Diaspore traits

Diaspore traits most obviously affecting seed-dispersal ecology include seed or fruit size (variously recorded as length, diameter and/or mass), fruit type (e.g. hard, fleshy, dehiscent) and seed-dispersal mode (e.g. zoochory, anemochory, barochory) (Howe & Smallwood Reference HOWE and SMALLWOOD1982). To investigate trends in these traits with increasing altitude we compiled data comprising diaspore traits for 867 tree species along five montane tropical forest altitudinal gradients over 17 sites in Thailand, the Philippines, Tanzania, Malawi and Nigeria (Figure 2). These data were sourced from the published literature, online databases including Kew Seed Information Database, Africa Tree Database and JSTOR Global Plants, as well as unpublished data from author contributions (Table 1).

Figure 2. Map showing general location of the five montane tropical forest altitudinal gradients in Malawi, Nigeria, the Philippines, Tanzania and Thailand.

A lack of data across all diaspore traits and the inconsistent way in which traits have been recorded across studies necessitated a simplified analytical approach. As more data were available on fruits than seeds for most species, we used fruit as analogous to diaspore, given that in many cases it is the fruit that is transported by dispersal agents. Among the fruit traits we evaluated – fruit size (length and diameter), fruit type and dispersal mode – fruit size was analysed as continuous, while fruit type and dispersal mode were converted into ordinal factors as follows: (1) fruit type was an ordinal factor where 0 = dry fruits and 1 = fleshy fruits; and (2) dispersal mode was treated as 0 = abiotically dispersed species and 1 = animal-dispersed species. From the latter, higher values of community weighted means (CWM) for these three fruit traits represent larger, animal-dispersed, fleshy fruits.

To determine the relationship between fruit traits and altitude we used ‘species per site’ and ‘trait per species’ matrices to calculate CWM for each study site, using the ‘matrix.t’ procedure in the ‘SYNCSA’ package for R software. We then checked for collinearity among trait CWM using the function ‘corrplot’ from the R package ‘corrplot’.

Our analysis of five altitudinal gradients found that altitude accounted for 30% of the variation in fruit length, and 20% of the variation in fruit diameter. Fruit length was significant, indicating a decrease in diaspore size with increasing altitude (F_1,15 = 7.87; P = 0.013; adjusted R² = 0.30; Figure 3a). Although other traits related to diaspore size tended to decrease with altitude, the relationship was weak (F_1,15 = 3.81; P = 0.07; adjusted R² = 0.14; Figure 3b). A community-wide decrease in diaspore size (both fruit and seed) with increasing altitude in tropical forests is well documented, especially in the Neotropics (Figure 1 and references therein). Species with small fleshy fruits are the norm at higher altitudes and are common at lower altitudes, while species with large fleshy fruits tend to be absent at high altitudes (Almeida-Neto et al. Reference ALMEIDA-NETO, CAMPASSI, GALETTI, JORDANO and OLIVEIRA-FILHO2008, Duivenvoorden et al. Reference DUIVENVOORDEN and CUELLO2012, Friis Reference FRIIS1992).

Figure 3. Regression analysis of community weighted means (CWM) for (a) fruit length (cm) and (b) fruit diameter against altitude (m asl) from 867 tree species along five tropical forest altitudinal gradients in Malawi, (M), Nigeria (N), the Philippines (Ph), Tanzania (Tz) and Thailand (Th). M.1 – 1250 m asl, M.2 – 1830 m asl, M.3 – 1980 m asl, M.4 – 2075 m asl, N.1 – 230 m asl, N.2 – 230 m asl, N.3 – 1500 m asl, N.4 – 1830 m asl, N.5 – 2090 m asl, Ph.1 – 1000 m asl, Ph.2 – 1450 m asl, Tz.1 – 240 m asl, Tz.2 – 1025 m asl, Th.1 – 700 m asl, Th.2 – 795 m asl, Th.3 – 1100 m asl, Th.4 – 1700 m asl. These data were sourced from the published literature, online databases including Kew Seed Information Database, Africa Tree Database and JSTOR Global Plants, as well as unpublished data from author contributions.

