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Pollen Dispersal Patterns in a Fragmented

Population of Carapa nicaraguensis (Meliaceae)

Article in International Journal of Plant Sciences · February 2014

DOI: 10.1086/673304

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Pollen Dispersal Patterns in a Fragmented Population of Carapa nicaraguensis (Meliaceae)
Author(s): Jorge Lobo Segura and Dennis Jiménez Vargas
Source: International Journal of Plant Sciences, Vol. 175, No. 2 (February 2014), pp. 176-185
Published by: The University of Chicago Press
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Int. J. Plant Sci. 175(2):176–185. 2014.
䉷 2013 by The University of Chicago. All rights reserved.
1058-5893/2014/17502-0003$15.00 DOI: 10.1086/673304

POLLEN DISPERSAL PATTERNS IN A FRAGMENTED POPULATION OF

CARAPA NICARAGUENSIS (MELIACEAE)
Jorge Lobo Segura1,* and Dennis Jiménez Vargas*
*Escuela de Biologı́a, Universidad de Costa Rica, San José, Costa Rica

Editor: Michele R. Dudash

Premise of research. Pollen-dispersal distances may be flexible and dependent on a variety of landscape
factors. The study of the effect of plant density and forest fragmentation on dispersal distances is important
to understand the response of plant populations to habitat loss or harvesting, especially in tropical timber
tree species.
Methodology. A comparison was made of the pollen-dispersal curves of the timber tree Carapa nicara-
guensis in three different habitats in southern Costa Rica: (i) forest remnants in hills with low density of the
study species, (ii) a gallery forest in a swampy area with high density of the study species, and (iii) isolated
trees in pastures. Microsatellite genotypes were used to determine the genealogical relationships between adults,
seeds, and seedlings collected below tree crowns. Bayesian methods were used to simultaneously estimate the
dispersal-distribution parameters, genealogical relationships, genotyping error rates, and numbers of unsampled
males.
Pivotal results. The pollen-dispersal distances were influenced primarily by the surrounding matrix and
degree of spatial isolation of the local population. Pollen dispersal was more extensive between trees in forest
fragments than in other habitats. Predominant selfing was found in a single tree isolated in pastures. Evidence
of seed dispersal to a different tree crown was found for trees in forest fragments.
Conclusions. The results are consistent with those of previous studies indicating that pollen-dispersal
patterns are dependent on the degree of isolation and tree density of local populations. Genetic connectivity
across the fragmented landscape is maintained by trees in low-density forest fragments and isolated trees in
pastures, whereas trees in high-density gallery forests are genetically isolated from the rest of the population.

Keywords: pollen flow, seed dispersal, forest fragmentation, genetic structure.

Introduction creasingly in-depth knowledge regarding gene flow in tropical

An understanding of pollen- and seed-mediated gene flow
in tropical plants is important for ecological studies and for
tropical ecosystem conservation. The distributions of pollen-
and seed-dispersal distances and their variability under differ-
ent demographic and environmental conditions determine the
genetic structure of a plant population and the capacity of the
population for genetic exchange in landscapes that have been
fragmented or altered by human activities. These concerns are
particularly important for tropical-canopy timber species that
are endangered by the joint effects of habitat loss and logging
activities. High deforestation rates (Achard et al. 2002) and
logging practices (Broadbent et al. 2008) are ongoing threats
to the viability of tropical tree populations, particularly for
slow-growing species that are better adapted to undisturbed
habitats.
Analyses using molecular genetic markers have provided in-
1
Author for correspondence; e-mail: jorgelobosegura@gmail.com,
jorge.lobo@ucr.ac.cr.
Manuscript received March 2013; revised manuscript received June 2013; elec-
tronically published November 12, 2013.
trees and have improved our understanding of mating systems
and seed and pollen dispersal. These analyses have demon-
strated the capacity for long-distance pollen and seed dispersal
in many tropical tree species, although short-range dispersal
events are generally more common (for reviews, see Hamrick
and Murawski 1990; Murawski and Hamrick 1991; Stacy et
al. 1996; Ward et al. 2005; Dick et al. 2008; Hamrick 2010).
The means and variances of pollen- and seed-dispersal dis-
tance distributions can vary greatly within and between pop-
ulations depending on differences in the environmental con-
ditions that affect the population or individual trees, such as
pollinator abundance and behavior, habitat fragmentation,
and population density. Pollination studies and genetic anal-
yses of temperate plant species with different densities and
spatial isolation levels indicate that a closer proximity between
inflorescences of the same individual or between different in-
dividuals is associated with shorter pollinator-flight distances
(Levin and Kerster 1969; Schmitt 1983; Goodell et al. 1997;
Garcı́a et al. 2005) and that female or hermaphroditic flowers
act as “pollen traps” that determine the dispersal-distance dis-
tribution. This trend has also been observed in genetic analyses
of tropical trees. For example, White et al. (2002) have shown

