Download Plant communities at the periphery of the Atlantic rain forest

Biological Conservation 142 (2009) 1201–1208
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Biological Conservation
journal homepage: www.elsevier.com/locate/biocon
Plant communities at the periphery of the Atlantic rain forest: Rare-species bias
and its risks for conservation
Fabio Rubio Scarano *
Universidade Federal do Rio de Janeiro, CCS, IB, Depto. de Ecologia, Caixa Postal 68020, cep21941-970, Rio de Janeiro, Brazil
Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Diretoria de Pesquisa Científica, Rua Pacheco Leão 915, cep22460-030, Rio de Janeiro, Brazil
a r t i c l e
i n f o
Article history:
Received 17 September 2008
Received in revised form 15 February 2009
Accepted 21 February 2009
Available online 25 March 2009
Keywords:
Conservation priorities
Ecotone
Marginal habitats
Species commonness
Species rarity
a b s t r a c t
Initiatives that establish species rarity as an indicator of conservation priority might be biased if they disregard important evolutionary and adaptive processes taking place in lower diversity communities and
ecotones. Conservation policies regarding the Atlantic forest strongly emphasize the core formation
(i.e. the rainforest stricto sensu) rather than the marginal habitats (e.g. restingas, swamps, and high altitude campos) and species that are rare/endemic. To discuss this issue I revisit a hypothesis I have forwarded in 2002 that postulates that plant colonization of habitats marginal to the Atlantic rain forests
of the State of Rio de Janeiro was largely related to terrestrial nurse plants that originally, in the rainforest
habitat, were canopy plants such as epiphytes or hemi-epiphytes. Adaptations to water and nutrient
restrictions, typical of life in the canopy, granted success to such plants upon migration to sandy, swampy
or rocky substrates in neighbouring areas. Many such species, then, behaved as nurse plants and favoured
colonization of these more extreme habitats by a number of other rainforest species. I now review recent
evidence that corroborate this hypothesis, while examining the nature of such nurse plants. In all marginal habitats, nurse plants are often highly abundant locally and have high ecophysiological vigour,
while both widespread and endemic species are found among them. Thus, nursing effect, local abundance, and ecophysiological performance are not related to species geographic distribution or to their
spectrum of habitat preference. Paradoxically, several abundant nurse plant species have low Darwinian
fitness. These studies provoke two reflections. First, the Atlantic forest sensu lato, i.e. the core formation
plus the peripheral ones, should be treated collectively as a biodiversity hotspot, rather than the core
rainforest formation alone. Second, widespread or common species play important functional roles in
such marginal habitats and, despite their ubiquity, ecologically they might be less fit than rare/endemic
ones at the local level due, for instance, to current constraints to sexual reproduction. Thus, they should
also be targeted as conservation priorities.
Ó 2009 Elsevier Ltd. All rights reserved.
1. Introduction
Species rarity and/or endemism are often targeted by conservation initiatives. These features are intuitively associated to vulnerability and risk of extinction. At least from a probabilistic point of
view, a rare species is more likely to go extinct than a common one.
Moreover, fossil records indicate that extinct species often had
small geographic range or low local densities (McKinney, 1997).
Thus, theory predicts (Henle et al., 2004) and it is also intuitive that
a given rare species might be biologically more fragile than a common one. However, this is not necessarily true. Gaston and Kunin
(1997) compared common and rare species, based on literature,
and did not find relevant bionomical differences between them.
* Address: Universidade Federal do Rio de Janeiro, CCS, IB, Depto. de Ecologia,
Caixa Postal 68020, cep21941-970, Rio de Janeiro, Brazil. Tel.: +55 21 25626317;
fax: +55 21 25626320.
E-mail address: [email protected]
0006-3207/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2009.02.027
Buckley and Kelly (2003), for instance, did not find bionomic differences while examining pairs of common-rare species within the
same phylogenetic group, within the same locality. Curiously, despite its potential applied relevance, this topic remains short of
empirical evidences (Henle et al., 2004). Nevertheless, rarity remains more of a priority than commonness when it comes to biodiversity conservation.