For those species for which seed-length data were available, we evaluated seed length across the altitudinal gradients; we grouped the sites into three altitudinal zones, 0–1000 m asl, 1100–1500 m asl and 1600–2100 m asl. Seed length (log-transformed) at the community level also declined with increasing altitude (ANOVA F_2,920 = 4.53, P = 0.011), and sites in the two higher altitudinal zones had smaller seeds on average (Mean ± SD; 1100–1500 m = 10.7 ± 11.1 mm; 1600–2100 m = 10.9 ± 11.8 mm; both P < 0.05) than the lowland zone (0–1000 m = 13.0 ± 12.9 mm); seeds from the two higher zones did not differ (P > 0.05). Including sites from higher altitudes (>2500 m), and from a wider geographic area is needed to verify the consistency of this trend in seed size with altitude.

Why does community-wide diaspore size decrease with increasing altitude in tropical forests and to what extent is this trend driven by abiotic or biotic factors? Almedia-Neto et al. (Reference ALMEIDA-NETO, CAMPASSI, GALETTI, JORDANO and OLIVEIRA-FILHO2008) point out that this is a difficult question to answer because seed size is positively correlated with other plant traits such as tree height and leaf size, that are more obviously affected by environmental factors (Wright et al. Reference WRIGHT, ACKERLY, BONGERS, HARMS, IBARRA-MANRIQUEZ, MARTINEZ-RAMOS, MAZER, MULLER-LANDAU, PAZ, PITMAN, POORTER, SILMAN, VRIESENDORP, WEBB, WESTOBY and WRIGHT2007). As tree height in TMF decreases with altitude (Figure 1) so does seed size, commensurate with a described allometric relationship between tree size and fruit size (Grubb Reference GRUBB1998). Likewise leaf size decreases with altitude and the allometric relationship between leaf size and inflorescence size is such that seed size also is predicted to decrease (Midgley & Bond Reference MIDGLEY and BOND1989). Small seed size disadvantages seedlings growing in shady habitats as it provides lower initial energy reserves needed to tolerate shade for longer and to grow faster to access as much light as possible (Leishman & Westoby Reference LEISHMAN and WESTOBY1994). The small seed size in TMFs may be partly due to low levels of available soil nitrogen (Fahey et al. Reference FAHEY, SHERMAN and TANNER2016). While larger seeds should theoretically be at an advantage in nutrient-poor soils (Moles & Westoby Reference MOLES and WESTOBY2004), large seeds require more nutrients to produce than small seeds, and at altitude where these nutrients are limited and trees consequently have relatively small stature, selection for less costly, abundant small seeds may enhance recruitment in TMF. At lower elevations there is selection pressure for large seeds because of higher metabolic costs associated with establishment (Lord et al. Reference LORD, EGAN, CLIFFORD, JURADO, LEISHMAN, WILLIAMS and WESTOBY1997). Numerous small seeds may ensure pioneer species are more competitive in montane forests through greater broadcast dispersal of seeds into gaps and forest edges (Dalling & Hubbell Reference DALLING and HUBBELL2002), especially in Afromontane forests where climatic fluctuations have led to continual recolonization (Grimshaw Reference GRIMSHAW, Huxley, Lock and Cutler1998).