176

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 LOBO & JIMÉNEZ—VARIATION OF GENE FLOW IN CARAPA NICARAGUENSIS
that the magnitude of pollen flow between groups of trees
distributed over a fragmented landscape depends on the pop-
ulation size and degree of isolation of each fragment. Spatially
isolated individuals in pastures frequently show higher selfing
rates and longer pollen-dispersal distances compared to indi-
viduals within denser populations in continuous areas (Aldrich
and Hamrick 1998; Dick 2001; Eckert et al. 2009; Fuchs and
Hamrick 2010). In relation to the effect of forest fragmentation
on seed dispersal, some researchers have proposed that seed
dispersal is affected by increased habitat fragmentation re-
sulting from reduced or altered foraging patterns of seed and
fruit dispersers and of their predator populations (Wright et
al. 2001; Chapman et al. 2003; Cordeiro and Howe 2003;
Ghazoul 2005; Galetti et al. 2006; Cramer et al. 2007). There-
fore, plant species’ pollen- and seed-dispersal patterns are flex-
ible because they arise from the interaction between floral and
fruit characteristics, dispersal agents, and landscape condi-
tions.
In view of the above considerations, more data are needed
on the variation of pollen- and seed-dispersal distributions in
heterogeneous landscapes with forest fragments that differ in
tree density, patch size, isolation level, and surrounding matrix
quality. These data would make it possible to study the effect
of landscape variation on gene-flow patterns. Studies using this
approach should be conducted on a scale that is sufficiently
large to capture the landscape variability and population struc-
tures of the study species. Gene flow should be analyzed using
methods that take into account the difficulty of exhaustive
sampling of parental individuals on a large spatial scale
(Smouse et al. 2001; Burczyk et al. 2006; Hadfield et al. 2006).
We studied the variation in pollen-dispersal distribution pa-
rameters for a Neotropical timber species, Carapa nicara-
guensis (Meliaceae), of which populations have been affected
by both habitat fragmentation and logging. For this study we
collected progenies (seeds and seedlings) below tree crowns of
a population located in a fragmented landscape in southern
Costa Rica. In southern Costa Rican wet forests, C. nicara-
guensis trees are found in a variety of forest fragments that
are fairly close to each other (0.5–2 km) but that differ in
terms of area, shape, topography, tree density, and isolation
level. The primary purpose of this study was to determine the
variation in pollen-dispersal distributions and selfing rates in
a C. nicaraguensis population within this fragmented land-
scape, based on a genetic analysis of progenies and adults
(maternal trees and pollen donors). However, due to the fact
that we observed some progenies genetically incompatible with
the genotype of the nearest tree, we also studied maternal or-
igin of seeds and seedlings found under tree crowns. The seed-
mediated gene flow of Carapa trees may be particularly sus-
ceptible to habitat fragmentation because of these species’
dependence on secondary seed dispersal by rodents (agoutis;
Guariguata et al. 2002; Forget and Jansen 2007). Specifically,
we studied (1) the effect of adult-progeny distance on the prob-
ability of progeny paternity, which was used as parameter for
measuring pollen-dispersal distances, (2) the variation in the
maternal provenance of seedlings and seeds found under tree
crowns, and (3) the variation in these parameters among neigh-
borhoods with different degrees of forest fragmentation and
population densities of C. nicaraguensis.
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177
Methods
Study Species
Carapa nicaraguensis C. DC (Meliaceae) is a canopy tree
species that is distributed from Nicaragua to the Pacific coast
of Colombia and Ecuador (Kenfack 2011a, 2011b) and is most
common in flat, swampy areas. Species-level taxonomic clas-
sification within the genus Carapa is controversial. However,
a recent review of the genus (Kenfack 2011a) permits us to
classify most Carapa populations in Costa Rica, including
those analyzed in our study, as C. nicaraguensis. This species
can be distinguished from the more widely distributed Carapa
guianensis by the presence of indumentum on the leaves, in-
florescences, and flowers and by the smaller size of the hilum
on the seeds (Kenfack 2011b). This species has large, com-
pound, alternate leaves and a cylindrical trunk of medium to
large size (up to 45 m height and 2 m dbh), although individ-
uals with trunks of dbh 1 20 cm may produce flowers and
occasionally fruits. The species is monoecious and bears small,
unisexual flowers (diameter ! 0.5 cm) in terminal inflores-
cences. Pollination is most likely performed by small insects,
including stingless bees and butterflies (J. A. Lobo Segura, per-
sonal observation). In Amazonian forests, pollinators of the
related species C. guianensis include stingless bees (Apidae)
and butterflies (Riodinidae and Lycaenidae; Maués 2006). The
inflorescences contain equal numbers of male and female flow-
ers (J. A. Lobo Segura, personal observation). In southern
Costa Rica, populations of this species display two periods of
flowering and fruiting: December–January and June–August
(Lobo et al. 2008). Fruit development takes ∼6.5 mo (Lobo
et al. 2008). The mating system is based predominantly on
outcrossing (Hall et al. 1994; Doliguez and Joly 1997; Cloutier
et al. 2007). The fruits are large and spherical and have large
seeds (5–6 # 4–6 cm). Seed dispersal is highly dependent on
secondary dispersal by large rodents (Dasyprocta punctata and
Agouti paca in the study area) that practice scatter hoarding
(Forget 1996; Guariguata et al. 2002), although dispersal by
water or gravity is also probable (Scarano et al. 2003). In our
study area, the species is found in riparian areas, plains, and
mountain ranges, although it reaches its highest densities in
flat, swampy areas. Although C. nicaraguensis is a shade-tol-
erant species, its seedlings and saplings show increased dia-
metric growth in response to light (Webb 1999).
Study Site
The studied population of C. nicaraguensis is distributed
throughout a landscape of forest fragments in the vicinity of
Mogos, Golfo Dulce Forest Reserve, Puntarenas Province,
Costa Rica (8⬚4625N, 83⬚2117W; fig. 1). It includes a south-
ern section of low mountain ranges (200 m elevation) with
steep slopes, which protect small hydrographic river basins
and streams draining to the northern section. The northern
section is composed primarily of flat, semiswampy areas that
have been deforested for cattle ranching and small forested
hills (fig. 1). Most of the study area is classified as pastures
and young secondary growth. Old-growth forest is restricted
to fragments in hills and gallery forests in swampy areas, with
a total extension of 88.5 ha. The life zone of the study area
is Tropical Rain Forest according to Holdridge’s (1969) clas-
178 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 1 Location of studied individuals and observed pollen flow patterns in a study population of Carapa nicaraguensis. Triangles are maternal
tree progeny sampled below tree crown; circles are sampled trees without progenies. Pollen flow events are based on paternity assignments with
a probability of 10.8. Light gray areas represent pastureland, black areas represent gallery forest, and dark gray areas represent forest fragments.
White areas represent young secondary forests, scrubland, and crops. The lines represent pollen flow routes from the pollen donor to the mother
tree. Solid lines represent pollen-movement events within neighborhoods, and dotted lines represent pollen-movement events between neigh-
borhoods. FF1, FF2, FF3, and FF4 refer to forest fragments; GF refers to gallery forest; and IT1, IT2, and IT3 refer to three neighborhoods of
isolated trees in pastures. The numbers over the pollen-movement arrows indicate the number of times each movement was observed.

