prompting increased insect herbivory, though evidence is extremely limited. Hunting may also indirectly modify plant competitive interactions. Herbivory is by definition a net loss for plants, regardless of the herbivore involved. However, these losses may be unevenly distributed across the plant community, particularly when hunting alters herbivore pressures. Plant species that are less often consumed by remaining herbivores as well as those that invest little in anti-herbivore defense may realize a new competitive advantage within the plant community. Designating resources toward the production of plant defense compounds can promote increased seedling survival (Molofsky and Fisher, 1993), but involves a trade-off with investment in growth (Coley et al., 1985). Fast growing, competitively dominant species thus typically suffer high rates of herbivory in intact forests because of the palatability of their tissues (Coley and Barone, 1996), though this regulatory pressure is lost in the absence of herbivores. In an exclosure experiment by Kurten (2010), herbivore removal indeed favored less defended, higher leaf nutrient species. Seedlings which more quickly exhaust their reserves through fast growth also have less of a chance to be damaged by rodents (Forget, 1997). In a community-level study, Poulsen et al. (2013) documented the proliferation of fast growing, low wood density species in forests subject to hunting pressure. By way of explaining this trend, the authors’ forest herbivore hypothesis implicates the relaxation of browsing by hunted mammals as the key mechanism of change. 159 Overall, current evidence suggests that hunting will favor plant species with fast growth, disadvantaging well-defended, high wood density species at the community level. This poses a concern for the regeneration of many timber species in hunted forests. Through its direct and indirect impacts on herbivory, hunting may alter the ‘‘competitive balance’’ between plant species (Wright, 2003), to the detriment of timber regeneration. 5. Conclusions Hunting can affect regeneration through a variety of pathways (Fig. 1). Vertebrate seed dispersers are strongly impacted by hunting pressure, reducing seed movement for many species and shifting community composition to favor those plants dispersed by small animals and abiotic means. Timber species with large seeds and fleshy fruit are at particular risk for dispersal and recruitment failure. Hunting also alters granivore communities, resulting in increased predation on species favored by insects and small rodents, and changing the spatial template of seed predation. There is abundant evidence to suggest that many timber species will be detrimentally affected by such altered seed predation regimes. Large vertebrate herbivores decline with hunting pressure, resulting in the modification of plant competitive interactions. This process disadvantages several traits that are common among timber trees, including relatively slow growth and high wood density. Timber species, like the broader tropical tree community, interact with wildlife through all stages of their life cycles. One cannot assume that regeneration will be successful in the face of hunting, when plant-animal interactions are so widely modified. A lack of appreciation for – and management of – these interactions could threaten forest biodiversity, limit future timber production, and increase the likelihood of forest conversion for other land uses. 5.1. Management considerations Hunting will no doubt continue to affect tropical forests worldwide, though there is great potential to curtail its effects in production forests, through improved management. Many natural management systems rely on unlogged concession lands both to preserve biodiversity and to promote recovery after harvesting from adjacent forest units. However, unlogged tracts may be too small to maintain viable animal populations and too isolated to allow re-colonization of logged areas (Pannell, 1989). Forest managers expecting sustained timber production must thus ensure that the processes that contribute to regeneration occur within logged areas themselves (Guariguata and Pinard, 1998). This is only possible if wildlife populations are maintained and the impacts of hunting are reduced across concessions. The most effective management modifications to reduce hunting in concessions are those which reduce market demand for wild meat and curb the transportation of hunters and their game (Auzel and Wilkie, 2000; Clark et al., 2009). One way to curtail access would be to ban the transport of hunters and game meat on logging trucks, enforced with road blocks and spot checks, and to close or destroy unused bridges and roads post-logging (Auzel and Wilkie, 2000). Removing the transportation infrastructure that hunters rely on can be a very successful intervention, as evidenced by the collapse of bushmeat markets and closure of local hunting camps that followed a brief halt in traffic of a large Congo concession (Pearce and Ammann, 1995). Demand for wild meat can only be reduced if alternatives are available at equal or lesser prices, perhaps subsidized by the logging companies themselves. This could be achieved by importing domestic animal meat, or by establishing livestock-raising programs within concessions (Auzel and Wilkie, 2000). Poulsen et al. (2009) outline several additional recommendations to reduce 160 C. Rosin / Forest Ecology and Management 331 (2014) 153–164 hunting within concessions, including: concession support for wildlife law enforcement, ensuring that any workers who hunt do so legally, formalizing resource management in land-use planning, especially for indigenous people, and avoiding urbanization in concessions. Such management requirements may seem extensive, but are not beyond the capacity of most extractive enterprises. In the Congolaise Industrielle des Bois (CIB) concessions in the Republic of Congo, wildlife and biodiversity are specifically managed through a combination of land-use planning, hunting law enforcement, developing economic and protein alternatives to hunting and wild meat, and formalizing wildlife management (Poulsen and Clark, 2010; Clark and Poulsen, 2012). Gabon’s Rabi concession, though focused on oil rather than timber, is another exemplary case. The concession prohibits nighttime driving, restricts access for nonemployees, and forbids the possession of firearms, snares, and bushmeat (Laurance et al., 2006). Workers are well compensated financially and domestic animal meat is made available at competitive prices (Laurance et al., 2006). Similarly, logging companies in Sarawak are tasked with enforcing a wildlife trade ban in rural areas and providing meat for workers, and