Facilitation influences patterns of perennial species abundance and richness in a subtropical dune system
Facilitation influences patterns of perennial species abundance and richness in a subtropical dune system
Cecilia E. S. Dalotto 2
Rafael B. Sühs 2
Michele S. Dechoum 1
Francisco I. Pugnaire 0
Nivaldo Peroni 2
Tânia T. Castellani 2
Associate Editor: Katharine J. M. Dickinson
0 Estación Experimental de Zonas Áridas , EEZA-CSIC, Ctra. de Sacramento s/n, 04120 La Cañada , Almería , Spain
1 Programa de pós-graduação em Biologia de Fungos, Algas e Plantas, Universidade Federal de Santa Catarina, CEP 88040-900 , Florianópolis, Santa Catarina , Brazil
2 Programa de pós-graduação em Ecologia, Universidade Federal de Santa Catarina, CEP 88040-900 , Florianópolis, Santa Catarina , Brazil
Positive interactions in plant communities are under-reported in subtropical systems most likely because they are not identified as stressful environments. However, environmental factors or disturbance can limit plant growth in any system and lead to stressful conditions. For instance, salinity and low nutrient and water availability generate a gradient of stressful conditions in coastal systems depending on distance to shore. In a tropical coastal system in SE Brazil, we aimed to assess whether Guapira opposita, a shrub common in restinga environments, acted as nurse involved in ecological succession and which factors influenced its facilitation process. We sampled perennial species above 10 cm in height under the canopy of 35 G. opposita individuals and in neighbouring open areas. Shrub height, canopy area and distance to freshwater bodies were measured in the field, and distance to the ocean was obtained from aerial images. In addition, we measured the distance to the closest forest patch as a potential source of seeds. Plant abundance and species richness were higher under the canopy of G. opposita than in open areas. Facilitation by G. opposita was mainly determined by shrub height, which had a positive relationship with woody and bromeliads abundance and species richness while there was no relationship with the other factors. Overall, our data evidence that tropical environments may be highly stressful for plants and that nurse species play a key role in the regeneration of restinga environments, where their presence is critical to maintain ecosystem diversity and function.
Guapira opposita; perch effect; plant community; plant-plant interactions; positive interactions; succession; vegetation dynamics
The process of ecological succession refers to directional
changes in the composition of species and community
structure over time
. In a successional
process guided by facilitation, some species are
central to the establishment of others by improving or
mitigating conditions, which allows less tolerant
species to establish
(Connell and Slatyer 1977)
. This model
© The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company.
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is properly cited.
of succession, centred on focal individuals, is known as
(Yarranton and Morrison 1974)
. From these
nuclei, some shrub or tree species can recruit different
individuals under their canopies and expand to form
large patches of continuous vegetation, affecting the
composition of future forests
(Yarranton and Morrison
1974; Slocum 2001)
Shrubs and trees that benefit other plant individuals
below their canopy, in both early or late successional
stages, are called nurse or facilitator species
et al. 1963)
. The benefit provided by these species occurs
through the mitigation of environmental conditions and
changes in distribution of resource availability, which
can affect local species richness and plant abundance
and alter the regeneration dynamic of the whole
(McIntire and Fajardo 2014)
. In environments
under high abiotic stress, such as coastal systems, nurse
species allow less stress-tolerant species to become
established, increasing local abundance and richness
(Armas and Pugnaire 2009; Cavieres et al. 2014)
Some specific plant characteristics can improve the
facilitation–nucleation process. For instance, species
with large crowns and dense canopies are often good
(Arantes et al. 2014)
, because they reduce
incident radiation and soil temperature, as well as
promote an increase in nutrient availability
Brooker et al. 2008)
. In addition, species with fleshy fruits
attract seed dispersers and act as perches, increasing
seed rain under their canopies
(McConkey et al. 2012)
Thus, shrubs with these traits can improve local
conditions and receive propagules via the attraction of animal
dispersers, increasing seedling recruitment under their
. In the potential nursing effect,
distance to seed sources is an important factor as
dispersal (hence seed availability) tends to decrease with
(Martínez-Garza et al. 2009)
. Therefore, the
shorter the distance to seed sources, the greater the
number of propagules arriving.
