Acta Oecologica 56 (2014) 32e40

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Acta Oecologica
journal homepage: www.elsevier.com/locate/actoec

Original article

Dispersal traits determine passive restoration trajectory of a Nigerian

montane forest
Andrew D. Barnes a, b, *, Hazel M. Chapman a
a
School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand
b
Systemic Conservation Biology, J.F. Blumenbach Institute of Zoology and Anthropology, University of Göttingen, Berliner Strasse 28,
37073 Göttingen, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Passive restoration methods offer great promise for tropical regions where resources are limited but the
Received 7 February 2014 success of such efforts can be variable. Using trait-based theory, we investigated the likely trajectories of
Accepted 25 February 2014 passive restoration efforts in a degraded Nigerian montane forest system recently protected from
Available online 15 March 2014
burning and cattle grazing. We quantified the density, species richness, and functional trait dispersion of
dispersed seeds and seedling communities at increasing distances from the forest edge. We then
Keywords:
determined which plant traits are responsible for colonisation by quantifying changes in functional-trait
Afromontane
dispersion and relative frequencies of dispersal-linked traits with increasing distance from the forest. We
Community assembly
Fruit traits
found a rapid decrease in density and species richness, and significant species turnover in both seeds and
Passive restoration seedlings just beyond the forest edge. This was mirrored by a significant decline in functional-trait
Seed dispersal dispersion and a shift in the relative frequencies of dispersal-linked traits. These findings suggest that
the reassembly of plant communities adjacent to remnant forest is dependent on functional traits pre-
sent in these remnant source populations, providing support for the incorporation of trait-based theory
in restoration management.
Ó 2014 Elsevier Masson SAS. All rights reserved.

1. Introduction Although potentially useful, passive restoration can be very slow

and often ineffective depending on landscape and ecological con-
Throughout the tropics, anthropogenic pressures have led to ditions (Duncan and Chapman, 1999; Laing et al., 2011; Myster,
such severe forest loss and degradation (Asner et al., 2009; Geist 2004). Factors such as insufficient seed rain (Cubiña and Aide,
and Lambin, 2002) that there is now a global effort towards their 2001; Duncan and Chapman, 1999; Martínez-Garza and Howe,
restoration (Chazdon, 2008; Holl, 2012) and the return of 2003; Muñiz-Castro et al., 2006), seed bank composition
ecosystem goods and services to local communities (Benayas et al., (Kalesnik et al., 2013), seed and seedling predation (Myster, 2004;
2009; Lamb et al., 2005). ‘Active’ restoration strategies, where Nepstad et al., 1990), lack of suitable microsites for germination
intervention techniques are used to re-establish forest, can be (Eriksson and Ehrlén, 1992), and competition from grasses
costly and impractical in areas where community involvement is (Chapman and Chapman, 1999; Duncan and Chapman, 1999) can
essential but resources are very limited (Holl and Aide, 2011; collectively hinder forest regeneration. Moreover, passive strategies
Parrotta et al., 1997). Alternatively, ‘passive’ restoration strategies, can lead to undesirable trajectories of ecosystem restoration
which involve only the restriction or total prevention of land-use because they are highly dependent on the potential for natural seed
practises from degraded land, are more easily employed and dispersal from nearby remnant habitat (Cole et al., 2011; del Castillo
require minimal resources (Holl and Aide, 2011; Morrison and and Ríos, 2008; Martínez-Garza and Howe, 2003). For example
Lindell, 2011). (Kalesnik et al., 2013) showed that after 30 years of abandonment,
commercial forests of exotic willow and poplar in Argentina
remained mixed secondary forest with a high frequency of invasive
species.
* Corresponding author. Systemic Conservation Biology, J.F. Blumenbach Institute
The likelihood of forest tree species dispersing into and estab-
of Zoology and Anthropology, University of Göttingen, Berliner Strasse 28, 37073
Göttingen, Germany. Tel.: þ49 551 395040. lishing within adjacent degraded habitat is highly variable and
E-mail address: abarnes@gwdg.de (A.D. Barnes). depends on a wide array of measurable factors including fruit and

http://dx.doi.org/10.1016/j.actao.2014.02.002
1146-609X/Ó 2014 Elsevier Masson SAS. All rights reserved.
 A.D. Barnes, H.M. Chapman / Acta Oecologica 56 (2014) 32e40 33