forestry laws in Bolivia mandate comparable practices (Robinson et al., 1999). The options open to forest managers are typically influenced by short-term financial and political priorities, often resulting in the dismissal of plant-animal interactions and the long-term consequences of disruptions to them (Smith and Garnett, 2004). However, these financial constraints are precisely why managers must strive to make informed decisions that promote efficient and cost-effective practices (Green, 2007). For example, protecting native seed dispersers can be much less expensive than artificially recreating lost dispersal services (Hougner et al., 2006). Management schemes and certification bodies such as the Forest Stewardship Council (FSC) should strive to be as specific as possible regarding wildlife and ecological services; this process has benefitted in recent years from biologists becoming more involved in setting guidelines (Bennett, 2001). Revised FSC principles and criteria now include mention of hunting and ecosystem function (FSC, 2012), but the language remains non-specific and non-prescriptive. Additionally, there is currently little information on whether certification and improved practices actually reduce the pressures on wildlife associated with timber harvest (Kuijk et al., 2009), despite this being a stated goal of such management. Ultimately, appropriate management decisions will come about only by recognizing the direct and indirect impacts the timber industry has on wildlife (Robinson et al., 1999; Poulsen et al., 2009). Few have acknowledged that wildlife management is a vital component of forest management (Smythe, 1987; Pannell, 1989; Terborgh, 1995; Corlett, 2011), though it is in many companies’ best interests to do so, as such explicit consideration would benefit both biodiversity and timber regeneration. 5.2. Future research priorities Knowledge of the ecological requirements and reproductive biology of most tropical timber species is sorely lacking (Bawa et al., 1990; Pinard et al., 1999). Though there is sufficient evidence to conclude that animals play many important roles (see Tables 1 and 2), few forestry studies directly address these relationships. The information presented here is far from exhaustive; these interactions are scattered few and far between in primary literature and natural history accounts, and very little is known on any generalizable scale. In particular, the impacts of potentially disruptive activities such as hunting must be documented and communicated well, so that governments, certifying bodies, and timber companies themselves can make informed management decisions. Fig. 1. Conceptual model of pathways by which hunting may affect the regeneration of timber; adapted with permission from Poulsen et al. (2013). Hypothesized effects on timber regeneration are presented by subscripts: green (+) effects are beneficial, red (!) effects are detrimental, and blue ( ) effects are variable, depending on specific plant traits. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) C. Rosin / Forest Ecology and Management 331 (2014) 153–164 One research priority is to obtain basic ecological data for timber trees and for hunted wildlife species, including their distribution, density, and rates of change under hunting (Milner-Gulland et al., 2003), particularly for animals that may play a role in timber regeneration. Such information is critically important for identifying important functional traits, as well as thresholds in plant-animal relationships beyond which wildlife are no longer ecologically effective in their roles (McConkey and Drake, 2006), or compensatory increases become deleterious to regeneration processes (see above). Specific studies addressing the dispersal, predation, or overall recruitment of timber trees with relation to wildlife are needed. Responses to hunting among wildlife and plant communities are not unidirectional; it is clear that disruptions to plant-animal interactions can vary in their downstream effects, promoting or inhibiting recruitment depending on several factors. Reconciling the sometimes contradictory outcomes of these processes will require manipulative field experiments. Regardless of the focal theme, researchers must strive to promote access to ecological knowledge among the international forestry community, and to improve its translation into tangible management action (Sheil and Van Heist, 2000). The most effective research to promote change and mitigate deleterious impacts on wildlife will be that which addresses silviculturally and financially viable alternatives to exploitative practices (Putz et al., 2001). Without such efforts, timber operations and the bodies that oversee them will be unable to make the important decisions that will define the future of tropical forestry. Forest wildlife and the ecological processes that influence regeneration can be of great importance for many timber species, and the effects of impacts such as hunting must be well understood in order to maintain them. The sustainability of logging from both an ecological and economic perspective will rely on careful management with a strong scientific foundation. Acknowledgements I thank John Poulsen for his insight and extensive comments on the manuscript. Feedback from two anonymous reviewers also substantially improved the quality of the final article. References Abernethy, K., Coad, L., Taylor, G., Lee, M.E., Maisels, F., 2013. Extent and ecological consequences of hunting in Central African rainforests in the twenty-first century. Philos. Trans. Roy. Soc. B 368, 1625. Adler, G.H., 1995. Fruit and seed exploitation by Central American spiny rats, Proechimys semispinosus. Stud. Neotrop. Fauna Environ. 30, 237–244. Adler, G.H., Levins, R., 1994. The island syndrome in rodent populations. Quart. Rev. Biol. 69, 473–490. Altricher, M., Carrillo, E., Saenz, J., Fuller, T., 2001. White-lipped peccary (Tayassu pecari, Artiodactyla: Tayassuidae) diet and fruit availability in a Costa Rican rain forest. Rev. Biol. Trop. 49, 1183–1192. Alves-Costa, C., 2004. Efeitos da defaunação de mamíferos herbívoros na comunidade vegetal. Universidade Estadual de Campinas. Appanah, S., Putz, F., 1984. Climber abundance in virgin dipterocarp forest and the effect of pre-felling climber cutting on logging damage. Malaysian Forester 47, 335–342. Arnold, J.P., Fonseca, C.R., 2011. Herbivory, pathogens, and epiphylls in Araucaria Forest and ecologically-managed tree monocultures. For. Ecol. Manage. 