sification, and the study area is part of the forest systems of
the Osa Peninsula and Golfo Dulce coastal regions of southern
Costa Rica. The climate in this region is characterized by high
annual precipitation (3500–5000 mm) and a short dry season
from January to March (monthly precipitation !100 mm). The
temperature is moderately high throughout the year, with a
minimum of 21⬚C and a maximum of 33.5⬚C. The highest
precipitation levels occur from August to October (monthly
precipitation 1000–2000 mm). Deforestation and forest frag-
mentation in the region occurred primarily during 1980–1995
due to the expansion of agriculture and cattle raising. A de-
crease in agricultural activity and the increased governmental
protection of forested areas have resulted in a significant re-
duction of the deforestation rate during the past 10 years.
Sampling Design
During a 3-yr period (September 2005–June 2008), we per-
formed an exhaustive search of C. nicaraguensis adult trees
(120 cm dbh) throughout the study area, which comprises
three main habitats: gallery forest (1.9 ha), forest fragments
(128.2 ha), and pastures (262.5 ha; see below for habitat de-
scriptions). We determined based on previous observations
that flowering of trees below 20 cm dbh is rare. We obtained
tissue samples from a total of 88 adult individuals located in
the three main habitats within the study area (fig. 1). Another
13 individual adult trees were located in forest fragments but
were not sampled because of their difficult access. The trees
were located using a handheld GPS device and mapped onto
a recent aerial photograph of the study area to help obtain a
clear definition of the forest cover.
In addition to sampling adult tissues, we collected seeds and
seedlings (plants of height !25 cm) under the canopies (within
a radius of 25 m around the trunk) of 38 of the 88 located
adults. These trees were designated as “maternal trees” because
most of the seeds and seedlings collected below tree crowns
are progenies descended from that tree (see “Results”). We
avoided collecting progeny in areas that displayed the super-
position of canopies from different adult individuals. The ma-
ternal trees were assigned to groups of nearby individuals,
which were called “neighborhoods.” The distance between
trees within a given neighborhood was 20–200 m. The distance
between a given tree and the nearest tree located in another
neighborhood was 415–736 m. The neighborhoods were lo-
cated within three habitat types, as described below.