seed traits (Cole, 2009; Dosch et al., 2007; Ingle, 2003; Muller- the opening of these grassland areas where the pasture penetrates
Landau et al., 2008; Muñiz-Castro et al., 2006; Teegalapalli et al., into the forest to prevent further livestock and fire encroachment.
2010). Seed traits have also been shown to be important for The grassland sites described in this study had therefore all been
determining the success of propagules from seed banks, which may free of grazing and burning for four years. The sites were at least
explain further variation in the reassembly of regenerating plant 1000 m apart, located around the perimeter of Ngel Nyaki forest.
communities (Pywell et al., 2003). However, despite the wealth of
evidence illustrating the importance of plant traits in mediating
community assembly (Cornwell and Ackerly, 2009; Shipley et al., 2.2. Quantification of seed rain and seedling establishment
2006), the role that fruit and seed traits play in determining
dispersal of propagules into adjacent regenerating habitats and Sampling was carried out within four grassland areas that
their germination potential at the early colonisation stage still re- ranged in size from ca 4400 m2 to ca 8800 m2, dispersed
quires further investigation (Lebrija-Trejos et al., 2010). This is throughout Ngel Nyaki forest. Within each of the four areas, five
especially necessary in African forests where, to our knowledge, sampling transects were established, spaced 10 m apart, at least
there have been no studies that have identified the trait de- 10 m from the fence-line and at least 30 m from the forest edge at
terminants of both seed dispersal distances and resulting seedling the end of the grassland area undergoing restoration (Fig. 1). Each
establishment with increasing distance from remnant forest sys- transect consisted of eight seed traps, spaced equidistantly at 5 m
tems into adjacent grassland. intervals, from 5 m within the forest edge to 30 m out from the edge
Here we go beyond differentiating between seed size, wind and in the adjacent grassland (Fig. 1). The edge (0 m) was defined as the
animal dispersal (Cubiña and Aide, 2001; Duncan and Chapman, drip line of the outermost canopy trees at the forest perimeter. Seed
1999; Muñiz-Castro et al., 2006; Teegalapalli et al., 2010), and in traps consisted of a 0.5  0.5 m piece of mesh netting held 0.3 m
addition include dispersal traits such as fruit colour and fruit type, above the ground with a wooden frame in order to prevent the
which may affect frugivore choice (Gautier-Hion et al., 1985b) and surrounding vegetation from interfering with seeds falling into the
even secondary dispersal (Babaasa et al., 2004). To detect the role of traps and were protected by chicken wire to prevent the removal of
dispersal-linked traits in shaping assembly trajectories of forest seeds by seed predators.
regeneration, we first measured the potential for seed dispersal and All seed traps were visited weekly over a five year period from
seedling establishment from nearby remnant-forest habitat into January 2006 to December 2010, upon which all seeds found within
grassland recently protected from cattle grazing and burning. the traps were counted and identified to the species level. In the
Secondly, we quantified the dependence of seed rain and seedling most recent year of sampling (2010), we sampled seedling estab-
species functional-trait composition on the distance from these lishment across all trap locations whereby all trees and
remnant forests. As such, this study aims to provide an indication of shrubs  1 m tall and present within 2 m in any direction from a
the potential for using dispersal-linked traits in the prediction of seed trap (an area of approximately 12.5 m2) were counted and
restoration trajectories for future passive-restoration attempts in
Afromontane forests.

2. Methods

2.1. Study site

The study was conducted at Ngel Nyaki Forest Reserve on the

Mambilla plateau in Taraba State, Nigeria. The plateau is part of the
Cameroonian Highlands Ecoregion (Olson et al., 2001). Ngel Nyaki
reserve covers a total area of 4600 ha and includes 750 ha of
continuous forest embedded within a savannah-grassland land-
scape (Beck and Chapman, 2008; Chapman and Chapman, 2001).
The forest is mid-altitude to sub-montane at 1400e1600 m asl
(Chapman and Chapman, 2001), the mean annual rainfall is
approximately 1800 mm (Nigerian Montane Forest Project [NMFP]
rainfall data) and the mean monthly maximum and minimum
temperatures for the wet and dry seasons are 26e13  C, and 23e
16  C, respectively (Matthesius et al., 2011).
Since the 1950’s, when cattle grazing pressure became severe on
the Mambilla Plateau (Bawden and Tuley, 1966), areas of over-
grazed grassland dominated by Sporobolus pyramidalis and Hyper-
rhenia rufa have been created within Ngel Nyaki forest by the
annual fires lit by Fulani pastoralists to clear forest and stimulate
grass growth in the grasslands around the forest perimeter. Fires
run down grassy spurs leading into the forest and penetrate the
forest edge so that, over time, forest gaps comprising overgrazed
grassland have been created. These grassland areas are predomi-
nantly grassland with a scattering of tall herbs including Dissotis
species (Melastomaceae), Ocimum gratisimum and O. basilicum
(Lamaceae) and Guizotia species (Asteraceae). Small shrubs of
Fig. 1. Layout of the four sampling-point transects in the regenerating grassland sites.
Maesa lanceolata and Psorospermun febrifugum were occasionally Values marked on the transects indicate the distance from the forest edge with
present in all sites. As part of an initiative to promote forest negative values used to denote sampling points within the forest and “0” to denote the
regeneration, in 2006 we established fences and fire breaks across forest edge.
34 A.D. Barnes, H.M. Chapman / Acta Oecologica 56 (2014) 32e40