262, 1041–1046. Asquith, N.M., Wright, S.J., Clauss, M.J., 1997. Does mammal community composition control recruitment in neotropical forests? Evidence from Panama. Ecology 78, 941–946. Asquith, N., Terborgh, J., Arnold, A., Mailén Riveros, C., 1999. The fruits the agouti ate: hymenaea courbaril seed fate when its disperser is absent. J. Trop. Ecol. 15, 229–235. Astaras, C., Waltert, M., 2010. What does seed handling by the drill tell us about the ecological services of terrestrial cercopithecines in African forests? Anim. Conserv. 13, 568–578. Augspurger, C.C.K., Franson, S.S.E., 1988. Input of wind-dispersed seeds into lightgaps and forest sites in a Neotropical forest. J. Trop. Ecol. 4, 239–252. Auzel, P., Wilkie, D., 2000. Wildlife use in Northern Congo: hunting in a commercial logging concession. In: Robinson, J.G., Bennett, E.L. (Eds.), Hunting for 161 Sustainability in Tropical Forests. Columbia University Press, New York, NY, pp. 413–426. Bakuneeta, C., Johnson, K., Plumptre, R., Reynolds, V., 1995. Human uses of tree species whose seeds are dispersed by chimpanzees in the Budongo Forest, Uganda. Afr. J. Ecol. 33, 276–278. Baur, G., 1964. The Ecological Basis of Rainforest Management. Forestry Commission of NSW, Sydney. Bawa, K., Seidler, R., 1998. Natural forest management and conservation of biodiversity in tropical forests. Conserv. Biol. 12, 46–55. Bawa, K., Ashton, P., Nor, S., 1990. Reproductive ecology of tropical forest plants: management issues. In: Bawa, K., Hadley, M. (Eds.), Reproductive Ecology of Tropical Forest Plants. UNESCO, pp. 1–13. Beaune, D., Bollache, L., Fruth, B., Bretagnolle, F., 2012. Bush pig (Potamochoerus porcus) seed predation of bush mango (Irvingia gabonensis) and other plant species in Democratic Republic of Congo. Afr. J. Ecol. 50, 509–512. Beaune, D., Bretagnolle, F., Bollache, L., Hohmann, G., Surbeck, M., Fruth, B., 2013. Seed dispersal strategies and the threat of defaunation in a Congo forest. Biodivers. Conserv. 22, 225–238. Beck, H., 2005. Seed predation and dispersal by peccaries throughout the Neotropics and its consequences: a review and synthesis. In: Forget, P.-M., Lambert, J., Hulme, P., Vander Wall, S. (Eds.), Seed Fate: Predation, Dispersal and Seedling Establishment. CAB International, Wallingford, UK, pp. 77–115. Becker, P., Wong, M., 1985. Seed dispersal, seed predation, and juvenile mortality of Aglaia sp. (Meliaceae) in lowland dipterocarp rainforest. Biotropica 17, 230– 237. Bennett, E., 2001. Timber certification: where is the voice of the biologist? Conserv. Biol. 14, 921–923. Berry, N.J., Phillips, O.L., Lewis, S.L., Hill, J.K., Edwards, D.P., Tawatao, N.B., Ahmad, N., Magintan, D., Khen, C.V., Maryati, M., Ong, R.C., Hamer, K.C., 2010. The high value of logged tropical forests: lessons from northern Borneo. Biodivers. Conserv. 19, 985–997. Blaser, J., Sarre, A., Poore, D., Johnson, S., 2011. Status of Tropical Forest Management 2011. International Tropical Timber Organization. Blate, G.M., Peart, D.R.D., Leighton, M., 1998. Post-dispersal predation on isolated seeds: a comparative study of 40 tree species in a Southeast Asian rainforest. Oikos 82, 522–538. Bodmer, R., 1991. Strategies of seed dispersal and seed predation in Amazonian ungulates. Biotropica 23, 255–261. Brodie, J., Gibbs, H., 2009. Bushmeat hunting as climate threat. Science 326, 364–365. Bulinski, J., McArthur, C., 1999. An experimental field study of the effects of mammalian herbivore damage on Eucalyptus nitens seedlings. For. Ecol. Manage. 113, 241–249. Buschbacher, R., 1990. Natural forest management in the humid tropics: ecological, social, and economic considerations. Ambio (Sweden) 19, 253–258. Carvalho, P., 1994. Espécies florestais brasileiras: recomendações silviculturais, potencialidades e uso da madeira. EMBRAPA-CNPF, Colombo. Clark, D., Clark, D., 1989. The role of physical damage in the seedling mortality regime of a neotropical rain forest. Oikos 55, 225–230. Clark, D., Clark, D., 1990. Distribution and effects on tree growth of lianas and woody hemiepiphytes in a Costa Rican tropical wet forest. J. Trop. Ecol. 6, 321–331. Clark, C., Poulsen, J.R., 2012. Tropical Forest Conservation & Industry Partnership: An Experience from the Congo Basin. Wiley-Blackwell. Clark, C.J., Poulsen, J.R., Malonga, R., Elkan, P.W., 2009. Logging concessions can extend the conservation estate for Central African tropical forests. Conserv. Biol. 23, 1281–1293. Clark, C.J., Poulsen, J.R., Levey, D.J., 2012. Vertebrate herbivory impacts seedling recruitment more than niche partitioning or density-dependent mortality. Ecology 93, 554–564. Clayton, L., Keeling, M., Milner-Gulland, E., 1997. Bringing home the bacon: a spatial model of wild pig hunting in Sulawesi, Indonesia. Ecol. Appl. 7, 642–652. Coley, P., Barone, J., 1996. Herbivory and plant defenses in tropical forests. Annu. Rev. Ecol. Syst. 27, 305–335. Coley, P., Bryant, J., Chapin III, F.S., 1985. Resource availability and plant antiherbivore defense. Science 230, 895–899. Connell, J.H., 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: den Boer, P.J., Gradwell, G.R. (Eds.), Dynamics of Populations. Centre for Agricultural Publications and Documentation, Wageningen, The Netherlands, p. 312. Corlett, R.T., 1998. Frugivory and seed dispersal by vertebrates in the Oriental (Indomalayan) Region. Biol. Rev. Camb. Philos. Soc. 73, 413–448. Corlett, R.T., 2007. The impact of hunting on the mammalian fauna of tropical Asian forests. Biotropica 39, 292–303. Corlett, R.T., 2011. The importance of animals in the forest. In: Wickneswari, R., Cannon, C. (Eds.), Managing the Future of Southeast Asia’s Valuable Tropical Rainforests, vol. 2. Advances in Asian Human-Environmental Research, pp. 83–92. Crawley, M.J., 1992. Seed predators and plant population dynamics. In: Fenner, M. (Ed.), Seeds: The Ecology of Regeneration in Plant Communities. CAB International, Wallingford, UK, pp. 157–191. Curran, L., Webb, C., 2000. Experimental tests of the spatiotemporal scale of seed predation in mast-fruiting Dipterocarpaceae. Ecol. Monogr. 70, 129–148. Davies, G., 1991. Seed-eating by red leaf monkeys (Presbytis rubicunda) in dipterocarp forest of northern Borneo. Int. J. Primatol. 12. DeMattia, E.A., Curran, L.M., Rathcke, B.J., Biology, E., Arbor, A., 2004. Effects of small rodents and large mammals on Neotropical seeds. Ecology 85, 2161–2170. DeSteven, D., Putz, F., 1984. Impact of mammals on early recruitment of a tropical canopy tree, Dipteryx panamensis, in Panama. Oikos 43, 207–216. 