Meanwhile, global change remains a major issue and forecasts
about species extinctions and ecosystem change are increasingly
pessimistic (e.g. Parmesan and Yohe, 2003; Root et al., 2003), albeit
some controversy (Botkin et al., 2007; Scarano, 2007a). Following
the probabilistic rationale mentioned earlier, it is also to be expected that rare and/or endemic species would be the main candidates for extinction. However, Holt (1990) argued that a given
species will either change in abundance, evolve or become extinct
in response to global change, and that we did not know enough
ecology, physiology and genetics to tell which species would meet
which of these outcomes. Holt’s argument still holds and there is
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F.R. Scarano / Biological Conservation 142 (2009) 1201–1208
apparently not enough empirical biological evidence to believe
that rare species might be less adaptable to environmental change.
The uprising of the biodiversity–ecosystem function paradigm
in Ecology also appeared as an indirect challenge to the notion that
species rarity should be more of a conservation priority than species ecological role. Do all species matter for the functioning of a
given ecosystem and its respective services? Are there expendable
species? Is there a role for rare species? These types of questions,
while provoking some controversy both among scientists and environmentalists (e.g. Srivastava and Vellend, 2005), have been addressed by an increasing number of researchers during the past
two decades (for a review see Kareiva and Levin, 2003).
These aspects cast doubt as to which extent species rarity
should be treated as an undisputable indicator of conservation priorities. Even if one fails to admit that there might be problems with
this indicator, it seems at least that low levels of rarity in a given
community or a common species itself should not be a priori discarded as priorities based solely on their biogeographic features.
In this paper I discuss the risks of being biased against common
species or against vegetation types with low levels of endemism
or rarity when establishing conservation priorities. I use the Atlantic rain forest complex as a case study and, therefore, I revisit a
hypothesis forwarded in Scarano (2002) that plant colonization
of habitats marginal to the rain forest sensu stricto (i.e. swamp forests, high altitude rock outcrops, and the open shrubby vegetation
of the coastal sandy plains locally called restinga) was largely related to terrestrial nurse plants that before migration, in their original rainforest habitat, were canopy plants such as epiphytes or
hemi-epiphytes. In this review I show new evidence reinforcing
the hypothesis, while focusing particularly on the nature of nurse
plants and rare plants at the marginal habitats. I sustain that the
ecological and evolutionary links between core and marginal habitats at the Atlantic forest complex demand a comprehensive treatment of the whole complex as regards conservation actions.
2. Habitats marginal to the Atlantic rain forest: a working
hypothesis
The high species diversity, high proportion of endemic and rare
species and high levels of past deforestation (only c. 12% of the original cover area remains; Ribeiro et al., 2009) of the Atlantic rain
forest have raised national and international concern with this vegetation type, which is now hailed as a biodiversity hotspot for conservation priority (Myers et al., 2000). While there is no doubt that
this should be so, it is not always clear what is meant by Atlantic
rain forest. In most cases, such as in Myers et al. (2000) or in the
Brazilian legislation that protects this vegetation type, reference
is clearly being made to only one of the various physiognomies
of a broader vegetation complex, namely the rain forest sensu stricto. Although broader definitions exist (e.g. Morellato and Haddad,
2000; Oliveira-Filho and Fontes, 2000), Rizzini (1979) has offered
the most comprehensive of all. He argued that the Atlantic forest
of Brazil should be seen as a complex formed by several plant communities, including the rain forest at its core and peripheral vegetation types such as forests (e.g. swamp forests and seasonally dry
forests) and also open vegetation types (e.g. open restingas, inselbergs and high altitude campos). Table 1 provides a brief overview
of the main characteristics of the vegetation types comprised by
the Atlantic forest complex in the State of Rio de Janeiro, where
most of the research reviewed here has been conducted. Schematic
representation of the spatial distribution of these vegetation types
can be found in Scarano (2002) and Lüttge (2006).