identified to species. We then calculated the number of seeds and 2011) with the ‘vegan’ package in R 3.0.1 (R Development Core
seedlings m2 to obtain a standardised measure of density. Team, 2013). Modified-Gower dissimilarity considers an order-of-
magnitude change in abundance (e.g., from 0.01 to 0.1) equal to a
2.3. Measurement of traits and functional dispersion change in composition (i.e. from 0 to 1 species), which therefore
accounts for changes in relative abundance of species in addition to
Traits that may contribute to the dispersal and recruitment changes in the community composition per se (Anderson et al.,
success of a species were obtained from the Nigerian Montane 2006). Compositional dissimilarity between the forest and adja-
Forest Project fruit database. Seed size was approximated by seed cent grassland was visualised using non-metric multidimensional
diameter in mm and fruit traits included three categorical traits scaling (NMDS) ordination. We then tested to see if the composi-
that characterised the fruit: dispersal mode, colour, and type tional dissimilarity between samples could be explained by the
(Table A.1). For dispersal mode, we specified whether the fruit is distance of the sampling point from the forest using a permuta-
ballistic, wind dispersed, gravity dispersed, and small (<10 mm tional distance MANOVA. ‘Distance to the forest edge’ was included
diameter) or large (>10 mm diameter) endozoochorous. Classifi- as a continuous predictor, with ‘site’ (n ¼ 4) specified as the strata
cation of fruit into small and large zoochorous was aimed at dis- within which to constrain permutations, thus avoiding pseudor-
tinguishing between seeds that were dispersed by small and large eplication resulting from the nested sampling design.
animal dispersers (Wheelwright, 1985); specifically, we assumed In order to quantify the trait determinants of community as-
that the large fruit could only be taken by primates and hornbills, sembly with increasing distance from the forest, we adopted a
whereas the small zoochorous fruit could be taken by all bird dis- multivariate approach for categorical variables whereby individuals
persers and also primates. Fruit colour was assessed by observation were coded by their relative functional trait values as opposed to
to give a potential indication of both the attractiveness of fruits to their taxonomic classification. With these data, we calculated
animal dispersers and the type of animal disperser likely to be resemblance matrices derived from the Gower dissimilarity metric
attracted (Gautier-Hion et al., 1985a; Willson and Whelan, 1990). as this measure can deal with categorical variable types and is not
Fruit type provided a proximate morphological description by affected by missing values (Laliberte and Legendre, 2010). From
indicating whether the fruit is a capsule, pod, winged, drupe, or these resemblance matrices, we performed a permutational
berry (Table A.1). MANOVA for each categorical trait (i.e. fruit type, dispersal mode,
To determine if there was a community-wide shift in the and fruit colour), with ‘distance to the forest edge’ as a continuous
dispersion of seed and fruit traits between the forest and adjacent predictor and ‘site’ as a blocking factor, to test the effect of distance
regenerating grassland, we calculated a distance-based metric of from the forest edge on both seed rain and seedling community
trait dispersion ‘FDis’ (Functional Dispersion) using the “FD” package trait-based compositional dissimilarity. For seed diameter, a
(Laliberte and Legendre, 2010) in R 3.0.1 (R Development Core Team, continuous variable, we used Generalised Additive Mixed Effects
2013). The FDis metric takes into account multiple traits of species Models to test for the effect of distance from the forest edge on
within a community and measures the distance of each species to community-weighted mean seed diameter with ‘seed-trap obser-
the trait-mean centroid of the whole community. It is a multivariate vations’ nested within ‘site’ as random effects.
adaptation of weighted-mean absolute deviation where the
weighting is given by the relative abundance of species (Laliberte 3. Results
and Legendre, 2010). Therefore, FDis is a weighted measure of trait
variation among species in a given community. As such, this measure 3.1. Rapid decline in seed and seedling density across the forest edge
provided an indication of the potential for trait-based filtering in
seed rain and seedling establishment into the adjacent grassland. From five years of seed trap data we recorded a total of 6332 seeds
comprising 31 species of trees and shrubs. We recorded a total of
2.4. Statistical analysis 2010 seedlings from 30 species across all sampling transects
(Table 1). 71% of these seedling species were also present in the seed
We analysed density, species richness, and functional dispersion trap data. There was a significant decline in seed-rain density from
in seed rain and seedling communities as non-linear functions of the remnant forest into the grassland (edf ¼ 5.701; P < 0.001), with a
distance from the forest edge into the adjacent grassland using 98% average decrease in seeds per m2 from the forest edge to 30 m
Generalised Additive Mixed Models (Wood, 2011) using the ‘mgcv’ into the grassland (Fig. 2a). This considerable decline in seed density
package in R 3.0.1 (R Development Core Team, 2013). Seed-trap with increasing distance into the grassland was mirrored by a 96%
observations were nested within site (n ¼ 4) as random effects in decrease in seedling densities (edf ¼ 6.177; P < 0.001; Fig. 2b). These
order to take into account the hierarchical layout of the sampling observed declines were only evident up to 10 m into the grassland,
design and avoid pseudoreplication (Zuur, 2009). To account for reaching asymptote beyond this point. Likewise, our results showed
non-normality and heterogeneity of variance, we modelled re- that the number of species from the seed rain data also declined
sponses of seed and seedling densities and species richness on a strongly with increasing distance from the forest (a 92% decrease;
Negative Binomial distribution, which also accounts for over- edf ¼ 1.422; P < 0.001; Fig. 2c) and the same trend was followed by
dispersion in the data (Zuur, 2009). We optimised smoothing pa- the number of seedling species (an 83% decrease; edf ¼ 1; P < 0.001;
rameters by selecting models based on the generalised cross- Fig. 2d). In contrast to the density responses, species richness showed
validation (GCV) criterion, whereby a lower GCV indicates lower a more continuous decline with increasing distance from the edge,
prediction error (Wood, 2011). As the GCV criterion has a tendency without reaching any clear asymptote within the 30 m range
to over-fitting, we applied a penalty on each degree of freedom, sampled. This was especially evident in seedling species richness,
whereby each effective degree of freedom (edf) was forced to be which showed no departure from a linear relationship (edf ¼ 1).
counted as 1.4 degrees of freedom in the GCV criterion (Kim and Gu,
2004). 3.2. Distance from source populations drives species composition
To test for spatial turnover in species relative abundances for and a decline in functional dispersion
dispersed seeds and seedling communities, we first calculated the
dissimilarity of species composition between sampling points using The NMDS visualisation indicated that the decrease in seed and
a log-base ten Modified-Gower distance metric (Anderson et al., colonising plant densities with increasing distance from the forest
 A.D. Barnes, H.M. Chapman / Acta Oecologica 56 (2014) 32e40 35