162 C. Rosin / Forest Ecology and Management 331 (2014) 153–164 Dick, C., 2001. Habitat change, African honeybees and fecundity in the Amazonian tree Dinizia excelsa (Fabaceae). In: Bierregaard, R., Gascon, C., Lovejoy, T., Mesquita, R. (Eds.), Lessons from Amazonia: the Ecology and Conservation of a Fragmented Forest. Yale University Press, New Haven, pp. 146–157. Dirzo, R., 2001. Plant-mammal interactions: lessons for our understanding of nature, and implications for biodiversity conservation. In: Press, M., Huntly, N., Levin, S. (Eds.), Ecology: Achievement and Challenge: the 41st Symposium of the British Ecological Society. Blackwell Science. Dirzo, R., Miranda, A., 1991. Altered patterns of herbivory and diversity in the forest understory: a case study of the possible consequences of contemporary defaunation. In: Price, P., Lewinsohn, T., Fernandes, G., Benson, W. (Eds.), Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions. John Wiley & Sons Inc., pp. 273–287. Dirzo, R., Mendoza, E., Ortíz, P., 2007. Size-related differential seed predation in a heavily defaunated neotropical rain forest. Biotropica 39, 355–362. Doran, D.M., McNeilage, A., Greer, D., Bocian, C., Mehlman, P., Shah, N., 2002. Western lowland gorilla diet and resource availability: new evidence, cross-site comparisons, and reflections on indirect sampling methods. Am. J. Primatol. 58, 91–116. Doucet, J.-L., 2003. L’alliance délicate de la gestion forestière et de la biodiversité dans les forêts du centre du Gabon. Doctoral Dissertation. Dyer, L.A., Letourneau, D.K., Chavarria, G.V., Amoretti, D.S., 2010. Herbivores on a dominant understory shrub increase local plant diversity in rain forest communities. Ecology 91, 3707–3718. Effiom, E., Nuñez-Iturri, G., Smith, H.G., Ottosson, U., Olsson, O., 2013. Bushmeat hunting changes regeneration of African rainforests. Proc. Roy. Soc. B 280. Embrapa. Am azonia. Oriental. 2004. Especies arboreas da Amazonia no. 6: Angelim-vermelho, Dinizia excelsa. Belem, PA, 6p. Fa, J.E., Peres, C.A., Meeuwig, J., 2002. Bushmeat exploitation in tropical forests: an intercontinental comparison. Conserv. Biol. 16, 232–237. Fa, J.E., Ryan, S.F., Bell, D.J., 2005. Hunting vulnerability, ecological characteristics and harvest rates of bushmeat species in Afrotropical forests. Biol. Conserv. 121, 167–176. Feer, F., 1995. Seed dispersal in African forest ruminants. J. Trop. Ecol. 11, 683–689. Fimbel, R., Grajal, A., Robinson, J. (Eds.), 2001. The Cutting Edge: Conserving Wildlife in Logged Tropical Forests. Columbia University Press, New York. Fleming, T., 1975. The role of small mammals in tropical ecosystems. In: Golley, F., Petrusewicz, K., Ryszkowski, L. (Eds.), Small Mammals: Their Productivity & Population Dynamics. Cambridge University Press, 268–198. Forget, P., 1989. La régénération naturelle d’une espèce autochore de la forêt guyanaise: Eperua falcata Aublet (Caesalpiniaceae). Biotropica 21, 115–125. Forget, P., 1990. Seed-dispersal of Vouacapoua americana (Caesalpiniaceae) by caviomorph rodents in French Guiana. J. Trop. Ecol. 6, 459–468. Forget, P.-M., 1997. Effect of microhabitat on seed fate and seedling performance in two rodent-dispersed tree species in rain forest in French Guiana. J. Ecol. 85, 693–703. Fox, J., 1968. Logging damage and the influence of climber cutting prior to logging in the lowland dipterocarp forest of Sabah. Malaysian Forester 31, 326–347. Fragoso, J.M.V., 1999. Perception of scale and resource partitioning by peccaries: behavioral causes and ecological implications. J. Mammol. 80 (3), 993–1003. Fredericksen, T.S., Mostacedo, B., 2000. Regeneration of timber species following selection logging in a Bolivian tropical dry forest. For. Ecol. Manage. 131, 47–55. Fredriksson, G., Wich, S., Trisno, 2006. Frugivory in sun bears (Helarctos malayanus) is linked to El Niño-related fluctuations in fruiting phenology, East Kalimantan, Indonesia. Biol. J. Linn. Soc. 89, 489–508. FSC, 2012. FSC Principles and Criteria for Forest Stewardship. Forest Stewardship Council. Galdikas, B., 1988. Orangutan diet, range, and activity at Tanjung Puting, Central Borneo. Int. J. Primatol. 9. Gálvez, D., Jansen, P.A., 2007. Bruchid beetle infestation and the value of Attalea butyracea endocarps for neotropical rodents. J. Trop. Ecol. 23, 381. Gautier-Hion, A., Duplantier, J., Quris, R., 1985. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia, 324–337. Gayot, M., Henry, O., Dubost, G., Sabatier, D., 2004. Comparative diet of the two forest cervids of the genus Mazama in French Guiana. J. Trop. Ecol. 20, 31–43. Ghiglieri, M., Butynski, T., Struhsaker, T., Leland, L., Wallis, S., Waser, P., 1982. Bush pig (Potamochoerus porcus) polychromatism and ecology in Kibale Forest, Uganda. Afr. J. Ecol. 20. Glanz, W.E., 1991. Mammalian densities at protected versus hunted sites in central Panama. In: Robinson, J.G., Redford, K.H. (Eds.), Neotropical Wildlife Use and Conservation. The University of Chicago Press, pp. 163–173. Goméz-Pompa, A., Burley, F., 1991. The management of natural tropical forests. In: Goméz-Pompa, A., Whitmore, T., Hadley, M. (Eds.), Rain Forest Regeneration and Management. UNESCO, Paris, France, pp. 3–18. Grauel, W.T., Putz, F.E., 2004. Effects of lianas on growth and regeneration of Prioria copaifera in Darien, Panama. For. Ecol. Manage. 190, 99–108. Gray, B., 1972. Economic tropical forest entomology. Annu. Rev. Entomol. 17, 313– 352. Green, R., 2007. Refining the conservation management of seed-dispersing frugivores and their fruits: examples from Australia. In: Dennis, A., Schupp, E., Green, R., Westcott, D. (Eds.), Seed Dispersal: Theory and its Application in a Changing World. CAB International, Wallingford, UK, pp. 579–598. Grogan, J., Galvão, J., 2006. Factors limiting post-logging seedling regeneration by big-leaf mahogany (Swietenia macrophylla) in southeastern Amazonia, Brazil, and implications for sustainable management. Biotropica 38, 219–228. Guariguata, M.R., Pinard, M.A., 1998. Ecological knowledge of regeneration from seed in Neotropical forest trees: implications for natural forest management. For. Ecol. Manage. 112, 87–99. Guariguata, M.R., Adame, J.J.R., Finegan, B., 2000. Seed removal and fate in two selectively logged lowland forests with constrasting protection levels. Conserv. Biol. 14, 1046–1054. Guariguata, M., Claire, H., Jones, G., 2002. Tree seed fate in a logged and fragmented forest landscape, northeastern Costa Rica. Biotropica 34, 405–415. Hall, J.S., 2008. Seed and seedling survival of African mahogany (Entandrophragma spp.) in the Central African Republic: implications for forest management. For. Ecol. Manage. 