The main factors that influence facilitation under
shrubs in coastal ecosystems are linked to
environmental stress, such as temperature, wind and salinity, or the
scarcity of resources, such as lack of water or nutrients
(Maestre et al. 2009)
. In stressful environments, the
frequency of facilitative interactions is expected to
predominate over competitive interactions
Callaway 1994; Callaway 2007)
. Thus, stressful coastal
environments offer good conditions to assess
facilitation processes, since salinity and low soil water
availability create gradients of stress that tend to decrease
away from the ocean and near to freshwater bodies,
respectively. These two gradients may have different
directions and at times cancel each other, but
individually they could potentially match the stress-gradient
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(SGH; Bertness and Callaway 1994)
with the reduction of physical severity, facilitative
interactions are expected to become less important than
competitive interactions in structuring plant
(Bertness and Callaway 1994; Pugnaire and Luque
2001; Callaway 2007; Callaway and Pugnaire 2007)
Brazilian restinga environments comprise a diverse
group of vegetation types along the Brazilian coast that
belong to the Atlantic Forest biome. These vegetation
types have developed on sandy, poor soils of marine,
alluvial or wind origin. The plant communities are diverse
and dominated by stress-tolerant species that often
provide adequate conditions for the germination and
growth of less stress-tolerant species
Environmental severity in restingas is linked to
nutrient limitation, high radiation, low soil water availability,
strong winds and burial by sand
colonizer species often act as facilitators, with an
important role in ecological succession and in the transition from
an herbaceous to an arboreal physiognomy
et al. 2015)
. Therefore, it could be expected that in
restinga environments woody species establishment would
be higher under the canopy of stress-tolerant shrubs
than in the herbaceous vegetation matrix or in bare sand.
In southern Brazil, Guapira opposita (Nyctaginaceae) is a
common species in coastal dune systems
is considered a nurse species
(Castanho et al. 2012)
its role in community composition and dynamics has not
Information on facilitation in tropical and
subtropical environments is still limited, despite its importance
to understand how succession occurs in restingas.
Thus, our main objective was to understand the role of
G. opposita in a restinga environment, and specifically
(i) evaluate whether richness and abundance of woody
species under the canopy of G. opposita differed from
areas dominated by herbaceous vegetation; i.e., its
facilitation effect; (ii) assess how G. opposita
morphology, distance to the ocean and freshwater bodies
influence facilitation; and (iii) evaluate the influence
of distance to forest patches on the facilitation effect.
We hypothesized that (i) abundance and richness of
woody species will be higher under G. opposita shrubs
than in surrounding areas dominated by herbaceous
vegetation; (ii) facilitation will be more intense under
larger and taller G. opposita individuals than under
smaller individuals; (iii) facilitation will depend on
environmental stress, which increases with distance
to freshwater bodies and with proximity to the ocean,
in parallel to gradients of water availability and
salinity; and (iv) proximity to forest patches will positively
influence plant establishment under the canopy of
The study was conducted in Dunas da Lagoa da Conceição
Municipal Park (DLCMP), a dune system on the
eastern coast of Santa Catarina Island, Florianópolis, Brazil
(27°37′33″S – 27°37′53″S, 48°27′28″W – 48°27′08″W).
The climate type is Cfa (mesothermal moist) according
to the Köppen–Geiger climate classification. Mean
temperature ranges from 26 °C in summer to 16 °C in winter,
with an annual mean of 20 °C
. Rainfall is
well distributed throughout the year but is more intense
during the summer months, with an annual average of
. Interspersed within the
moving and semi-fixed sand dunes there are permanent
freshwater bodies in dune slacks. These freshwater
bodies are temporarily flooded in rainy months (in the
summer) by groundwater that emerges naturally from
below the surface
(Beduschi and Castellani 2013)
plant community is typical for restinga and ranges from
herbaceous to shrubby physiognomy, including larger
shrubs in vegetation bands further from the ocean. Most
of the system is dominated by an herbaceous-subshrub
matrix with either isolated or densely clustered shrubs
Guapira opposita is a widely distributed species in
Brazil, where it occurs in the Atlantic Forest, Amazonian,
Caatinga and Cerrado domains (
Patrícia et al. 2000
the south-east, its distribution is restricted to
rainforests along the Atlantic coast and restingas. The
species is highly polymorphic (e.g. it can be 1 to 25 m tall),
which is directly influenced by the environment where it
occurs. In shallow or rocky soils it assumes a dwarf size;
in restinga environments its leaves are slightly shorter
and more coriaceous than in the rain forest. Ripe fruits
are fleshy and red to purple, and attract birds that act as
dispersers. It may be abundant in restingas, sometimes
forming dense thickets on the sandy, slightly undulating
terrain near the beach
The sampling area comprises a section of dunes
inside the DLCMP, between 50 and 600 m from the
ocean. Individuals of G. opposita are common in the
area as isolated individuals or in small nuclei with
individuals of Clusia criuva (Clusiaceae), Myrcia
palustris (Myrtaceae) and Ocotea pulchella (Lauraceae).