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 LOBO & JIMÉNEZ—VARIATION OF GENE FLOW IN CARAPA NICARAGUENSIS 179

i) Forest fragments on hills (FF): forest remnants with an
area of 20 ha or more, located in the southern, northeastern,
and central mountain ranges of the study area (fig. 1). The
calculated local density of C. nicaraguensis adults was 0.42
trees/ha (table 1). In this habitat, four neighborhoods (FF1,
FF2, FF3, and FF4) were located in four forest fragments (fig.
1).
ii) Gallery forest (GF): a narrow, linear forest fragment ∼500
m in length and 100 m in width extending along a riverbed
in the flat, swampy portion of the study area. GF was sur-
rounded by pastures and was separated from the nearest forest
fragments (FF2 and FF4) by a distance of 300–500 m. The
local density of C. nicaraguensis in GF was high (19.4 trees/
ha).
iii) Isolated trees (IT): a grouping of various isolated trees
located in flat pasture areas. Each tree was separated from
nearby forest fragments by a distance of at least 50 m. The
local density of C. nicaraguensis was low (0.04 trees/ha), but
the individuals were smaller (average dbh p 39 cm). Three
IT neighborhoods were defined, representing groups of isolated
trees in three different parts of the sampling area.
The average number of seeds or seedlings per maternal tree
(progeny group) was 14.1 (SD p 14.8). Collection of both
seeds and seedlings beneath the same tree crown was possible
for only nine of the maternal trees. The variation in progeny
group size per maternal tree is explained by the high variance
among tree crowns in the number of seeds and seedlings, re-
sulting from intertree differences in fertility, dispersal, and
progeny survival rates. Nevertheless, it was possible to obtain
similar sample sizes of progeny per habitat to compare dis-
persal parameters.
Genetic Analysis
Tissue samples from adult trees (bark or leaves) and progeny
(embryos or leaves) were homogenized with liquid nitrogen in
mortars, and DNA was extracted using the DNeasy Plant Mini
kit (Qiagen). Eight pairs of primers to amplify microsatellites,
developed for C. guianensis by Dayanandan et al. (1999; Cg5,
Cg6, Cg7) and Vinson et al. (2005; Cg01, Cg06, Cg11, Cg16,
and Cg17), were used in PCR multiplex reactions using the
Master Mix Multiplex kit (Qiagen). The PCRs were performed
in a total volume of 12.5 mL containing 6.25 mL Multiplex
Master Mix, 1.25 mL primer mix, 1 mL of DNA, and 4 mL of
water. The PCR sequence consisted of an initial step of 95⬚C
for 15 min, 30 amplification cycles (94⬚C for 30 s, 57⬚C for
90 s, 72⬚C for 60 s), and a final step of 72⬚C for 10 min. The
final PCR products were analyzed using an ABI 310 sequencer
(Applied Biosystems), and the samples were genotyped using
the Genotyper software program (Applied Biosystems). To es-
timate the average genotyping error rate per locus, 50 indi-
viduals were amplified two to three times each.
Data Analysis
The first objective of the data analysis was to compare the
effect of distance on the probability of paternity of progeny
among the three habitat types. The relationship between the
probability of paternity and distance is an estimate of the pol-
len-flow distribution. Although the large seed size in this spe-
cies suggests that all progeny under a nonoverlapping crown
are derived maternally from that tree, the genetic analysis
showed that a significant percentage of the progeny (∼8%; see
“Results”) did not share alleles for at least one locus with the
tree below which they were collected. Seed dispersal or ge-
notyping errors might account for this result. Accordingly, the
data analysis took into consideration the uncertainty of ma-
ternal origin and possible genotyping error in estimating the
pollen-dispersal parameters.
The Bayesian model proposed by Hadfield et al. (2006) was
used to estimate and compare parameters between the habitats.
This model was implemented in the program MasterBayes 2.47
(Hadfield et al. 2006), which is written in the R language (R
Development Core Team 2008). The MasterBayes model as-
sumes that the probability that an individual is the parent of
a particular progeny changes according to distance following
an exponential function, where l is the parameter that deter-
mines the rate of change of the probability in relation to dis-
tance. In our study, di will be the distance between a putative
mother and the progeny i in the case of seed dispersal. In the
case of pollen dispersal, the term di will be the distance between
a putative father and the putative mother of the progeny i.
When l ! 0, adult individuals that are closer to the progeny
are more likely to be the parents. When l 1 0, distant adults
are more likely to be the parents. When l p 0, parentage is
independent of distance. If the male parent is an unsampled
adult, the genotype and distance are unknown. The possibility
that the female parent is an unsampled adult can be dismissed
because of the limited seed-dispersal distance in this species
(see “Results”). In our study, the joint probability Pr(Aijk) that

Table 1
Adult (dbh 1 20 cm) Size and Density, Progeny-Adult Distances, and Sample Sizes in Three Different Habitats of
the Carapa nicaraguensis Study Populations
Density of reproductive individuals Sample size
Mean Progeny-adult
Density adult mean Adults Adults with Progeny
Habitat (trees/ha) dbh (cm) distancea sampledb progeny sampledc
Forest fragments .42 54.0 64.5 (30.5) 41 18 139
Gallery forest 19.4 47.3 15.2 (8.7) 37 8 150
Isolated trees .04 38.9 44.1 (22.3) 10 5 75
a
Average distance to the nearest adult of all progeny within the habitat. Numbers in parentheses are standard errors.
b
Number of adults sampled per habitat.
c
Number of seeds and seedlings sampled per habitat.