Table 1
List of all species and associated families found in samples with the total number of individuals recorded from seed traps and seedling plots for distance categories: 5 to 0 m,
5e15 m, and 20e30 m from the forest edge.

Family Species Seeds Seedlings

5 to 0 m 5 to 15 m 20 to 30 m 5 to 0 m 5 to 15 m 20 to 30 m

Mimosaceae Albizia gummifera 4 5 4 1

Caesalpiniaceae Anthonotha noldeae 48 9 43 23 13
Euphorbiaceae Bridelia speciosa 2474 126 355 153 48 20
Meliaceae Carapa oreophylla 51 1
Cannabaceae Celtis gomphophylla 1
Oleaceae Chionanthus africanus 1
Rutaceae Clausena anisata 100 1 9 241 3
Combretaceae Combretum molle 66 31 4 1 2
Euphorbiaceae Croton macrostachyus 1
Sapindaceae Deinbollia pinnata 10 60
Ebenaceae Diospyros sp. 127 595 5
Malvaceae Dombeya ledermannii 5 3 4 5 1
Meliaceae Entandrophragma angolense 2 2 1 9 6
Mimosaceae Entada abyssinica 25 3 1
Myrtaceae Eugenia gilgii 23 4
Clusiaceae Garcinia smeathmanii 7
Annonaceae Isolona deightonii 95 7
Apocynaceae Landolphia landolphioides 270 22 3
Leeaceae Leea guineensis 137 8 150 16 1
Myrsinaceae Maesa lanceolata 274 4
Mimosaceae Newtonia buchananii 61 35 123 13
Buddlejaceae Nuxia congesta 111 9 4 10 2
Rubiaceae Oxyanthus recemosus 1 5
Mimosaceae Parkia filicoidea 1
Sapindaceae Paullinia pinnata 40 13
Araliaceae Polyscias fulva 127 2 10 2
Sapotaceae Pouteria altissima 1 29
Clusiaceae Psorospermun febrifugum 60 5 33 88 50 18
Rubiaceae Psychotria sp. 435 28 4
Rubiaceae Psychotria succulenta 413 5 107 48 6 146
Apocynaceae Rauvolfia vomitoria 7
Malvaceae Sterculia setigera 16
Olacaceae Strombosia scheffleri 16
Clusiaceae Symphonia globulifera 7
Sapotaceae Synsepalum sp. 3
Myrtaceae Syzygium guineense 276 8 3 24 8 1
sub sp. guineense
Ulmaceae Trema orientalis 103 96
Moraceae Trilepesium madagascariense 2 2
Rutaceae Zanthoxylum leprieurii 1