Nuclei vary in size (1.5–5 m2) and increase over time
(C. E. S. Dalotto, pers. comm.). Forest patches close to
arboreal restingas sharing similar plant species can
also be found. These patches are very similar in size
and occupy 2 ha on average. Shallow, subjected to
temporary flood are common, especially in periods of
Thirty-five G. opposita shrubs, at least 20 m apart from
each other, were randomly selected and georeferenced.
For each shrub, we measured canopy diameter to
calculate the area as that of an ellipse, as well as height and
distance to the closest freshwater body. Under the
canopy of each shrub, we sampled all individuals of woody
species with a minimum height of 10 cm, as well all
individuals of bromeliad species. Plants were identified to the
species level or, when not possible, to the genus level.
We randomly selected an area similar in size and near
to every sampled shrub (open areas) and all bromeliads
and woody individuals at least 10 cm tall were sampled.
Then, using coordinates obtained in the field, the
distance from each shrub to the ocean and to the closest
forest patch were calculated using satellite images from
Google Earth Pro 7.1.2.
We used generalized linear models (GLMs) to compare
abundance and richness of woody species and
bromeliads in the two conditions (under the canopy of
G. opposita individuals and in open areas). In each model, the
explanatory variable ‘condition’ was considered a fixed
effect. A Poisson distribution with a logarithmic function
was used to relate response (species abundance and
richness) and the explanatory variable.
To evaluate the strength of facilitation exerted by the
shrub in relation to the adjacent area, the relative
interaction index (RII) was used
(Armas et al. 2004)
B - Bo
RII = w
Bw + Bo
were Bw is the number of individuals or species growing
under the influence of G. opposita and Bo is the number
of individuals or species growing outside the shrub
influence (open areas). The resulting values can vary from −1
to 1, where positive values show facilitation and
negative values mean competition
(Armas et al. 2004)
We used GLMs to test how G. opposita facilitates plant
abundance and species richness under the canopy. The
explanatory variables used as fixed effects were height
and canopy area, distance to the ocean, to the closest
forest patch and to the closest freshwater body. Model
selection was based on the Akaike information criterion (AIC).
Statistical analysis were performed and figures were built
using the packages ‘car’, ‘MASS’ and ‘ggplot2’ of the
statistical software R version 2.3.1 (R Core Team 3.2.5).
The 35 sampled G. opposita individuals ranged in
height between 0.8 and 3 m (mean 1.84 ± 0.11 m) and
had a canopy area between 0.24 and 9.9 m2 (mean
3.74 ± 0.52 m2). These individuals were found 55 to
600 m from the ocean (mean 249.37 ± 21.68 m) and 1
to 25 m from a freshwater body (mean 5.74 ± 1.03 m).
The distance to the closest forest patch varied from 95
to 710 m (372.51 ± 31.23 m). Relative interaction index
values were positive both for abundance (0.28 ± 0.09)
and richness (0.22 ± 0.08), showing a facilitation effect
of G. opposita in this restinga environment.