255, 292–299. Hallwachs, W., 1986. Agoutis (Dasyprocta punctata): the inheritors of guapinol (Hymenaea courbaril: Leguminosae). In: Estrada, A., Fleming, T. (Eds.), Frugivores and Seed Dispersal. Springer, Dordrecht, Netherlands, pp. 285–304. Hammond, D.S.D., Brown, V., 1998. Disturbance, phenology and life-history characteristics: factors influencing distance/density-dependent attack on tropical seeds and seedlings. In: Newbery, D., Prins, H., Brown, N. (Eds.), Dynamics of Tropical Communities. Blackwell Science, Inc., Malden, MA. Hammond, D., Schouten, A., van Tienen, L., Weijerman, M., Brown, V., 1992. The importance of being a forest animal: implications for Guyana’s timber trees. In: Annual Review of Conference Proceedings, Tropenbos Guyana. Hammond, D.S., Gourlet-Fleury, S., van der Hout, P., ter Steege, H., Brown, V., 1996. A compilation of known Guianan timber trees and the significance of their dispersal mode, seed size and taxonomic affinity to tropical rain forest management. For. Ecol. Manage. 83, 99–116. Hammond, D., Brown, V., Zagt, R., 1999. Spatial and temporal patterns of seed attack and germination in a large-seeded neotropical tree species. Oecologia 119, 208– 218. Hamzah, K., Parlan, I., Sulaiman, A., Faidi, M., Yong, H., Kamarazaman, I., 2010. Gonystylus Bancanus: Jewel of the Peat Swamp Forest. Forest Research Institute Malaysia. Happold, D.C.D., 1995. The interactions between humans and mammals in Africa in relation to conservation: a review. Biodivers. Conserv. 4, 395–414. Harrison, R.D., Tan, S., Plotkin, J.B., Slik, F., Detto, M., Brenes, T., Itoh, A., Davies, S.J., 2013. Consequences of defaunation for a tropical tree community. Ecol. Lett. 16, 687–694. Hautier, Y., Saner, P., Philipson, C., Bagchi, R., Ong, R.C., Hector, A., 2010. Effects of seed predators of different body size on seed mortality in Bornean logged forest. PLoS ONE 5, e11651. Hawthorne, W., 1995. Ecological Profiles of Ghanaian Forest Trees. Oxford Forestry Institute. Henry, O., Feer, F., Sabatier, D., 2000. Diet of the Lowland Tapir (Tapirus terrestris L.) in French Guiana1. Biotropica 32, 364–368. Hougner, C., Colding, J., Söderqvist, T., 2006. Economic valuation of a seed dispersal service in the Stockholm National Urban Park, Sweden. Ecol. Econ. 59, 364–367. Howe, H., 1977. Bird activity and seed dispersal of a tropical wet forest tree. Ecology 58, 539–550. Howe, H., Miriti, M., 2000. No question: seed dispersal matters. Trends Ecol. Evol. 15, 434–436. Howe, H.F., Smallwood, J., 1982. Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13, 201–228. Howe, H., Schupp, E., Westley, L., 1985. Early consequences of seed dispersal for a neotropical tree (Virola surinamensis). Ecology 66, 781–791. Hulme, P., 1993. Post-dispersal seed predation by small mammals. Symp. Zool. Soc. Lond. 65, 269–287. Hulme, P., 1998. Post-dispersal seed predation: consequences for plant demography and evolution. Perspect. Plant Ecol., Evol. Syst. 1, 32–46. Hulme, P., 2002. Seed-eaters: seed dispersal, destruction and demography. In: Levey, D., Silva, W., Galetti, M. (Eds.), Seed Dispersal and Frugivory: Ecology, Evolution and Conservation. CABI Publishing, New York, pp. 257–273. Ickes, K., Dewalt, S.J., Appanah, S., 2001. Effects of native pigs (Sus scrofa) on woody understorey vegetation in a Malaysian lowland rain forest. J. Trop. Ecol. 17, 191–206. Isabirye-Basuta, G., Kasenene, J., 1987. Small rodent populations in selectively felled and mature tracts of Kibale Forest, Uganda. Biotropica 19, 260–266. ITTO, 2012. Annual Review and Assessment of the World Timber Situation. International Tropical Timber Organization. Jansen, P.A., Forget, P.-M., 2001. Scatterhoarding rodents and tree regeneration. In: Bongers, F., Charles-Dominique, P., Forget, P.-M., Thery, M. (Eds.), Nouragues: Dynamics and Plant-Animal Interactions in a Neotropical Rainforest. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 275–288. Jansen, P.A., Zuidema, P., 2001. Logging, seed dispersal by vertebrates, and natural regeneration of tropical timber trees. In: Fimbel, R., Grajal, A., Robinson, J. (Eds.), The Cutting Edge: Conserving Wildlife in Logged Tropical Forests. Columbia University Press, New York, NY, pp. 35–59. Jansen, P., Muller-Landau, H., Wright, S., 2010. Bushmeat hunting and climate: an indirect link. Science 327, 30. Janzen, D.H., 1970. Herbivores and the number of tree species in tropical forests. Am. Nat. 104, 501–528. Janzen, D.H., 1971. Seed predation by animals. Annu. Rev. Ecol. Syst. 2, 465–492. Janzen, D., Vázquez-Yanes, C., 1991. Aspects of tropical seed ecology of relevance to management of tropical forested wildlands. In: Gómez-Pompa, A., Whitmore, T., Hadley, M. (Eds.), Rain Forest Regeneration and Management. UNESCO, Paris, France, pp. 137–158. Johns, A.D., 1985. Selective logging and wildlife conservation in tropical rain-forest: problems and recommendations. Biol. Conserv. 31, 355–375. C. Rosin / Forest Ecology and Management 331 (2014) 153–164 Johns, A.D., 1988. Effects of ‘‘selective’’ timber extraction on rain forest structure and composition and some consequences for frugivores and folivores. Biotropica 20, 31–37. Johns, A.D., 1997. Timber Production and Biodiversity Conservation in Tropical Rainforests. Cambridge University Press, Cambridge, UK. Johns, J.S., Barreto, P., Uhl, C., 1996. Logging damage during planned and unplanned logging operations in the eastern Amazon. For. Ecol. Manage. 89, 59–77. Kanwatanakid-Savini, C., Poonswad, P., Savini, T., 2009. An assessment of food overlap between gibbons and hornbills. Raffles Bull. Zool. 57, 189–198. Kasenene, J., 1980. Plant Regeneration and Rodent Populations in Selectively Felled and Unfelled Areas of the Kibale Forest, Uganda. Makerere University, Kampala, Uganda. Kasenene, J., 1984. The influence of selective logging on rodent populations and the regeneration of selected tree species in the Kibale Forest, Uganda. Trop. Ecol. 25, 179–195. Keesing, F., 1998. Impacts of ungulates on the demography and diversity of small mammals in central Kenya. Oecologia 116, 381–389. Knogge, C., Heymann, E.W., 2003. Seed dispersal by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis: diversity and characteristics of plant species. Folia Primatol. 74, 33–47. Kuijk, M. Van, Putz, F.E., Zagt, R., 2009. Effects of Forest Certification on Biodiversity. Tropenbos International, Wageningen, the Netherlands. Kuprewicz, E.K., 2012. Mammal abundances and seed traits control the seed dispersal and predation roles of terrestrial mammals in a Costa Rican forest. Biotropica 45, 333–342. Kurten, E., 2010. Functional Trait Mediation of Plant-Animal Interactions: Effects of Defaunation on Plant Functional Diversity in a Neotropical Forest. Stanford University. Kurten, E.L., 2013. Cascading effects of contemporaneous defaunation on tropical forest communities. Biol. Conserv. 163, 22–32. Lahm, S., 1986. Diet and habitat preference of Mandrillus sphinx in Gabon: implications of foraging strategy. Am. J. Primatol. 26, 9–26. Lambert, T.D., Adler, G.H., 2000. Microhabitat use by a tropical forest rodent, Proechimys semispinosus, in Central Panama. J. Mammal. 