Frugivores may exert selection pressure on fruit size or vice versa where fruit size may determine the structure of the frugivore guild. The direction of selection is difficult to elicit in this instance. Correa et al. (Reference CORREA, ÁLVAREZ and STEVENSON2015), Jordano (Reference JORDANO1995), Lambert & Garber (Reference LAMBERT and GARBER1998) and Lord et al. (Reference LORD, EGAN, CLIFFORD, JURADO, LEISHMAN, WILLIAMS and WESTOBY1997) all argue that frugivores select for diaspore size because gape width and body size limit the size of fruit that a frugivore can swallow (Moermond & Denslow Reference MOERMOND and DENSLOW1985, Wheelwright Reference WHEELWRIGHT1985). Mashers, birds that mandibulate fruits to drop seeds and ingest only fruit pulp or juice (Levey Reference LEVEY, Estrada and Fleming1986), strongly select for small seed size by virtue of their seed treatment, and are common in Neotropical montane forests (Moermond & Denslow Reference MOERMOND and DENSLOW1985). The general trend in TMF is that frugivore body size decreases with increasing altitude (Figures 1, 4, 5). Figure 4 illustrates how body mass of frugivorous birds tends to decrease at higher altitudes (ANOVA F _2,1185 = 3.5, P = 0.03). Specifically, birds from lower altitudes (< 1000 m) were larger on average than those from middle altitudes (1000–2000 m; Tukey HSD, P = 0.033); body mass of birds from higher altitudes (>2000 m) did not differ from those at middle and lower elevations (Ps > 0.05).

Figure 4. Body mass (n = 1206), log transformed, of frugivorous birds from lower (< 1000 m), middle (1000–2000 m) and upper (>2000 m) altitudinal ranges. Data from Handbook of the birds of the world (HBW 1992–2013).

Figure 5. Body mass (g) (n = 1206) of fruit-eating birds at the community level at three altitudinal ranges: lower (< 1000 m asl), middle (1000–2000 m asl) and upper (>2000 m asl) in five different regions: Australasia, Africa, Indomalaya, Neotropics and Oceanica. Data from Handbook of the birds of the world (HBW 1992–2013).

A decrease in bird body size is generally associated with smaller gape size (Wheelwright Reference WHEELWRIGHT1985), and this body size–gape size trend was confirmed in TMF (Wenny et al. Reference WENNY, SEKERCIOGLU, CORDEIRO, ROGERS, KELLY, Sekercioglu, Wenny and Whelan2016). However, a comparison of frugivorous birds' body mass across Australia, Africa, Indonesia, the Neotropics and Oceania illustrated that the extent of the general trend toward smaller body size at higher altitudes differs among regions (ANOVA F _4,1181 = 9.2, P < 0.001). Specifically, birds from Africa were smaller on average than those from Australasia (Tukey HSD, P = 0.011), and birds from the Neotropics were smaller on average than those from Australasia (P < 0.001) and Indomalaya (P < 0.009). Avian body mass did not differ significantly for the other possible pairwise comparisons among geographic regions (Ps > 0.05).

Where large-seeded species persist at relatively high altitudes in TMF, they are likely to have specialized and coevolved dispersal syndromes. For example, in high montane forest in the Drakensberg of South Africa the large seeds of Calodendrum capensis may be dispersed by bats and the large Rameron pigeon (Columba arquatrix; Coates Palgrave Reference COATES PALGRAVE2003). Similarly, in Nigerian and Tanzanian TMF, large-seeded tree species such as Carapa and Allanblackia, respectively, have nuts that are eaten and dispersed by Cricetomys rodents (Aliyu et al. Reference ALIYU, ADAMU, MOLTCHANOVA, FORGET and CHAPMAN2014, Seltzer et al. Reference SELTZER, KREMER, NDANGALASI and CORDEIRO2015). In general, however, large-bodied frugivores in TMF are rare and therefore the exception that proves the rule that frugivore size likely selects for small seed size in TMF.

Another well-documented trend is an increase in the relative proportion of anemochorous species with altitude (Figure 1). For example, Grubb & Stevens (Reference GRUBB and STEVENS1985) found that anemochorous species in New Guinea forests increased from 7% (lower montane) to 13% (upper montane) to 20% (subalpine). Vázquez & Givnish (Reference VÁZQUEZ-G. and GIVNISH1998) report similar increases from 1500–2500 m asl in Mexico, and Tanner (Reference TANNER1982) reported a higher proportion of anemochorous diaspores in montane versus lowland forest in Jamaica. Friis (Reference FRIIS1992), found evidence for increased anemochorous tree species with altitude in Ethiopian forests, but not as strongly as the broader taxonomic studies.