In the Atlantic forest complex there is a dualism between the
core rain forest and its marginal habitats. While core rain forest
presents elevated diversity, high levels of community endemism
and habitat destruction, the marginal vegetation types do not always do so (although high altitude campos are a notable exception). Thus, marginal habitats are less of a conservation priority
and, for instance, it was long before Brazil had the creation in
1998 of the Restinga de Jurubatiba National Park, the first federal
conservation unit in the country to protect a restinga ecosystem
(Barbosa et al., 2004).
Despite marked physiognomic and floristic differences, habitats
marginal to the Atlantic rain forest bear some striking structural
and functional resemblance to each other (Scarano, 2002). First,
the floristic composition of the marginal vegetation is strongly
influenced by the rain forest at the core of the complex. In the lowlands, the geologically young restingas and swamps have more
than 80% of their flora originated in the rainforest (Araujo, 2000).
The geologically older seasonally dry forest, by the coast, also
bears a high floristic similarity with the rainforest (Sá, 2006).
The high altitude campos, the geologically oldest habitat type, is
more of an exception in this sense, since it can be described as
an island of plants originated from temperate floras (Behling
et al., 2007; Ribeiro et al., 2007). However, in the rock outcrops
found here, mat species that provide substrate for fixation of other
plants are often originated in the rainforest (Ribeiro et al., 2007;
see also Martinelli, 2007; Scarano, 2007b). Second, although plant
species richness and diversity of the marginal vegetation types are
typically lower than that of the rainforest sensu stricto, species
richness is often high when compared to other vegetation types
elsewhere, particularly when one considers the intensity and/or
frequency of the abiotic limitations they are exposed to: long-term
phreatic flooding (e.g. swamps), nutrient and water shortage (e.g.
Table 1
Some of the main plant communities of the Atlantic forest complex in the State of Rio de Janeiro, southeastern Brazil. The rain forest is the predominant formation in area and
diversity, whereas the associated formations are poorer in species (adapted from Scarano, 2002).
Habitats
Location
Limiting factors
References
High
altitude
High altitude campos (including marshes and
rocky outcrops), as well as Araucaria forest on
the treeline; >2000 m above sea level
Sea level to ca. 1500 m above sea level
Coast and inland, mainly inselbergs; elevations
from 0 to 1400 m above sea level
Coastal lowlands
Frost, drought, shallow or absent soil, and high light
irradiation
Medina et al. (2006), Martinelli (2007), and Ribeiro
et al. (2007)
Deep shade
Drought, shallow or absent soil, salinity (coast)
Rizzini (1979)
Scarano et al. (2005b), Scarano (2007b)
Flooding
Scarano et al. (1997), Scarano (2006)
Drought, salinity, and low nutrient
Araujo (1997), Gebler et al. (2005b)
Drought, salinity, and low nutrient
Scarano et al. (2005b), Pimentel et al. (2007)
Rain forest
Rocky
outcrops
Swamp
forest
Dry forests
Restingas
Coastal lowlands (mainly at Búzios-Cabo Frio
region, north of Rio de Janeiro)
Vegetation mosaic that occupies the coastal
sandy plains. Open clumped vegetation (where
studies reviewed took place) is one of the most
common physiognomies.
F.R. Scarano / Biological Conservation 142 (2009) 1201–1208
restingas) or absence of structured soil (e.g. rock outcrops), seasonal drought (e.g. seasonally dry forest), and more than 60 nights
per year with freezing temperatures (e.g. high altitude campos).
Third, diversity is more commonly lower than in the core formation because these marginal vegetation types often have a strong
oligarchic structure, with a few dominant species and many locally
rare species.
These three features, common to most of the habitats marginal
to the Atlantic rain forest of Rio de Janeiro, were the background to
the hypothesis on the origin and maintenance of their diversity, i.e.
that plant colonization of such habitats was largely related to terrestrial nurse plants that originally, in the rainforest habitat, were
canopy plants such as epiphytes or hemi-epiphytes (Scarano,
2002). Adaptations to water and nutrient restrictions, typical of life
in the canopy, granted colonization success to such plants upon
migration to sandy, swampy or rocky substrates in neighbouring
areas. Many such species, then, behaved as nurse plants and created conditions to subsequent colonization of these more extreme
habitats by a number of other rainforest species. Thus, nurse
plants, irrespective of whether or not they are pioneers, are
stress-tolerators and, in turn, ameliorate their local habitats and allow less tolerant species to establish.