81, 70–76. Lambert, T.D., Adler, G.H., Riveros, C.M., Lopez, L., Ascanio, R., Terborgh, J., 2003. Rodents on tropical landbridge islands. J. Zool. 260, 179–187. Lambert, T.D., Malcolm, J.R., Zimmerman, B.L., 2005. Effects of mahogany (Swietenia macrophylla) logging on small mammal communities, habitat structure, and seed predation in the southeastern Amazon Basin. For. Ecol. Manage. 206, 381–398. Laurance, W.F., Croes, B.M., Tchignoumba, L., Lahm, S.A., Alonso, A., Lee, M.E., Campbell, P., Ondzeano, C., 2006. Impacts of roads and hunting on Central African rainforest mammals. Conserv. Biol. 20, 1251–1261. Lemmens, R., Soerianegara, I., Wong, W. (Eds.), 1995. Plant Resources of South-East Asia No 5(2): Timber Trees: Minor Commercial Timbers. Backhuys Publishers, Leiden. Levi, T., Peres, C.A., 2013. Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree. Biol. Conserv. 163, 99–106. Loiselle, B.A.B., Ribbens, E., Vargas, O., 1996. Spatial and temporal variation of seed rain in a tropical lowland wet forest. Biotropica 28, 82–95. Lwanga, J.J.S., 1994. The Role of Seed and Seedling Predators and Browsers in the Regeneration of Two Forest Canopy Species (Mimusops bagshawei and Strombosia scheffleri) in Kibale Forest Reserve. University of Florida, Gainesville, Uganda. Maisels, F., Strindberg, S., Blake, S., Wittemyer, G., Hart, J., Williamson, E.a, Abaa, R., Abitsi, G., Ambahe, R.D., Amsini, F., Bakabana, P.C., Hicks, T.C., Bayogo, R.E., Bechem, M., Beyers, R.L., Bezangoye, A.N., Boundja, P., Bout, N., Akou, M.E., Bene, L.B., Fosso, B., Greengrass, E., Grossmann, F., Ikamba-Nkulu, C., Ilambu, O., Inogwabini, B.-I., Iyenguet, F., Kiminou, F., Kokangoye, M., Kujirakwinja, D., Latour, S., Liengola, I., Mackaya, Q., Madidi, J., Madzoke, B., Makoumbou, C., Malanda, G.-A., Malonga, R., Mbani, O., Mbendzo, V.a, Ambassa, E., Ekinde, A., Mihindou, Y., Morgan, B.J., Motsaba, P., Moukala, G., Mounguengui, A., Mowawa, B.S., Ndzai, C., Nixon, S., Nkumu, P., Nzolani, F., Pintea, L., Plumptre, A., Rainey, H., de Semboli, B.B., Serckx, A., Stokes, E., Turkalo, A., Vanleeuwe, H., Vosper, A., Warren, Y., 2013. Devastating decline of forest elephants in central Africa. PloS one 8, e59469. Malcolm, J.R., Ray, J.C., 2000. Influence of timber extraction routes on Central African small-mammal communities, forest structure, and tree diversity. Conserv. Biol. 14, 1623–1638. Marquis, R., 2005. Impacts of herbivores on tropical plant diversity. In: Burslem, D., Pinard, M., Hartley, S. (Eds.), Biotic Interactions in the Tropics: Their Role in the Maintenance of Species Diversity. Cambridge University Press. Marshall, A.J., Cannon, C.H., Leighton, M., 2009. Competition and niche overlap between gibbons (Hylobates albibarbis) and other frugivorous vertebrates in Gunung Palung National Park, West Kalimantan, Indonesia. In: Whittaker, D., Lappan, S. (Eds.), The Gibbons: New Perspectives on Small Ape Socioecology and Population Biology. Springer, New York, New York, NY, pp. 161–188. Massey, F., Press, M., Hartley, S., 2005. Have the impacts of insect herbivores on the growth of tropical tree seedlings been underestimated. In: Burslem, D., Pinard, M., Hartley, S. (Eds.), Biotic Interactions in the Tropics: Their Role in the Maintenance of Species Diversity. Cambridge University Press, pp. 347– 365. Mbelli, H., 2002. Plant-Animal Relations: Effects of Disturbance on the Regeneration of Commercial Tree Species. The Tropenbos-Cameroon Programme, Kribi, Cameroon. McConkey, K.R., Drake, D.R., 2006. Flying foxes cease to function as seed dispersers long before they become rare. Ecology 87, 271–276. 163 McConkey, K., Galetti, M., 1999. Seed dispersal by the sun bear Helarctos malayanus in Central Borneo. J. Trop. Ecol. 15, 237–241. McKey, D., Gartlan, J., Waterman, P., FLS, Choo, G., 1981. Food selection by black colobus monkeys (Colobus satanas) in relation to plant chemistry. Biol. J. Linn. Soc. 16, 115–146. Meijaard, E., Sheil, D., Nasi, R., Augeri, D., Rosenbaum, B., Iskandar, D., Setyawati, T., Lammertink, M., Rachmatika, I., Wong, A., Soehartono, T., Stanley, S., O’Brien, T., 2005. Life After Logging: Reconciling Wildlife Conservation and Production Forestry in Indonesian Borneo. CIFOR and UNESCO. Mendoza, E., Dirzo, R., 2007. Seed-size variation determines interspecific differential predation by mammals in a Neotropical rain forest. Oikos 116, 1841–1852. Milner-Gulland, E.J., Bennett, E.L., S. 2002 A. M. W. M. Group, 2003. Wild meat: the bigger picture. Trends Ecol. Evol. 18, pp. 351–357. Molofsky, J., Fisher, B., 1993. Habitat and predation effects on seedling survival and growth in shade-tolerant tropical trees. Ecology 74, 261–265. Morgan, D., Sanz, C., 2007. Best Practice Guidelines for Reducing the Impact of Commercial Logging on Great Apes in Western Equatorial Africa. IUCN, Gland, Switzerland. Mudappa, D., Kumar, A., Chellam, R., 2010. Diet and fruit choice of the brown palm civet Paradoxurus jerdoni, a viverrid endemic to the Western Ghats rainforest, India. Trop. Conserv. Sci. 3, 282–300. Muller-Landau, H., Hardesty, B., 2005. Seed dispersal of woody plants in tropical forests: concepts, examples and future directions. In: Pinard, B.D.M., Hartley, S. (Eds.), Biotic Interactions in the Tropics: Their Role in Species Diversity. Cambridge University Press, Cambrindge UK, pp. 267–309. Mumford, A., 2009. A Preliminary Assessment of Seed Dispersal by Two Ape Species in the Sabangau. University of Oxford. Nabe-Nielsen, J., Kollmann, J., Peña-Claros, M., 2009. Effects of liana load, tree diameter and distances between conspecifics on seed production in tropical timber trees. For. Ecol. Manage. 257, 987–993. Nair, K., 2007. Tropical Forest Insect Pests: Ecology, Impact, and Management. Cambridge University Press. Norconk, M.a, Veres, M., 2011. Physical properties of fruit and seeds ingested by primate seed predators with emphasis on sakis and bearded sakis. Anat. Rec. 294, 2092–2111. Norghauer, J.M., Malcolm, J.R., Zimmerman, B.L., Felfili, J.M., 2006. An experimental test of density- and distant-dependent recruitment of mahogany (Swietenia macrophylla) in southeastern Amazonia. Oecologia 148, 437–446. Notman, E., Villegas, A., 2005. Patterns of seed predation by vertebrate versus invertebrate seed predators among different plant species, seasons, and spatial distributions. In: Forget, P.-M., Lambert, J., Hulme, P., Vander Wall, S. (Eds.), Seed Fate: Predation, Dispersal and Seedling Establishment. CABI Publishing, Cambridge, MA, pp. 55–76. Nuñez-Iturri, G., Olsson, O., Howe, H.F., 2008. Hunting reduces recruitment of primate-dispersed trees in Amazonian Peru. Biol. Conserv. 