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180 INTERNATIONAL JOURNAL OF PLANT SCIENCES
a male parent j (with multilocus genotype Fj) and a female
parent k (with multilocus genotype Mk) are the parents of
progeny i (with genotype Oi) is
Pr A ijk p
Pr(OFM
i k , F)
j culated from the posterior probability distribution of the pa-
冘 冘
n
jp1
n
kp1 Pr(OFM
i j ⫹ 冘kp1 (N ⫺ n)Pr(OFM
k , F)
n
i k , A)
e d jklF e d iklM
# # ,
冘jp1 e djklF 冘kp1 e diklM
n n
where A is the population gene frequencies, N is the real size
of the male-parent population, n is the number of sampled
adults, and l F and lM are the parameters of the exponential
function of the effect of distance for male and female parents,
respectively. The MasterBayes model can also estimate the
probability of error due to allelic dropout (E1) or other sources
of genotyping error (E2). The number of unsampled male par-
ents (N ⫺ n) is estimated jointly with the l parameters, the
error rates, and the genealogy of the sample (Hadfield et al.
2006). The parameters are estimated through iterations that
estimate the joint probability distribution using the Gibbs sam-
pling technique. The joint estimation of parentage and the
population parameters increases the power of the paternity
assignment, reduces the estimation bias, and estimates the un-
certainty of the paternity assignment and parameters more
precisely (Walling et al. 2010). To help discriminate maternal
and paternal parentage of progenies, different normal distri-
butions were used as priors for lM (m p ⫺0.15, s 2 p 0.01)
and l F (m p ⫺0.01, s 2 p 0.01). The priors determine that the
effect of distance on the probability of maternity is much higher
than the probability of paternity, as corresponds to a species
with large seed size. The specific values chosen for the priors
create normal distributions with average dispersal distances of
7 m and 100 m approximately for seed and pollen dispersal
distances, respectively. A distance of 7 m was the mean distance
between adult trees and collected seeds below these crowns in
this study. The average distance between trees within neigh-
borhoods is 100 m. For the prior of the number of unsampled
male parents, we assumed that most of the unsampled trees
were located in forest fragments because exhaustive sampling
is more difficult in this habitat. Because there were 13 unsam-
pled trees from this habitat, a prior lognormal distribution
with mean p 20 and variance p 0.5 was used. To restrict the
number of potential female parents of each progeny, the pop-
ulation of possible maternal parents was limited to adult in-
dividuals within a neighborhood with a radius !500 m, in
view of the large seed size. The Markov chains converged
(autocorrelation values ! 0.1) after 250,000 iterations, with a
burn-in interval of 10,000 iterations and a thinning interval
of 100 iterations. When the iterations were finished, the most
probable genealogy was calculated using the MasterBayes
modeP function. From this genealogy, the paternity and ma-
ternity assignments that had probabilities higher than 0.8 were
selected. From these assignments, the distribution of pollen-
dispersal distances was calculated, and the maternal origin and
the distance traveled by seeds collected below tree crowns was
determined. Pollen-dispersal events were drawn on a map. To
study the differences in pollen- and seed-dispersal distances
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between the progeny in each habitat, the distances were
grouped according to the habitat of the seed or seedling, and
the average values and standard errors were calculated by
habitat.
The average values and 95% confidence intervals of the
parameters (l and the number of unsampled males) were cal-
rameters (Hadfield et al. 2006). To determine whether the dis-
persal parameters (l F and lM) differed between developmental
stages (seeds vs. seedlings), progeny groups composed of both
seeds and seedlings (9 maternal trees) were chosen for a total
of 66 seedlings and 70 seeds. Because of the reduced sample
size, the values of N ⫺ n, E1, and E2 were fixed to those ob-
tained for the entire population, and only the l parameters
were estimated. Because this comparison did not result in sig-
nificant differences (see “Results”), each of the parameters
(l F, lM, N ⫺ n, E1, and E2) was estimated for the full set of
progeny (seeds ⫹ seedlings) for each habitat condition, and
the average values, standard errors, and 95% confidence in-
tervals were compared to determine the differences between
habitats in the magnitude of pollen and seed dispersal.
In this study, the parameter lM served as an auxiliary pa-
rameter or nuisance parameter that allowed for the pollen-
distribution parameter to be estimated in each habitat. The
sampling design for the progeny (under tree crowns) did not
allow the complete measurement of seed dispersal. For C. ni-
caraguensis, we assumed that most of the progeny found under
a given tree crown were descended from that tree, and our
data supported this assumption (see “Results”). However,
some cases of mismatch between the nearest tree and progeny
created uncertainty regarding their maternal origin. This un-
certainty may be taken into account by estimating maternity
as an exponential function with the dispersal restrictions men-
tioned above.
Results
Genetic Variability
Eight loci were analyzed using the primers developed by
Dayanandan et al. (1999) and Vinson et al. (2005). One of
these loci (Cg16) was found to be monomorphic. The number
of alleles and genetic diversity parameters for each locus and
developmental stage are shown in table 2. The adult and prog-
eny samples showed similar degrees of variability (Ne p
2.55 and 2.56 in adults and progeny, respectively; He p
0.417 and 0.452 in adults and progeny, respectively) and low
inbreeding values, significant in the progeny group (F p
0.056 and 0.049 in adults and progeny, respectively). These
values can be explained partly by the presence of null alleles,
but there was also strong evidence of selfing in one of the
sampled progeny groups (see below), and positive and signif-
icant inbreeding values were observed in four out of seven loci
in progenies (table 2), which might indicate the presence of
inbreeding. Considering the diversity of all of the loci, the
exclusion probability of one progenitor without knowing the
other (e.g., the exclusion probability of maternity without
knowing paternity) was 0.744, and the exclusion probability
of one progenitor given the genotype of the other (e.g., exclu-
sion of paternity) was 0.924. However, this exclusion prob-
 LOBO & JIMÉNEZ—VARIATION OF GENE FLOW IN CARAPA NICARAGUENSIS 181