was not equally distributed among species. This was suggested by 3.3. Trait-based filtering of propagules determines composition of
the gradient of increasing compositional dissimilarity from the colonising plant communities
forest to adjacent grassland (Fig. B.1), indicating an overall shift in
species’ relative abundances for seed rain and seedling commu- Community-weighted mean seed diameter did not significantly
nities. Furthermore, the permutational multivariate ANOVA respond to the distance from forest edge for either seed rain
revealed a highly significant effect of distance from the forest edge (edf ¼ 1; P ¼ 0.749) or seedling communities (edf ¼ 1.507;
on the dissimilarity of seed species composition (F ¼ 6.574, P ¼ 0.331) and appeared to vary idiosyncratically with increasing
P < 0.001) and the same was found for seedling communities distance from the edge (Fig. B.2a and b). However, for all three
(F ¼ 12.390, P < 0.001). Interestingly, we found that distance from categorical traits (i.e. fruit type, dispersal mode, and colour) there
the forest explained considerably more variation in seedling were clear changes in the relative proportion of traits with
composition (R2 ¼ 0.127) compared to seed rain composition increasing distance from the forest edge. In particular, fruit
(R2 ¼ 0.070). dispersal mode in the seed rain data significantly responded to
With the significant decline in seed rain and seedling estab- distance from the forest (F ¼ 7.420, R2 ¼ 0.078, P < 0.001) with
lishment away from the forest, we also found a decline in the range wind, small zoochorous and large zoochorous fruited species such
of trait composition. In particular, there was a significant decline in as Combretum molle, Bridelia speciosa, and Landolphia landolphioides
functional trait dispersion (FDis) from the forest to the adjacent respectively, having the highest dispersal potential beyond w20 m
grassland (edf ¼ 4.182; P < 0.001; Fig. 3a). While this was also the (Fig. 4c, Table 1). Furthermore, there was a significant effect of
case for seedling communities (edf ¼ 1; P < 0.001; Fig. 3b), the distance on seed rain community dissimilarity based on fruit type
degree of change in the functional trait dispersion of communities (F ¼ 9.132, R2 ¼ 0.094, P < 0.001) and colour (F ¼ 5.306, R2 ¼ 0.057,
was greater for seed rain composition than for establishing plant P < 0.001), whereby seed from drupes and capsules were most
communities (86% compared to only 75% decline for seed rain and likely to reach distances up to 30 m, with red and blue fruits
seedlings, respectively), with the greatest rate of change in FDis having the highest frequency of dispersal to greater distances
within 10 m of the forest edge for the seed rain. (Fig. 3e and g).
36 A.D. Barnes, H.M. Chapman / Acta Oecologica 56 (2014) 32e40

Fig. 2. Generalised additive mixed models demonstrating the relationships between distance from the forest edge and density (abundance m2) of seeds (a) and seedlings (b), and
the number of species recorded from the seed-rain (c) and seedling data (d). Smoothed lines are fitted values and shaded area is the 95% confidence interval. R2 is the proportion of
explained deviance. Negative and positive x-axis values denote forest and matrix, respectively, with 0 to denote the edge.