This hypothesis and the knowledge available on the Atlantic
forest complex and its marginal habitats is here the background
for a discussion on the inadequacy of the species rarity bias when
establishing conservation priorities, based on the following
grounds: (a) widespread, common plants are among nurse plants
that are keystone species in the marginal habitats, and despite high
abundance might have low seed output; (b) locally rare plants or
endemics might be highly ecologically plastic or may assume an
invasive behaviour and become abundant after disturbance; (c)
taxonomy of some key plant groups is still poor, which hinders biogeographic interpretations and turns fuzzy the rare vs. common pigeon-holes. These three topics are discussed next.
3. Nurse plants and fitness
The nurse-plant syndrome takes place when plant species shelter seedlings, young and/or adult individuals of other species
throughout their ontogeny (Franco and Nobel, 1989). Therefore,
nurse plants promote facilitation enhancing fitness, survival and/
or growth of associated species (Callaway et al., 2002; Bruno
et al., 2003; Brooker et al., 2008). This syndrome often results in
the process of nucleation, i.e. formation of vegetation clumps or islands, which is well known for arid and alpine zones but still
amounts to only a few examples from tropical environments
(Duarte et al., 2006; Dias and Scarano, 2007). Whenever nurse
plant effects go beyond the scope of facilitation only and affect
the physical space where other species live, and such direct effects
last longer than their lifetime, they are called ecosystem engineers
(Hastings et al., 2006). Here, I make no distinction if sheltered
plants grow underneath or on the top of such nurse plants and,
therefore, the cases described here will be seen in the literature
under different designations (e.g. mat species, nucleation plants,
etc.).
3.1. Case studies
Clusia hilariana Schltdl. – Although field observations suggest
that a nurse plant effect might occur in the case of other Clusia species in the Brazilian restingas (e.g. Clusia fluminensis Pl. et Tr. and
Clusia spiritu-sanctensis Mariz & Weinberg), C. hilariana has been
more thoroughly studied in this respect (see review in Dias and
Scarano, 2007). It is phytosociologically dominant at the so-called
Clusia scrub, which is the predominant physiognomy in the restin-
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gas at the northern coast of the State of Rio de Janeiro (Pimentel
et al., 2007). It consists of vegetation islands of various sizes surrounded by white sand.
This tree can be as tall as 8 m (Dias et al., 2006) and displays a
number of peculiar features, such as (1) dioecy (Faria et al., 2006),
(2) seedling occurrence predominantly inside the tanks of terrestrial bromeliads (Scarano, 2002), (3) CAM metabolism (Franco
et al., 1999; Scarano et al., 2005b; Lüttge, 2006), and (4) an aboveground biomass stock and understorey litter comparable to the entire woody component of many neotropical savannas (Dias et al.,
2006). Curiously, however, Clusia is a genus with many hemi-epiphytic stranglers and/or rupicolous species (Lüttge, 2006) that live
in the neighbouring rainforest habitats.
More importantly, C. hilariana is the most abundant woody species locally (Pimentel et al., 2007) and my hypothesis was that it
had a nursing effect on other plants (Scarano, 2002). In order to
irrefutably confirm the key role of this species as a nurse plant,
experimental set ups in the field to simulate a situation where this
species is not present, i.e. removal experiments, would be commendable (see Díaz et al., 2003; Kareiva and Levin, 2003). The removal and the eventual ‘disappearance’ of the species from a
given point in space simulate a disturbance of such extent as to locally extinguish the species. Such experiments demand a huge logistic effort for set up, monitoring and analysis. They also require
special permits from environmental officials. Alternatively, we
used structural equation modelling (SEM) to assess the extent
and the mechanisms underlying this positive effect (Dias and Scarano, 2007). SEM is an analytical method that allows hypothesis
testing involving multiple interacting variables. Its origins can be
traced back to path analysis and its development to present has
been mostly promoted under the scope of social sciences (Bollen,
1989; Hoyle, 1995; Pearl, 2000; Shipley, 2000). Conclusions of this
study were that C. hilariana has a positive effect on both understorey seedling density and richness, which is partly related to the
activity of seed dispersers that use male and female plants indistinctly, confirming previous evidence (Liebig et al., 2001; Dias
et al., 2005).