Table 2 persed near the maternal tree in all habitats (5–10 m; table 4).
Nevertheless, the possibility of seed movement to locations
Genetic Variability in Adults and Progeny of a Carapa
nicaraguensis Population in Costa Rica
beneath the crowns of trees other than the maternal tree was
supported by the observation of mismatch between progeny
Group and locus Na Ne Ho He F and nearest tree genotypes of 15.9% of the progeny. The fre-
Adults: quency of this mismatch at two or more loci was 8%. These
cg-6 4 1.57 .364 .365 .004** frequencies are too high to be explained by the calculated
cg-5 10 6.85 .795 .854 .069** genotyping error rates, especially because not all genotyping
cg-01 6 1.99 .432 .499 .134 errors lead to excluding true maternities. The frequency of
cg-06 4 1.52 .330 .342 .038 mismatch between progeny and the genotype of the nearest
cg-7 6 1.97 .432 .492 .122 tree at one or more loci was highest in forest fragments (28%),
cg-17 2 1.01 .011 .011 ⫺.006
intermediate in gallery forest (16%), and low in isolated trees
cg-11 8 4.48 .750 .777 .035
Mean 5.12 2.55 .389 .417 .056
(5%).
SE 1.06 0.72 .103 .110 .019
Progeny: Comparison of Pollen Dispersal between Habitats
cg-6 5 1.72 .376 .418 .100**
cg-5 13 6.47 .794 .846 .060* The estimated effect of distance on paternity probability
cg-01 10 2.40 .583 .584 .002** showed the most extensive pollen dispersal in the forest frag-
cg-06 5 1.70 .409 .411 .006 ment progeny, for which the average pollen-dispersal distance
cg-7 10 2.38 .588 .581 ⫺.013** based on the paternity assignments was ∼808 m (table 3).
cg-17 2 1.04 .036 .040 .115* Pollen dispersal was much more limited in gallery forest and
cg-11 10 3.81 .680 .737 .078 isolated trees (34.3 and 32.7 m, respectively). The estimated
Mean 6.62 2.56 .433 .452 .049* number of unsampled pollen donors was smaller in forest frag-
SE .08 .03 .005 .006 .001 ments (7.10) than in gallery forest and isolated trees (14.1 and
Note. The diversity parameters are shown by locus with their 10.5, respectively), although the differences among habitats
standard errors. Samples sizes are 88 adults and 364 progenies. Na p were smaller than the confidence intervals of the estimates.
average number of alleles/locus; Ne p effective number of alleles per We obtained 137 paternity assignments with probability
locus; Ho and He p observed and expected heterozygosity; F p in- greater than 0.8. The pollen-movement patterns that were in-
breeding coefficient. ferred from the paternity assignments are summarized graph-
* P ! 0.005.
ically in figures 1 and 2. Paternity assignments in the 0–50 m
** P ! 0.0001; Ho: F p 0.
distance range are much more frequent in the progeny of iso-
lated trees and gallery forest trees (81% and 89%, respectively)
ability must be weighted by the genotyping error estimates of than in the progeny of forest fragment trees (6.0%; fig. 2). The
0.02 per locus for type I errors and 0.015 per locus for type frequency of dispersal events among nearby fragments (225–
II errors. According to equation (1) of Wang (2004), the error 275 m) was high (33%) in the latter group. Long-distance
probability would be 0.066 in determining a heterozygote ge- (1500 m) pollen-dispersal events were rare but did occur in
notype and 0.03 in determining a homozygote genotype. between trees located in forest fragments and trees located in
other habitats. Fifteen long-distance pollen-dispersal events
Effect of Adult-Progeny Distance on the were inferred between different forest fragments or between a
Probability of Paternity forest fragment and an isolated tree or gallery forest tree. Evi-
dence of selfing was found in a single isolated tree located in
The 95% confidence intervals (CIs) of the l parameter es-
IT1 (fig. 1), all of whose progeny (a mixture of seeds and
timates for seedlings and seeds overlapped; therefore, seedlings
seedlings) were products of selfing with a probability 10.8
growing below a given tree crown do not show different dis-
according to the paternity assignments.
persal rates than seeds found in the same place. In view of this
In the gallery forest located in the center of study area (GF),
finding, we combined the genetic data for seedlings and seeds
seeds and seedlings were fertilized exclusively by pollen from
from the same source habitat.
the same neighborhood. The same fact was observed in two
The probability of maternity or paternity declined signifi-
neighborhoods of isolated trees surrounded by pastures (IT1
cantly as the distance between the adult and progeny increased.
and IT2). Movement of pollen within neighborhoods was also
The rate of this decline differed for female versus male pro-
frequent in the isolated trees that were nearest to forest frag-
genitors; distance had a much greater effect on the probability
ments in the western part of the study area (IT3; 54% of the
of maternity (table 4).
events) and in the forest fragment in the western part of the
study area (FF4; 54% of the events). Notably, FF4 and IT3
Variation in the Maternal Provenances of Seedlings and are close to each other and form part of a small watershed
Seed Found under Tree Crowns with high local densities of Carapa nicaraguensis.
The comparison of the 95% CI of the l parameters for each
habitat showed significant differences between habitats (tables Discussion
3, 4). The effect of distance on maternity probability was high-
est for isolated trees, intermediate for trees in gallery forest, In the study area, differences in the population structure of
and lowest for trees in forest fragments. Most seeds are dis- Carapa nicaraguensis were reflected in the varied effect of spa-