Out of a total of 770 individuals, 537 (69.7 %) were
recorded under G. opposita and 233 (30.3 %) in open
areas. Of the 27 species recorded, 17 (62.9 %) occurred
exclusively under the shrub canopy and 10 (37.1 %) were
present in both conditions. Only four species (14.8 %)
were more abundant in open areas but none of them
were exclusively in this situation. Trees were the most
frequent life form, followed by shrubs and subshrubs. Most
of the species are typical of restinga with a shrubby
vegetation physiognomy [see Supporting Information—
Table S1]. Abundance and richness of woody plant and
bromeliad species were higher under G. opposita
canopies than in adjacent open areas (Table 1). Mean
abundance and species richness under G. opposita canopies
more than doubled that of open areas (Table 1).
With regards to RII values, models that best fit the
data were those that included shrub height, distance
to freshwater bodies and distance to forest patches
(Table 2) [see Supporting Information—Table S2].
However, only shrub height was significant, explaining
48 % and 65 % of variation in abundance and richness,
respectively (Fig. 1) [see Supporting Information—
Table S2]. There was a positive relationship between
shrub height and abundance of individuals and species
richness (Fig. 1). The variables canopy area and distance
to the ocean were not included in the best fit models.
Our results show that both abundance and richness of
woody species and bromeliads are higher under the
canopy of G. opposita shrubs than in adjacent open areas.
They also confirm that facilitation provided by this
species is stronger under taller shrubs. Despite the fact that
distance to freshwater bodies and distance to forest
patches were not significant in the best fit model, the
combined effect of these variables with shrub height best
explained data variation, suggesting gradients not strong
enough to influence interaction intensity. The canopy
area of G. opposita plants and distance to the ocean were
not relevant for facilitation under our shrub species.
Evidence of a positive interaction between nurse
plants and their understory species has been widely
reported in several ecosystems around the world, most
notably in dry and high-elevation habitats
and Callaway 2006; Zhao et al. 2007; Pugnaire et al.
2011; Schöb et al. 2012; Semchenko et al. 2012; Cavieres
et al. 2014)
. Reports of facilitation in tropical and
subtropical ecosystems are far less frequent. There are,
however, reports from tropical grasslands
, high mountains
(Anthelme et al. 2015)
and restinga environments
(Castanho et al. 2012)
a low availability of published data concerning the
tropics may be related to the formulation of the SGH, which
led to search for positive interactions in stressful
(Bertness and Callaway 1994)
. However, in
subtropical coastal systems there may be significant
levels of plant stress related to nutrient limitation, low
soil water availability and/or high salinity levels
which would make facilitation important for plant
In our coastal system, despite abundant rainfall and
high mean annual temperature, different stress
factors lead to a rather demanding environment, such as
high radiation, high salinity levels, desiccating winds
and low nutrient availability
(Castanho et al. 2015)
Therefore, the higher plant abundance and species
richness recorded under the canopy of G. opposita can be
explained mainly by shading which, along with lower soil
temperatures, organic matter and nutrient accruement,
favoured plant establishment and niche creation
et al. 1997; Bruno et al. 2003; Schöb et al. 2012)
also keeps temperatures close to the plant physiological
equilibrium, as temperatures above 50–60 °C causes
, reducing evaporation
and keeping better plant water balance
(Pugnaire et al.
. Some of these changes may affect interaction
intensity by, e.g., increasing competition among
beneficiary species (
Schöb et al. 2014
), but the overall effect of
the canopy would allow the presence of more
individuals and increased species richness under the canopy of
the facilitator species
(Moro et al. 1997; Castanho et al.
2012; McIntire and Fajardo 2014)
Facilitation provided by G. opposita shrubs is higher
when shrubs are taller, presumably by two factors—the
darker shade they cast and the perch effect. Taller plants
are more attractive to seed dispersers
(Debussche et al.
and seed rain is larger under perches
(Pausas et al.
, while nurse shadow favours seed germination
and seedling establishment. The most abundant woody
species found under the canopy of G. opposita have
fleshy fruits dispersed by birds—C. criuva, G.
brasiliensis, M. palustris, O. pulchella and G. opposita as
predicted as consequences of the perch effect
et al. 2014)
. Species in the Lauraceae, Myrtaceae and
Primulaceae were found exclusively under G. opposita
[see Supporting Information—Table S1], in
accordance with previous reports where these species were
described as typical of arboreal restinga physiognomy
and rarely found in herbaceous restinga environments
). This shows that G. opposita facilitates
preferentially the establishment of tree species that
otherwise do not have the capacity to recruit in exposed
In addition, most species found under G. opposita are
typical in arboreal restingas (
) and were
more abundant in forest patches than in the herbaceous
matrix. This is an evidence that, although distance to
forest patches was not significant in the best fitted model,
it contributes to the observed results. In the studied
system, forest patches act as seed sources and isolated
shrubs (such as G. opposita plants) function as stepping
stones for seed dispersers in an herbaceous matrix.