The increasing proportion of anemochorous species along altitudinal gradients in tropical montane forests may in part be a phylogenetic constraint (Jordano Reference JORDANO1995); temperate floristic elements have a higher representation in TMF than in TLFs, and many of these are herbaceous or shrubby and anemochorous (Buitrón-Jurado & Ramírez Reference BUITRÓN-JURADO and RAMÍREZ2014, Gentry Reference GENTRY, Bullock, Mooney and Medina1995, White Reference WHITE1983). Vascular epiphytes, many of which, but by no means all, are orchids with tiny seeds, increase in abundance with altitude in cloud forests (Grubb Reference GRUBB1977, Murray et al. Reference MURRAY, KINSMAN, BRONSTEIN, Nadkarni and Wheelwright2000, Vázquez & Givnish Reference VÁZQUEZ-G. and GIVNISH1998). However, it is a reasonable assumption that this may also reflect adaptation to windier conditions in TMF. Buitrón-Jurado & Ramírez (Reference BUITRÓN-JURADO and RAMÍREZ2014) tested for phylogenetic independence of anemochory, and concluded that the greater phylogenetic overdispersion in upper relative to lower montane forests in the Andes was evidence for anemochory being adaptive at higher altitudes.

In our analyses CWM fruit type changed with increasing altitude with fleshy fruit species increasing relative to non-fleshy species (F_1,15 = 2.64, P = 0.125, Figure 6). A similar trend is observed in South-East Asia where anemochorous/barochorous dipterocarp species decrease in frequency with increasing altitude and are ‘replaced’ by ornithochorous Lauraceae (Padmawathe et al. Reference PADMAWATHE, QURESHI and RAWAT2004). This suggests that the increase in anemochory reported above is not universal, or that it is more obvious at the upper elevational limits of TMF (above ~ 2200 m asl) or under different biogeographic pressures.

Figure 6. Regression analysis of community weighted means (CWM) for fruit type (dry fruits = 0, fleshy fruits =1) against altitude (m asl) from 867 tree species along five tropical forest altitudinal gradients in Malawi (M), Nigeria (N), the Philippines (Ph), Tanzania (Tz) and Thailand (Th). M.1 – 1250 m asl, M.2 – 1830 m asl, M.3 – 1980 m asl, M.4 – 2075 m asl, N.1 – 230 m asl, N.2 – 230 m asl, N.3 – 1500 m asl, N.4 – 1830 m asl, N.5 – 2090 m asl, Ph.1 – 1000 m asl, Ph.2 – 1450 m asl, Tz.1 – 240 m asl, Tz.2 – 1025 m asl, Th.1 – 700 m asl, Th.2 – 795 m asl, Th.3 – 1100 m asl, Th.4 – 1700 m asl. These data were sourced from the published literature, online databases including Kew Seed Information Database, Africa Tree Database and JSTOR Global Plants, as well as unpublished data from author contributions.