In contrast to the seed rain data we found that along with small- effects of the distance from the forest edge on trait-based compo-
zoochorous and wind-dispersed propagules, ballistic propagules sitional dissimilarity for fruit type (F ¼ 12.702, R2 ¼ 0.130,
(mainly from the species Anthonotha noldeae and Dombeya leder- P < 0.001) and colour (F ¼ 11.067, R2 ¼ 0.115, P < 0.001) in seedling
mannii) also made it to larger distances and successfully germi- communities. Whilst dispersed seedlings from drupes were still the
nated (Fig. 3d, Table 1) with an overall significant effect of distance most frequent across all distances, we found that seedlings from
from the forest on relative abundances of fruit dispersal modes species such as A. noldeae and C. molle with pods and winged
(F ¼ 15.354, R2 ¼ 0.153, P < 0.001). We also found highly significant propagules were also present at greater distances, albeit in low

Fig. 3. Generalised additive mixed models demonstrating the relationships between distance from the forest edge and functional trait dispersion (FDis) for seed-rain (a) and
seedling communities (b). Smoothed lines are fitted values and shaded area is the 95% confidence interval. R2 is the proportion of explained deviance. Negative and positive x-axis
values denote forest and matrix, respectively, with 0 to denote the edge.
 A.D. Barnes, H.M. Chapman / Acta Oecologica 56 (2014) 32e40 37

Seed rain Seedlings

(a) (b)
1.00

Category (proportion)
0.75

B
G
0.50 LZ
SZ
W

0.25

0.00

1.00
(c) (d)

0.75
Type (proportion)

B
C
0.50 D
P
W

0.25

0.00

(e) (f)
1.00

0.75
Color (proportion)

Bl
Br
0.50 Gr
Pu
Re
Wh
0.25

0.00
−5 0 5 10 15 20 25 30 −5 0 5 10 15 20 25 30
Distance from edge (m) Distance from edge (m)

Fig. 4. Relative proportions of dispersal mode categories for seed rain (a) and seedlings (b), frequencies of fruit type categories for seed rain (c) and seedlings (d), and frequencies of
fruit colours for seed rain (e) and seedling communities (f). Legend abbreviations for dispersal categories are: ballistic (B), gravity (G), large zoochorous (LZ), small zoochorous (SZ),
and wind (W). Fruit types are: berry (B), capsule (C), drupe (D), pod (P), and winged (W). Proportion areas for fruit colour are indicated by their actual colour. X-axis values of 5 and
0 denote 5 m within the forest and the forest edge, respectively.

frequencies (Fig. 3f, Table 1). However, seedlings from red and blue montane forest from burning and cattle grazing will not lead
fruits remained the most frequent across all distances from the directly to the rapid reassembly of forest communities, but instead
forest edge. to communities dominated by tree and shrub species characterised
by small, fleshy, red or blue drupes mainly dispersed by birds and
4. Discussion primates. However, mostly within this functional group we found
much more potential for forest regeneration in seed rain and early
4.1. What is the likelihood of success for passive restoration seedling establishment than has been recorded elsewhere in Africa
attempts in Afromontane forests? (Duncan and Chapman, 1999). We found seedlings in the grassland
up to 30 m away from the forest edge of grassland trees and shrubs
Our study demonstrates that dispersal-linked traits mediate the such as D. ledermannii and Psorospermun febrifugum, forest-edge
reassembly trajectory of regenerating plant communities under- tree species including Eugenia gilgii and Nuxia congesta and the
going passive restoration following severe human-induced land- large, leguminous forest tree species Albizia gummifera and
scape degradation. Through a combination of ecological filters such Anthonotha noldeae.
as dispersal limitation and factors inhibiting germination, our re- Of those seed species recovered from the traps, only 71% were
sults suggest that simply protecting cleared areas of West African present as seedlings, and of those seedlings found beyond five m
38 A.D. Barnes, H.M. Chapman / Acta Oecologica 56 (2014) 32e40