Some 25 % of the individuals sampled under the
canopy of G. opposita were not found outside this influence
[see Supporting Information—Table S1], which shows
the critical contribution of this shrub species to local
biodiversity. For instance, the bromeliad Vriesea fribugensis
is a wind-dispersed species that thrives in environments
with diffuse light and which allow water to accumulate
in its leaves
. By contrast, two of the three
most common species found in open areas (Baccharis
dracunculifolia and Dodonaea viscosa) are
anemochorous shrubs and tolerate environments of extreme
Distance to freshwater bodies may be a limiting
factor in restinga environments as soil humidity can limit
the development of plants
(Wilson and Sykes 1999)
Therefore, it could be expected a facilitation gradient
since water availability decreases with increasing
distance to freshwater bodies, in agreement with the SGH
(Bertness and Callaway 1994)
. However, there was not a
direct relationship between distance to freshwater bodies
and facilitation under G. opposita, which implies that soil
humidity is not a limiting resource for the studied system.
In fact, short distances to freshwater bodies could also
be considered as a stressor for the local plant
communities due to (un)predictable flooding
(Scarano et al. 1997)
These mixed effects of distance to freshwater bodies
must have neutralized its relevance on the best fit model.
Salinity, here represented by distance to the ocean as
a proxy, is also a stress factor in coastal environments
. Contrary to our expectations, it did not
determine abundance of individuals under G. opposita
(Castanho et al. 2012)
, as the 600 m distance
to the ocean seems not to be strong enough to notice
the effects of salinity on plant establishment.
We conclude that G. opposita shrubs increased
richness and abundance of other woody and bromeliad
species under its canopy compared to the
surrounding herbaceous matrix. The main factor determining
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facilitation intensity was individual shrub size (shade
and perch effect) which positively influenced native
species abundance and richness. Also, our data show that
shrub canopy area, distance to forest patches, distance
to freshwater bodies and distance to the ocean (as a
proxy for salinity) were not important factors influencing
facilitation. To sum up, subtropical environments may be
stressful for plants and nurse species play a key role in
the regeneration of restinga environments, where their
presence is critical to maintain ecosystem diversity and
Sources of Funding
This work was funded by the Brazilian government
(CAPES/CNPq). C.E.S.D. and R.B.S. were recipient of
scholarships from the Ecology Postgraduate Program of the
Federal University of Santa Catarina (UFSC). F.I.P. and
M.S.D. were supported by the CAPES/CNPq ‘Science
without Borders’ Program, through the project ‘Plant
interactions and community dynamics in tropical, seasonal
systems’ (ref. UFSC 114A-2013).
Contributions by the Authors
C.E.S.D., F.I.P. and T.T.C. conceived the original ideas.
C.E.S.D., R.B.S. and M.S.D. executed the fieldwork and
analysed the data. C.E.S.D. wrote the first draft of the
manuscript with contributions of all co-authors.
Conflict of Interest
The following additional information is available in the
online version of this article—
Table S1. Total abundance of woody and bromeliad
species sampled under the canopies of Guapira opposita
(canopy) and adjacent open areas (open) in a coastal
dune ecosystem, in Florianópolis, Santa Catarina, Brazil.
Life form and occurrence in each of the restinga
physiognomies are showed—herbaceous (H), shrubby (S) and
Table S2. Statistical results of the chosen
generalized linear models (GLMs) built to explain the relative
interaction index (RII) for abundance and richness of
woody and bromeliad species sampled under the
canopies of Guapira opposita (canopy) and adjacent open
areas (open) in a coastal dune system, in Florianópolis,
Santa Catarina, Brazil. df = degrees of freedom;
dist = distance.
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