141, 1536–1546. Paine, C.E.T., Beck, H., 2007. Seed predation by Neotropical rain forest mammals increases diversity in seedling recruitment. Ecology 88, 3076–3087. Pannell, C., 1989. The role of animals in natural regeneration and the management of equatorial rain forests for conservation and timber production. Commonw. Forest. Rev. 68, 309–313. Pearce, J., Ammann, K., 1995. Slaughter of the Apes: How the Tropical Timber Industry is Devouring Africa’s Great Apes. World Society for the Protection of Animals, London. Peres, C.A., 2000. Effects of subsistence hunting on vertebrate community structure in Amazonian forests. Conserv. Biol. 14, 240–253. Peres, C.A., Dolman, P.M., 2000. Density compensation in Neotropical primate communities: evidence from 56 hunted and nonhunted Amazonian forests of varying productivity. Oecologia 122, 175–189. Peres, C.A., Palacios, E., 2007. Basin-wide effects of game harvest on vertebrate population densities in Amazonian forests: implications for animal-mediated seed dispersal. Biotropica 39, 304–315. Peres, C.A., Van Roosmalen, M., 2002. Primate frugivory in two species-rich Neotropical forests: implications for the demography of large-seeded plants in overhunted areas. In: Levey, D.J., Silva, W., Galetti, M. (Eds.), Seed Dispersal and Frugivory: Ecology, Evolution and conservation. CABI International, Oxford, UK, pp. 407–421. Phillips, O., 1997. The changing ecology of tropical forests. Biodivers. Conserv. 6, 291–311. Pinard, M.A., Putz, F.E., Rumiz, D., Guzman, R., Jardim, A., 1999. Ecological characterization of tree species for guiding forest management decisions in seasonally dry forests in Lomerı´o, Bolivia. For. Ecol. Manage. 113, 201–213. Plumptre, A., Reynolds, V., Bakuneeta, C., 1994. The Contribution of Fruit Eating Primates to Seed Dispersal and Natural Regeneration after Selective Logging. ODA Project, Report, R4738. Poulsen, J.R., Clark, C.J., 2010. Congo basin timber certification and biodiversity conservation. In: Sheil, D., Putz, F., Zagt, R. (Eds.), Biodiversity Conservation in Certified Forests. Tropenbos International, Wageningen, the Netherlands, pp. 55–60. Poulsen, J.R., Clark, C.J., Connor, E.F., Smith, T.B., 2002. Differential resource use by primates and hornbills: implications for seed dispersal. Ecology 83, 228–240. Poulsen, J.R., Clark, C.J., Mavah, G., Elkan, P.W., 2009. Bushmeat supply and consumption in a tropical logging concession in northern Congo. Conserv. Biol. 23, 1597–1608. Poulsen, J.R., Clark, C.J., Bolker, B.M., 2011. Decoupling the effects of logging and hunting on an Afrotropical animal community. Ecol. Appl. 21, 1819–1836. 164 C. Rosin / Forest Ecology and Management 331 (2014) 153–164 Poulsen, J.R., Clark, C.J., Palmer, T., 2013. Ecological erosion of an Afrotropical forest and potential consequences for tree recruitment and forest biomass. Biol. Conserv. 163, 122–130. Putz, F.E., 1982. Natural History of Lianas and their Influences on Tropical Forest Dynamics. Cornell University, New York. Putz, F.E., 1991. Silvicultural effects of lianas. In: Putz, F.E., Mooney, H.A. (Eds.), The Biology of Vines. Cambridge University Press. Putz, F.E., Redford, K., Robinson, J., Fimbel, R., Blate, G.M., 2000. Biodiversity Conservation in the Context of Tropical Forest Management. The World Bank. Putz, F.E., Sirot, L.K., Pinard, M.A., 2001. Tropical forest management and wildlife: silvicultural effects on forest structure, fruit production, and locomotion of arboreal animals. In: Fimbel, R., Grajal, A., Robinson, J. (Eds.), The Cutting Edge: Conserving Wildlife in Logged Tropical Forests. Columbia University Press, New York, NY, pp. 11–34. Putz, F.E., Zuidema, P.A., Synnott, T., Peña-Claros, M., Pinard, M.A., Sheil, D., Vanclay, J.K., Sist, P., Gourlet-Fleury, S., Griscom, B., Palmer, J., Zagt, R., 2012. Sustaining conservation values in selectively logged tropical forests: the attained and the attainable. Conserv. Lett. 5, 296–303. Rao, M., Myint, T., Zaw, T., Htun, S., 2005. Hunting patterns in tropical forests adjoining the Hkakaborazi National Park, north Myanmar. Oryx 39, 292–300. Redford, K., 1992. The empty forest. Bioscience 42, 412–422. Redford, K., Feinsinger, P., 2001. The half-empty forest: sustainable use and the ecology of interactions. In: Reynolds, J.D., Mace, G.M., Redford, K.H., Robinson, J.G. (Eds.), Conservation of Exploited Species. Cambridge University Press, Cambridge, UK, pp. 370–400. Redford, K., Robinson, J., 1987. The game of choice: patterns of Indian and colonist hunting in the Neotropics. Am. Anthropol. 89, 650–667. Reynolds, V., 2005. The Chimpanzees of the Budongo Forest: Ecology, Behaviour, and Conservation. Oxford University Press, New York. Ribeiro, S., Pimenta, H., Fernandes, G., 1994. Herbivory by chewing and sucking insects on Tabebuia ochracea. Biotropica 26, 302–307. Rice, R., Gullison, R., Reid, J., 1997. Can sustainable management save tropical forests? Sci. Am. Robinson, J.G., Bennett, E.L., 2000. Hunting for Sustainability in Tropical Forests. Columbia University Press. Robinson, J., Redford, K., Bennett, E., 1999. Wildlife harvest in logged tropical forests. Science 284, 595–596. Roldán, A., Simonetti, J.A., 2001. Plant-mammal interactions in tropical Bolivian forests with different hunting pressures. Conserv. Biol. 15, 617–623. Rosin, C., Swamy, V., 2013. Variable density responses of primate communities to hunting pressure in a western Amazonian river basin. Neotrop. Primates 20, 25– 31. Sabater-Pí, J., 1979. Feeding behaviour and diet of chimpanzees (Pan troglodytes troglodytes) in the Okorobiko Mountains of Rio Muni (West Africa). Zeitschrift fuer Tierpsychologie 50, 265–281. Schnitzer, S.A., Dalling, J.W., Carson, W.P., 2000. The impact of lianas on tree regeneration in tropical forest canopy gaps: evidence for an alternative pathway of gap-phase regeneration. J. Ecol. 88, 655–666. Schupp, E., 1988. Seed and early seedling predation in the forest understory and in treefall gaps. Oikos 51, 71–78. Schupp, E., 1993. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107, 15–29. Schupp, E., Frost, E., 1989. Differential predation of Welfia georgii seeds in treefall gaps and the forest understory. Biotropica 21, 200–203. Sheil, D., Van Heist, M., 2000. Ecology for tropical forest management. Int. Forest. Rev. 2, 261–270. Silman, M., Terborgh, J., Kiltie, R., 2003. Population regulation of a dominant rain forest tree by a major seed predator. Ecology 84, 431–438. Silvius, K.M., 2002. Spatio-temporal patterns of palm endocarp use by three Amazonian forest mammals: granivory or ‘‘grubivory’’? J. Trop. Ecol. 18, 707–723. Simmen, B., Sabatier, D., 1996. Diets of some French Guianan primates: food composition and food choices. Int. J. Primatol. 