from the forest edge, over 90% germinated from small, fleshy and have been found not to contribute usefully to seed rain in forest
drupes. The 29% of seed species found in traps but never as seed- regeneration elsewhere in Africa (Duncan and Chapman, 1999).
lings comprised a wide range of seed types and their apparent lack While investigation of the role of birds in dispersing seeds into
of regeneration is presumably explained by a combination of post these grasslands is currently underway at Ngel Nyaki, the fact that
dispersal factors such as unsuitable microsites and seed predators such fruits are also dispersed by several primate species including
(Chapman and Chapman, 1999), competition from grasses such as tantalus monkeys (Chlotocebus tantalus), which regularly enter and
the introduced Sporobilis sp. and Hyperrhenia sp. (Chapman and feed in grassland (Agmen et al., 2010), may explain the pattern of
Chapman, 2001) and drought during the six month dry season seed rain we observed. Moreover, our finding that seed diameter
(NMFP rainfall records). Additionally, while there may be sufficient appeared to be of little importance for the dispersal potential of
seed dispersal and even germination of forest plant species, there seeds and germination of seedlings with increasing distance from
are likely to be other barriers limiting their recruitment, such as the the forest edge is also most likely explained by primate dispersal as
requirement of larger established trees for colonizing vine species the wider gape of primates relative to passerine birds allow them to
like Landolphia landolphioides (Table 1). swallow larger seed (Jordano et al., 2007). While such findings are
Seed rain density declined dramatically only just beyond the also in contrast to previous Neotropical studies (Cubiña and Aide,
forest edge, indicating that the matrix is important for mediating 2001; Holl, 1999) they are similar to those of Teegalapalli et al.
rates of dispersal across the forestegrassland interface (Barnes (2010) who investigated the dispersal of large seed from Indian
et al., 2014; Holl, 2012). Relatively high numbers of dispersed dry forest into pasture related to grazing patterns of large
seed were still found 5 m out from the forest edge, but beyond this mammalian frugivores.
point seed densities dropped to only 2% of the densities found A particularly interesting finding was the relatively high density
under the forest canopy within 5 m of the forest edge. While of seedlings from ballistic-dispersed seeds across larger distances
densities of animal dispersed seeds appeared to remain relatively from the forest, despite relatively lower numbers within the forest
constant beyond 5 m out from the forest edge, even at the sampling points. For example the very large, nutritious seeds of
maximum distance measured of 30 m, this was not the case for Anthonotha noldeae were rarely found in seed traps beyond 5 m into
wind dispersed seed which had dropped off dramatically ten m into the grassland, yet seedlings were found up to 30 m away from the
the grassland. Such a rapid decrease in density of wind dispersed forest edge. Such a pattern is indicative of dispersal by secondary
seed is to be expected and has been recorded in previous studies seed dispersers such as scatter-hoarding rodents (Nyiramana et al.,
from the Neotropics (Cubiña and Aide, 2001; Holl, 1999) and dry 2011). While not included in this study, we have observed a similar
forest in India (Teegalapalli et al., 2010). In regard to animal phenomenon in Carapa oreophylla whose seedlings establish many
dispersed seed our findings suggests that in these regenerating metres from the forest edge (personal observation). Wind was also
grasslands, which are often no wider than 60 m, regardless of the found to be a successful mode of dispersal for trees to colonise
distance from the forest edge we can expect equal densities of seed these grasslands as both seed and/or germinating seedlings from
rain from the adjacent forest. wind/winged classed species, such as Albizia gummifera, Com-
In addition to the decline in seed and seedling densities, we bretum molle and Entandrophragma angolense, were found at low
found that there was significant turnover in species composition but relatively consistent numbers across all distances.
with increasing distance from the forest edge, despite the relatively
fine-scale gradient of 5 m incremental changes in distance. For 4.3. Applications for trait-based theory in habitat restoration
example, seedlings of pioneer species with small, fleshy fruit such
as Bridelia speciosa and Psychotria succulenta became relatively By quantifying patterns in functional trait dispersion and
more common with distance from the forest edge relative to forest changes in community trait composition of seeds and seedlings
species such as Pouteria altissima and Deinbollia pinnata, which across the interface of remnant forest and passively regenerating
have larger, green fruit. While it is possible that recruitment is grassland, this study shows that regenerating plant communities
strongly limited after seedlings germinate due to factors such as undergo trait-based filtering, which appears to increase in intensity
those described above (Duncan and Chapman, 1999; Holl, 1999; with increasing distance from the forest. Despite the strong
Nepstad et al., 1990) our findings suggest that in naturally regen- filtering of species dispersing into these adjacent grasslands, the
erating West African montane systems, dispersal limitation may be somewhat high density and diversity of germinating seedlings in-
playing an important role in the early stages of community reas- dicates that there is still promise for passive restoration efforts in
sembly, even across small spatial scales. Afromontane forest landscapes. It must be noted, however, that this
study has only taken into account a relatively short time-scale of
4.2. Can fruit and seed traits predict restoration outcomes? regeneration time (over just 5 years) and therefore provides insight
into the initial recolonisation process. It is likely that over a much
From these findings, the question arises as to which factors are greater time-scale there may be rare, chance dispersal events that
determining the varying levels of dispersal limitation. The answer result in the dispersal of important pioneer species into these
may be pivotal to understanding how forest communities are likely regenerating communities which may in fact catalyse the restora-
to reassemble during passive restoration efforts. We found that tion process (Rodrigues et al., 2004). Furthermore, there is evidence
from the four selected dispersal-linked trait measures used, in in the Afrotropics that regeneration can be arrested due to dispersal
almost all instances they changed in relative frequency with limitation and/or the competitive dominance of other non-forest
increasing distance away from the parent populations. Most species (Babaasa et al., 2004; Duncan and Chapman, 1999). Still,
obvious was the finding that seed from fruits that were small- our study provides a characterisation of the early recolonisation
zoochorous red drupes were dispersed relatively more often and processes that are likely to take place in passive restoration at-
in greater quantities across most distances and were found at least tempts, which is important for identifying the mechanisms that can
up to distances of 30 m more frequently than any other propagules. potentially lead to undesirable restoration trajectories.
These results point to the importance of traits that are linked to While previous studies have shown that plant traits play an
avian dispersal as these would be among the most attractive fruit to important role in later phases of community assembly within
such dispersers (Duncan and Chapman, 1999; Willson and Whelan, passively restored habitats (Muñiz-Castro et al., 2006; Pywell et al.,
1990). However, birds are known to be extremely habitat selective 2003) we still lack an understanding of how these traits determine
 A.D. Barnes, H.M. Chapman / Acta Oecologica 56 (2014) 32e40 39