Faunal composition

Faunal assemblage structure and body size change along altitudinal gradients in response to reduced ecosystem productivity – diets become less diverse and of lower quality and quantity (Figure 1), and the relative abundance and diversity of small and large mammals (Heaney et al. Reference HEANEY, HEIDEMAN, RICKART, UTZURRUM and KLOMPEN1989, Ingle Reference INGLE2003, Steinmetz et al. Reference STEINMETZ, CHUTIPONG, SEUATURIEN and CHIRNGSAARD2008) and birds (Dehling et al. Reference DEHLING, FRITZ, TÖPFER, PÄCKERT, ESTLER, BÖHNING-GAESE and SCHLEUNING2014, Ferger et al. Reference FERGER, SCHLEUNING, HEMP, HOWELL and BÖHNING-GAESE2014, Terborgh Reference TERBORGH1977) shifts towards smaller-bodied species (Rodríguez et al. Reference RODRÍGUEZ, OLALLA-TÁRRAGA and HAWKINS2008). Large-mammal assemblages are less species rich and have lower densities with increasing altitude. Elephants and tapirs drop out of TMF with altitude (Steinmetz et al. Reference STEINMETZ, CHUTIPONG, SEUATURIEN and CHIRNGSAARD2008), there are fewer primate species at upper elevations in African (Goodman & Rasolonandrasana Reference GOODMAN and RASOLONANDRASANA2001, Marshall et al. Reference MARSHALL, TOPP-JØRGENSEN, BRINK and FANNING2005), Asian (Caldecott Reference CALDECOTT1980, Grow et al. Reference GROW, GURSKY and DUMA2013) and South American TMF (Almeida-Neto et al. Reference ALMEIDA-NETO, CAMPASSI, GALETTI, JORDANO and OLIVEIRA-FILHO2008, Geise et al. Reference GEISE, PEREIRA, BOSSI and BERGALLO2004, Shanee Reference SHANEE2009, Reference SHANEE, Defler and Stevenson2014), and fewer fruit bats in TMF in the Philippines (Hamann & Curio Reference HAMANN and CURIO1999), Peruvian Andes (Patterson et al. Reference PATTERSON, PACHECO and SOLARI1996) and oceanic Africa (Goodman & Rasolonandrasana Reference GOODMAN and RASOLONANDRASANA2001). Primates (Grow et al. Reference GROW, GURSKY and DUMA2013), fruit bats and birds (Figure 4) are all generally smaller bodied at high altitudes. Rodents also decline in species richness with increasing altitude, with major changes occurring at ecotones between lowland and montane forest (Willig & Presley Reference WILLIG and PRESLEY2016). However, small-mammal densities tend to peak everywhere in mid-elevation forest (Heaney Reference HEANEY2001, McCain Reference MCCAIN2004, Moreira et al. Reference MOREIRA, MANDUCA, GONÇALVES, MORAIS, PEREIRA, LESSA and DERGAM2009), the mid-domain effect (Colwell & Lees Reference COLWELL and LEES2000). In addition, at higher altitudes primate species switch diets from a predominantly fruit diet to a more mixed diet (Fourrier Reference FOURRIER2013, Gross-Camp et al. Reference GROSS-CAMP, MASOZERA and KAPLIN2009, Ramírez et al. Reference RAMÍREZ, MÓNICA, GALVIS, VARGAS, LÉON, CIFUENTES, STEVENSON, Grow, Gursky-Doyen and Krzton2014, Twinomugisha et al. Reference TWINOMUGISHA, CHAPMAN, LAWES, WORMAN, DANISH, Newton-Fisher, Notman, Reynolds and Paterson2006, Yamagiwa & Basabose Reference YAMAGIWA and BASABOSE2006) so that overall, at higher altitudes ornithochory (avian frugivory) is prominent and far less seed is removed by primates (Gonzales & Stevenson Reference GONZALEZ, STEVENSON, Potoki and Krasinski2009).

The increase in relative frequency of frugivorous birds versus mammals with increasing altitude (Figure 1) may in part be due to the generally smaller body size (and therefore nutritional needs) of birds but also because the temporal fruit availability in TMF leads to downslope migration of avian frugivores in times of fruit scarcity (Cox Reference COX2010, Leighton & Leighton Reference LEIGHTON, LEIGHTON, Sutton, Whitmore and Chadwick1983, Loiselle & Blake Reference LOISELLE and BLAKE1991, Wright Reference WRIGHT, Dew and Boubli2005). This more general finding contrasts with Kimura et al. (Reference KIMURA, YUMOTO and KIKUZAWA2001), who report more constant fruit production in montane forests, relative to lowland forests of Mt. Kinabalu, Borneo. This may contribute to explanations for the greater relative abundance of birds year-round in this locale. However untangling cause and effect is complicated as an increase in the relative proportion of birds versus mammals at higher elevations may select for smaller, fleshy fruit (Duivenvoorden & Cuello Reference DUIVENVOORDEN and CUELLO2012, Lord et al. Reference LORD, EGAN, CLIFFORD, JURADO, LEISHMAN, WILLIAMS and WESTOBY1997).