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182 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Table 3
Parameters of the Exponential Distributions for Pollen Dispersal, Estimated from the Full Probability Model of
Genealogical Reconstruction under Three Different Habitat Conditions
Effect of distance on paternity Forest Gallery Isolated
probability fragments forest trees
l parameter .00031 (.00040) ⫺.013 (.0024) ⫺.013 (.0032)
95% confidence limits ⫺.0005, .0010 ⫺.018, ⫺.0083 ⫺.020, ⫺.0084
Mean dispersal distance (m) 808.8 (108.1) 34.3 (7.4) 32.7 (6.3)
Number of unsampled males (SE) 7.10 (3.02) 14.1 (5.20) 10.5 (4.32)
95% confidence limits 2.72, 14.26 5.59, 25.5 4.01, 20.97
Note. The means and standard errors (in parentheses) of pollen-dispersal distances estimated from paternal
assignments with posterior probabilities 10.8 are also shown.

tial distance on seed- and pollen-dispersal probabilities. The
progenies obtained in the high-density population located in
an isolated gallery forest (GF), as well as the progenies of
isolated trees (IT), showed high probabilities of short-distance
pollen dispersal, and the maternal origin was almost always
the nearest tree. The values of the l dispersal parameters and
the distribution of pollen-dispersal distances for the gallery
forest (GF) population indicated that this population is ge-
netically isolated from those in nearby neighborhoods. This
result can be explained by the high density of adults within
the GF neighborhood and the degree of isolation enforced by
the surrounding agricultural pasturelands. The limited seed
and pollen dispersal of IT trees can be explained by the loss
of forest cover and the consequently limited arrival of seed-
and pollen-dispersal agents. The effects of fragmentation on
pollen quality and quantity in plants have been reported in
previous studies (for reviews, see Ghazoul 2005; Aguilar et al.
2008). Changes in pollinator abundance and composition have
also been reported for isolated trees (Dick 2001; Aizen and
Feinsinger 1994; Quesada et al. 2003). Some studies have
shown increased pollen-flow distances in fragmented habitats
(Aldrich and Hamrick 1998; Dick 2001; White et al. 2002).
We suggest that patterns of pollen flow in isolated trees are
complex and species specific. These patterns depend on the
specific pollinator taxa, their responses to open habitats, and
the spatial arrangement of other trees surrounding the isolated
tree. In this study, for example, pollen movement between for-
est fragments and isolated trees was asymmetric. Isolated trees
in pastures and gallery forest trees donated pollen to distant
trees, but the progeny produced by isolated maternal trees were
mostly fertilized by nearby trees. This pattern is difficult to
explain without more information about pollinator compo-
sition and behavior in this species. It could be proposed that
larger traveling time/cost leads to longer stay of pollinators in
a patch of isolated trees, according to the optimal foraging
theory. Prolonged visitation within the patch decreases the
fraction of immigrant pollen and increases the fraction of pol-
len emigration because the pollen carried by the bee is almost
completely replaced with pollen of the isolated tree. The higher
frequency of nests of insects in forest fragments compared to
isolated trees can reinforce this pattern. Whatever the mech-
anism, this study confirms genetic connectivity between iso-
lated trees and forests, an observation made in previous studies
of tropical tree species in fragmented landscapes (Chase et al.
1996; Aldrich and Hamrick 1998; Fuchs and Hamrick 2010;
Lander et al. 2010).
We propose that in the gallery forest located in the swampy
area (GF) and in one of the forest fragments (FF3), the high
local density of C. nicaraguensis may reinforce local pollen
dispersal. The small insects that pollinate C. nicaraguensis may
respond to the greater availability of pollen per unit area, in-
creasing the time and energy spent on pollen collection within
individual trees and reducing the frequency of movement be-
tween trees. In GF, concentrated pollinator foraging within the
forest fragment reinforces the limited levels of external pollen
flow caused by the surrounding matrix. This pattern has been
proposed in many experimental studies of insect-pollinated
plants (Levin and Kerster 1969; Schmitt 1983; Harder 1990;
Goodell et al. 1997; Richards et al. 1999). Genetic analyses
of insect-pollinated species have demonstrated that local tree
density is important in determining mating distances and the

Table 4
Distance and Frequency of Seed Dispersal Events below Different Tree Crowns under
Three Different Habitat Conditions
Effect of distance on maternity Forest Gallery Isolated
probability fragments forest trees
l parameter ⫺.017 (.0037) ⫺.101 (.013) ⫺.346 (.165)
95% confidence limits ⫺.026, ⫺.012 ⫺.130, ⫺.076 ⫺.718, ⫺.112
Mean dispersal distance (m) 9.9 (1.7) 7.1 (.7) 4.8 (.4)
Mismatch frequency between progenies
and nearest tree (%) 28 16 5
Note. The l parameter is the effect of distance on the probability of maternity. The means and standard errors
(in parentheses) of seed-dispersal distances estimated from maternity assignments with posterior probabilities 10.8.
Frequency of genetic mismatch between progeny and the nearest maternal tree (maternity exclusion) is also shown.