17. Smith, K., Garnett, S., 2004. Animal-plant interactions: a rainforest conservation manager’s perspective. In: Kanowski, J., Catterall, C., Dennis, A., Westcott, D. (Eds.), Animal-Plant Interactions in Conservation and Restoration: Workshop Proceedings. Cooperative Research Centre for Tropical Rainforest Ecology and Management, Rainforest RCR., Cairns, Australia, pp. 17–19. Smythe, N., 1986. Competition and resource partitioning in the guild of neotropical terrestrial frugivorous mammals. Annu. Rev. Ecol. Syst. 17, 169–188. Smythe, N., 1987. The importance of mammals in Neotropical forest management. In: Figueroa Colon, J., Wadsworth, F., Branham, S. (Eds.), Management of the Forests of Tropical America: Prospects and Technologies. Institute of Tropical Forestry, pp. 79–98. Snow, D., 1981. Tropical frugivorous birds and their food plants: a world survey. Biotropica 13, 1–14. Soerianegara, I., Lemmens, R. (Eds.), 1993. Plant Resources of South-East Asia No 5(1): Timber Trees: Major Commercial Timbers. Pudoc Scientific Publishers, Wageningen. Sork, V., 1987. Effects of predation and light on seedling establishment in Gustavia superba. Ecology 68, 1341–1350. Sosef, M., Hong, L., Prawirohatmodjo, S. (Eds.), 1998. Plant Resources of South-East Asia No 5(3): Timber Trees: Lesser Known Timbers. Backhuys Publishers, Leiden. Stevens, G., 1987. Lianas as structural parasites: the Bursera simaruba example. Ecology 68, 77–81. Stoner, K.E., Vulinec, K., Wright, S.J., Peres, C.A., 2007. Hunting and plant community dynamics in tropical forests: a synthesis and future directions. Biotropica 39, 385–392. Struhsaker, T., 1997. Ecology of an African Rain Forest. University Press of Florida, Gainesville, FL. Synnott, T., 1975. Factors Affecting the Regeneration and Growth of Seedlings of Entandrophragma utile (Dawe and Sprague) in Budongo Forest and Nyabyeya Nursery-Uganda. Makerere University, Kampala, Uganda. Ter Steege, H., Boot, R.G.A., Brouwer, L.C., Caesar, J.C., Ek, R.C., Hammond, D.S., Haripersaud, P.P., van der Hout, P., Jetten, V.G., van Kekem, A.J., Kellman, M.A., Khan, Z., Polak, A.M., Pons, T.L., Pulles, J., Raaimakers, D., Rose, S.A., van der Sanden, J.J., Zagt, R.J., 1996. Ecology and Logging in a Tropical Rain Forest in Guyana, with Recommendations for Forest Management. The Tropenbos Foundation, Wageningen, The Netherlands. Terborgh, J., 1995. Wildlife in managed tropical forests: a Neotropical perspective. In: Lugo, A., Lowe, C. (Eds.), Tropical Forests: Management and Ecology. Springer-Verlag, New York. Terborgh, J., 2012. Enemies maintain hyperdiverse tropical forests. Am. Nat. 179, 303–314. Terborgh, J., 2013. Using Janzen–Connell to predict the consequences of defaunation and other disturbances of tropical forests. Biol. Conserv. 163, 7–12. Terborgh, J., Nuñez-Iturri, G., 2006. Disperser-free tropical forests await an unhappy fate. In: Laurance, W., Peres, C. (Eds.), Emerging Threats to Tropical Forests. The University of Chicago Press, Chicago, pp. 241–252. Terborgh, J., Wright, S.J., 1994. Effects of mammalian herbivores on plant recruitment in two Neotropical forests. Ecology 75, 1829–1833. Terborgh, J., Losos, E., Riley, M., Riley, M., 1993. Predation by vertebrates and invertebrates on the seeds of five canopy tree species of an Amazonian forest. Vegetatio 107, 375–386. Terborgh, J., Feeley, K.J., Silman, M., Nuñez, P., Balukjian, B., 2006. Vegetation dynamics of predator-free land-bridge islands. J. Ecol. 94, 253–263. Terborgh, J., Nuñez-Iturri, G., Pitman, N.C.A., Valverde, F.H.C., Alvarez, P., Swamy, V., Pringle, E.G., Paine, C.E.T., Nuñez-Iturri, G., 2008. Tree recruitment in an empty forest. Ecology 89, 1757–1768. Toy, R., 1988. The Pre-Dispersal Insect Fruit-Predators of Dipterocarpaceae in Malaysian Rain Forest. University of Aberdeen. Traveset, A., 1998. Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspect. Plant Ecol., Evol. Syst. 1, 151–190. Traveset, A., Verdu, M., 2002. A meta-analysis of the effect of gut treatment on seed germination. In: Levey, D., Silva, W., Galetti, M. (Eds.), Seed Dispersal and Frugivory: Ecology, Evolution and Conservation. CABI Publishing, New York. Turner, I., 1990. The seedling survivorship and growth of three Shorea species in a Malaysian tropical rain forest. J. Trop. Ecol. 6, 469–478. Tutin, C.E.G., Fernandez, M., 1993. Composition of the diet of chimpanzees and comparisons with that of sympatric lowland gorillas in the lopé reserve, gabon. Am. J. Primatol. 30, 195–211. Tutin, C., Williamson, E., Rogers, M., Fernandez, M., 1991. A case study of a plantanimal relationship: Cola lizae and lowland gorillas in the Lope Reserve, Gabon. J. Trop. Ecol. 7, 181–199. Ungar, P.S., 1995. Fruit preferences of four sympatric primate species at Ketambe, northern Sumatra, Indonesia. Int. J. Primatol. 16, 221–245. Van Roosmalen, M., 1985. Fruits of the Guianan Flora. Utrecht University, Wageningen, Netherlands. Van Roosmalen, M., Mittermeier, R., Fleagle, J., 1988. Diet of the northern bearded saki (Chiropotes satanas chiropotes): a neotropical seed predator. Am. J. Primatol. 14, 11–35. Van Vliet, N., Nasi, R., 2008. Mammal distribution in a Central African logging concession area. Biodivers. Conserv. 17, 1241–1249. Vanthomme, H., Bellé, B., Forget, P.-M., 2010. Bushmeat hunting alters recruitment of large-seeded plant species in Central Africa. Biotropica 42, 672–679. Vieira, E.M., Pizo, M.A., Izar, P., 2003. Fruit and seed exploitation by small rodents of the Brazilian Atlantic forest. Mammalia 67, 533–540. Weetman, G., Vyse, A., 1990. Natural regeneration. In: Parish, R., Lavendar, D., Johnson, C., Montgomery, G., Vyse, A., Willis, R., Winston, D. (Eds.), Regenerating British Columbia’s Forests. UBC Press, Vancouver, BC, pp. 118–129. Wenny, D., 2000. Seed dispersal, seed predation, and seedling recruitment of a neotropical montane tree. Ecol. Monogr. 70, 331–351. Wilkie, D., Shaw, E., Rotberg, F., Morelli, G., Auzel, P., 2000. Roads, development, and conservation in the Congo Basin. Conserv. Biol. 14, 1614–1622. Williamson, E.A., Tutin, C.E.G., Rogers, M.E., Fernandez, M., 1990. Composition of the diet of lowland gorillas at Lope in Gabon. Am. J. Primatol. 21, 265–277. Willson, M., Traveset, A., 2000. The ecology of seed dispersal. In: Fenner, M. (Ed.), Seeds: The Ecology of Regeneration in Plant Communities. CABI Publishing, New York, pp. 85–110. Willson, M., Irvine, A., Walsh, N., 1989. Vertebrate dispersal syndromes in some Australian and New Zealand plant communities, with geographic comparisons. Biotropica 21, 133–147. Wright, S.J., 2003. The myriad consequences of hunting for vertebrates and plants in tropical forests. Perspect. Plant Ecol., Evol. Syst. 6, 73–86. Wright, S.J., Hernandéz, A., Condit, R., 2007. The bushmeat harvest alters seedling banks by favoring lianas, large seeds, and seeds dispersed by bats, birds, and wind. Biotropica 39, 363–371.

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