Shorter dispersal distances and restricted seed shadows

While dispersal mode is not a strong predictor of dispersal distance in TLF (Clark et al. Reference CLARK, POULSEN, BOLKER, CONNOR and PARKER2005, Muller-Landau et al. Reference MULLER-LANDAU, WRIGHT, CALDERÓN, CONDIT and HUBBELL2008), large-bodied frugivores do tend to disperse seeds farther away from the parent tree than small-bodied ones (Jordano et al. Reference JORDANO, GARCIA, GODOY and GARCIA-CASTANO2007), and small passerine birds mostly disperse seeds only relatively short distances (Breitbach et al. Reference BREITBACH, BÖHNING-GAESE, LAUBE and SCHLEUNING2012, Jordano et al. Reference JORDANO, GARCIA, GODOY and GARCIA-CASTANO2007, Murray Reference MURRAY1988). Therefore, the distance seeds are dispersed should theoretically decline at the community level with increasing altitude in TMF. We found no published evidence for differences in movement range of primates between TMF and TLF, corroborating the findings of Chapman & Russo (Reference CHAPMAN, RUSSO, Campbell, Fuentes, MacKinnon, Panger and Bearder2007). However, the general finding that more of the available endozoochorous seeds are dispersed by passerine birds than primates in TMF points to relatively more seeds experiencing shorter gut passage times and shorter dispersal distances in TMF than TLFs. This hypothesis needs testing.

Dispersal

Several factors suggest that seed dispersal patterns should differ in a predictable way between TMF and TLF. Dispersal distances vary with frugivore species, so that fewer seed dispersing species in TMF should result in a narrower distribution of dispersal distances. The increase in smaller-bodied avian frugivores may arguably lead to more dispersal close to the parent tree in TMF relative to TLF. For reasons of propulsion and diaspore type, anemochorous diaspores tend to have shorter average dispersal distances than zoochorous ones (Augspurger Reference AUGSPURGER1986, Greene & Johnson Reference GREENE and JOHNSON1989, Nathan Reference NATHAN2006); given the relatively high proportion of anemochory in TMF this should also result in more dispersal closer to the parent tree in TMFs than LTFs (Figure 1).

Steeper slopes in TMF than TLF may cause more seeds to be washed downhill, away from the parent tree. Again, this aspect of TMF dispersal ecology has not received any attention – the only empirical investigation we found on clumping in TMF was from Ngel Nyaki forest in Nigeria where, at 1600 m asl, Matthesius (Reference MATTHESIUS2006) found that two tree species groups tested had a greater number of conspecific nearest neighbours than would be expected to occur by chance alone.