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 LOBO & JIMÉNEZ—VARIATION OF GENE FLOW IN CARAPA NICARAGUENSIS 183

Fig. 2 Frequency of paternity assignments according to the distance between the progeny and the assigned parent. Black, gray, and white
bars represent progeny in forest fragments (FF), in gallery forest (GF), and under isolated trees (IT), respectively. The frequencies are calculated
on the basis of 40 (FF), 49 (GF), and 65 (IT) total assignments with a probability 10.8.

diversity of pollen received by maternal trees (Stacy et al. 1996;
Garcı́a et al. 2005; Oddou-Muratorio et al. 2006).
Matings in forest fragments show a high probability of pol-
len dispersal at distances greater than 200 m (fig. 2). This fact
is consistent with the conclusions of Cloutier et al. (2007) in
a study of Carapa guianensis in continuous forests in Tapajós,
Brazil. Based on microsatellite markers (including loci that
were analyzed in the present study), these authors concluded
that the average distribution of pollen-dispersal distances in
the population was within the 159–252 m interval. The av-
erage pollen-dispersal distance decreased following selective
logging (which reduced the density of adults), although not
significantly. These authors found no differences in the levels
of outcrossing or biparental inbreeding after logging. However,
their pollen-dispersal estimates were calculated using indirect
methods based on the TwoGener procedure (Austerlitz and
Smouse 2001), which determines the dispersal parameters that
best fit the genetic differentiation coefficient between the male
gametes (Fft) of different maternal progeny. The accuracy of
such estimates depends on knowledge of the local effective
density of adults (Austerlitz and Smouse 2001). In our study,
the pollen-dispersal distances were estimated based on direct
paternity and maternity assignments (i.e., genealogical recon-
struction) and joint estimation of the effect of distance on these
assignments (Hadfield et al. 2006). Paternity assignments have
the advantages of (i) allowing the detection of individual pol-
len-dispersal events and the distance associated with each
event, making it possible to study the variation in dispersal
distances among individuals and populations, and (ii) using
all available sources of information, including adult trees that
lack progeny but are potential pollen donors. The requirement
of exhaustive sampling of reproductive individuals within
plots, indicated as a disadvantage of paternity assignment
(Sork and Smouse 2006), is solved in this study with the es-
timation of the number of unsampled sires using the methods
of the Masterbayes software.
The detection of a highly selfing isolated individual reveals
the presence of self-compatible individuals in a population that
has a predominantly outcrossed mating system. Earlier studies
have shown the possibility of selfing in species of the genus
Carapa, although the mating system is predominantly out-
crossed (Doliguez and Joly 1997; Cloutier et al. 2007). Do-
liguez and Joly (1997) found that outcrossing rates decreased
after logging in populations of Carapa procera in French Gui-
ana, but this phenomenon was not observed in populations of
C. guianensis (Cloutier et al. 2007). The presence of a highly
selfing individual in our study may be explained by genetic
variability in the self-incompatibility system or by flexibility
in the expression of this system (Levin 1996; Lipow and Wyatt
2000). Certain spatially isolated individuals, like the selfing
individual detected in our study population, may produce
selfed progeny as a result of a higher probability of geito-
nogamy, owing to its isolation from other trees and optimal
foraging strategies of pollinators.
In regard to the maternal provenance of seeds and seedlings,
the rapid decrease in maternity probability with distance and
the inability to rule out nearby maternal sources for most prog-
eny indicate that most seeds fall and germinate under the
crown of the maternal tree. However, the maternal exclusion
of certain progeny, particularly in low-density conditions in
forest fragments, indicates that dispersal away from the ma-
ternal tree to locations beneath conspecific trees is possible.
These dispersal events were less frequent in the gallery forest
and were not detected in isolated trees. The seed-dispersal

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184 INTERNATIONAL JOURNAL OF PLANT SCIENCES
mechanisms may be nonbiological (e.g., by gravity or water),
although the presence of displaced seeds under the crowns of
conspecific trees can be better explained by the foraging pat-
terns of animal dispersers. Scatter-hoarding rodents have been
identified as the seed dispersers for Carapa. In the study region,
these rodents are primarily Agouti paca and Dasyprocta punc-
tata, although other rodents can also be dispersal agents
(McHargue and Hartshorn 1983). Carapa seeds are quickly
removed by scatter-hoarding rodents from their positions un-
der the crown (Forget 1996) and eaten or hidden a few meters
away, although occasional dispersal events at more than 20 m
have been observed (Guariguata et al. 2002). Differences in
dispersal distances between forest fragments and other habitats
may be due to an effect of forest fragmentation on seed-move-
ment distance, possibly caused by reduced numbers or behav-
ioral changes in seed-dispersal agents. Forget and Jansen
(2007) found that the hunting of large rodents reduced the
dispersal of C. procera seeds, whereas Guariguata et al. (2002)
found no difference between forest fragments and continuous
forests in the removal rate of C. guianensis seeds. Genetic
analyses of seedlings of other tropical tree species primarily
dispersed by birds (Hardesty et al. 2006; Sezen et al. 2009)
have revealed that proximity does not determine parentage and
that long-distance seed-dispersal events are frequent in tropical
tree species that are dispersed by vertebrates.
Our findings show the importance of tree populations in
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