community reassembly at the initial stages of habitat regeneration. del Castillo, R.F., Ríos, M.A.P., 2008. Changes in seed rain during secondary suc-
cession in a tropical montane cloud forest region in Oaxaca, Mexico. J. Trop.
This study highlights the value of quantifying these trait de-
Ecol. 24, 433e444.
terminants so that they can be utilised to gain a priori knowledge of Dosch, J.J., Peterson, C.J., Haines, B.L., 2007. Seed rain during initial colonization of
the potential for success and likely trajectory of passive restoration abandoned pastures in the premontane wet forest zone of southern Costa Rica.
efforts, depending on the functional-trait composition of nearby J. Trop. Ecol. 23, 151e159.
Duncan, R.S., Chapman, C.A., 1999. Seed dispersal and potential forest succession in
parent populations. Therefore, we recommend that future attempts abandoned agriculture in tropical Africa. Ecol. Appl. 9, 998e1008.
to passively restore tropical forests should first quantify the po- Eriksson, O., Ehrlén, J., 1992. Seed and microsite limitation of recruitment in plant
tential for species to colonise target-restoration areas from nearby populations. Oecologia 91, 360e364.
Gautier-Hion, A., Duplantier, J.-M., Quris, R., Feer, F., Sourd, C., Decoux, J.-P.,
remnant forests by utilising the ‘library’ of functional traits found Dubost, G., Emmons, L., Erard, C., Hecketsweiler, P., 1985a. Fruit characters as a
within these communities. basis of fruit choice and seed dispersal in a tropical forest vertebrate commu-
nity. Oecologia 65, 324e337.
Gautier-Hion, A., Duplantier, J.M., Quris, R., Feer, F., Sourd, C., Decoux, J.P., Dubost, G.,
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Thiollay, J.M., 1985b. Fruit characters as a basis of fruit choice and seed dispersal
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We thank the Taraba State Forest Service for inviting us to work
Geist, H.J., Lambin, E.F., 2002. Proximate causes and underlying driving forces of
in Ngel Nyaki Forest, Usman Abubakar for assistance in the field, tropical deforestation. Bioscience 52, 143e150.
and the other Nigerian Montane Forest Project staff for logistical Holl, K.D., 1999. Factors limiting tropical rain forest regeneration in abandoned
support at the NMFP field station. Kristy Udy, Laura Young, and the pasture: seed rain, seed germination, microclimate, and soil. Biotropica 31,
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Chapman lab group provided invaluable comments on earlier drafts Holl, K.D., 2012. Tropical forest restoration. In: Andel, J.V., Aronson, J. (Eds.),
of the manuscript. We also thank two anonymous reviewers for Restoration Ecology. Blackwell Publishing, Malden, MA, pp. 103e114.
providing comments and suggestions that substantially improved Holl, K.D., Aide, T.M., 2011. When and where to actively restore ecosystems? For.
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this paper. The study was funded by the North of England Ingle, N.R., 2003. Seed dispersal by wind, birds, and bats between Philippine
Zoological Society (Chester zoo), Nexen Inc. and the A. G. Leventis Montane rainforest and successional vegetation. Oecologia 134, 251e261.
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secondary forest in the Lower Delta of the Paraná River (Argentina). Acta Bot.
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