Post-dispersal seed fate

Predation/dispersal balance. Very little has been published on the predation/dispersal balance in TMF despite the dependence of many tropical forest trees on secondary dispersal (Aliyu et al. Reference ALIYU, ADAMU, MOLTCHANOVA, FORGET and CHAPMAN2014). Post-dispersal seed fate strongly affects forest regeneration (Wright Reference WRIGHT2003). Seed and seedling predators can act as selective filters to recruitment and establishment. Seed predators include mammals, birds and invertebrates but sometimes these predators inadvertently act as dispersers by moving but not immediately consuming seeds. This is particularly significant in the case of large nutrient-rich seeds which are sometimes secondarily dispersed by rodents through seed caching or scatterhoarding. The fate of cached/buried seeds will depend in part on rodent densities and overall fruit abundance. When overall fruit abundance is low, the ratio of predation to scatterhoarding or caching increases (Forget Reference FORGET1996) so that the potential for secondary dispersal declines. As overall fruit abundance is lower in TMF than in TLF and small-mammal densities increase up to mid-altitude forests, we predict higher predation/dispersal ratios in TMF than in TLFs. Meng et al. (Reference MENG, GAO, CHEN and MARTIN2012) found indirect evidence to support this hypothesis – higher densities of rodents in montane than lowland forest in southern China increased seed predation of experimental wild banana seeds. Even stronger support comes from Cannon (Reference CANNON2001). Cannon (Reference CANNON2001) found that some Asian Lithocarpus species, that typically have a well defended acorn, had a more extensive cupule than others and that these well defended species were more common in montane than lowland forest. The latter suggests greater selection for protection from predators at higher elevation (but see Chen et al. Reference CHEN, CANNON and CONKLIN-BRITTAN2012, Payne et al. Reference PAYNE, FRANCIS and PHILLIPS1985). Seed predation can be greater at higher altitudes, for example, an experiment using Carapa procera seeds in a Rwandan montane forest above 2000 m asl resulted in almost 100% predation, mainly by the African pouched rat (Cricetomys spp.) (Nyiramana et al. Reference NYIRAMANA, MENDOZA, KAPLIN and FORGET2011). In contrast, a similar experiment in Nigerian TMF at 1600 m asl found the dispersal probabilities for Carapa oreophylla seeds by Cricetomys spp. were close to those recorded from lowland Neotropical Carapa guianensis (Aliyu et al. Reference ALIYU, ADAMU, MOLTCHANOVA, FORGET and CHAPMAN2014). However, in a lean fruiting year at the same site almost 100% C. oreophylla seeds were predated (Chapman & Godwin unpubl. data). We hypothesize that higher predation rates of dispersed seeds in TMF lead to greater dispersal and recruitment limitation at higher altitudes than in TLFs.

Density-dependent mortality (DDM). Light, herbivory and pathogens exert strong density-dependent effects on seed and seedling survival and can affect plant species diversity in tropical forests. While a reasonable hypothesis is that DDM is less prevalent in TMF relative to TLF because TMF are less light-limited, have fewer herbivores and pathogens and are colder, more nutrient-poor environments (Xu & Yu Reference XU and YU2014), this needs testing. For example, Comita et al. (Reference COMITA, MULLER-LANDAU, AGUILAR and HUBBELL2010) found that common species are not as susceptible to DDM as rare species, a finding which supports our hypothesis because TMF tree diversity is often dominated by a few species, especially at higher-elevations (Martin et al. Reference MARTIN, FAHEY and SHERMAN2011). In contrast, Zhu et al. (Reference ZHU, WOODALL, MONTEIRO and CLARK2015) found that DDM was stronger for common than rare species. Lambers et al. (Reference LAMBERS, CLARK and BECKAGE2002) found that temperate forests have equally strong DDM as tropical forests. Studies within TMF also present equivocal findings. For example, Wenny (Reference WENNY2000) found no evidence of distance dependency in either seeds or seedlings of Ocotea endresiana in Costa Rican montane forest. In a Nigerian montane forest, only the seedling survival of Pouteria altissima, one of six species examined, displayed strong distance and density effects to herbivory (Matthesius et al. Reference MATTHESIUS, CHAPMAN and KELLY2011). In a ballistochorous species Philenoptera sutherlandii, Boudreau & Lawes (Reference BOUDREAU and LAWES2008) found no evidence for either density- or distance-dependent seedling survival (i.e. typically dense seedling populations in the canopy shade of parent trees) in an Afrotemperate forest. They found a hump-shaped dispersal kernel with predator satiation at high seedling densities near the parent tree.

A strong test of whether DDM is more important in TMF than TLF is to compare low and high elevation sites – only one field study has done this (Xu &Yu Reference XU and YU2014). In submontane China, Xu & Yu (Reference XU and YU2014) found lower seedling mortality due to soil-borne pathogens and less DDM among conspecific seedlings at high-elevation than low-elevation sites. Clearly, the extent to which seed dispersal accounts for differences between TMF and TLF in community structure and dynamics remains uncertain. Our proposition is that TMF communities may have better community resilience to disturbance, because of their small, light-adapted seeds, tolerance of low soil fertility and their dependence on small rather than large frugivores for dispersal.