Two additional results open new avenues for research on this
interesting species. First, Dias et al. (2006) indicated that slow
decomposition may play an important role on carbon accumulation and that, C. hilariana, despite its conservative strategy of carbon acquisition via CAM, gives a high contribution to biomass
stock in this nutrient-poor coastal vegetation. Therefore, in addition to the positive role played on local biodiversity, this plant
might also strongly affect ecosystem processes such as productivity and nutrient cycling that, in turn, are also likely to affect
recruitment process and species composition. Thus, the combination of biotic effects with a long-lasting physical effect on ecosystem processes qualify this species as an ecosystem engineer,
according to the definition of Hastings et al. (2006). SEM is currently being used to allow a synthetic framework of community
and ecosystem dynamics of this vegetation.
Second, we proposed that succession in this vegetation is cyclic
(Scarano et al., 2004). However, we found new evidence that challenges the original succession model proposed. Originally we
thought that C. hilariana was the climax species of the vegetation
and that upon its local decline and death, vegetation islands would
reduce in complexity and return to early successional stages. Evidence in Dias et al. (2005) indicated that Clusia may have dominated in the past some of the present-day non-Clusia patches.
After nursing seedlings of various species, when such species reach
later ontogenetic stages, competitive interactions may take place
between Clusia and these understorey plants. For instance, upon
senescence and death of C. hilariana, understorey plants increase
in size and density (Dias and Scarano, 2007). Further, we have
recently found a strongly positive association between adults of
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F.R. Scarano / Biological Conservation 142 (2009) 1201–1208
C. hilariana and juveniles of Protium icicariba (DC.) Marchand
(unpublished data). P. icicariba is co-dominant to C. hilariana in this
vegetation and is the most common plant occupying the non-Clusia
patches. Thus, rather than a step back into succession, non-Clusia
patches are possibly a step forward, and therefore C. hilariana is
probably a mid-successional species. Clearly, removal experiments
shall prove useful to uncover further mechanisms and causal factors for such nursing effect and consequent successional process.
Bromeliads – Bromeliads in the swamp forests (e.g. Nidularium
procerum Lindm.), in the restingas (e.g. Aechmea nudicaulis (L.) Griseb.) and in the high altitude rock outcrops (e.g. Fernseea itatiaiae
(Wawra) Backer) have been shown to provide safe germination
sites to plants of other species (Scarano et al., 1997; Scarano,
2002; Medina et al., 2006). They all have in common that in the
Atlantic rain forest they are typically epiphytes, whereas in the
marginal habitats they are often terrestrial playing a role as nurse
plants. Moreover, as in the case of C. hilariana, these plants are all
highly abundant locally, and with the exception of F. itatiaiae (Scarano et al., 2001), they all have crassulacean acid metabolism
(CAM).
Seed germination on the nutrient-poor and often hot exposed
soils of the restinga, or on rocks, or on flooded soils, is a difficult
hurdle to overcome. Germination of C. hilariana, for instance, is predominantly associated to the rosette of tank-bromeliads such as
Aechmea nudicaulis and also Neoregelia cruenta (Graham) L.B. Sm.
(Scarano, 2002; Dias and Scarano, 2007). Thus, bromeliads are
important nurse plants of the restingas. Interestingly, however,
seedlings of such bromeliads are hardly ever found in these sites,
which suggest that they seem unable to germinate on the bare
sand (e.g. Pinheiro and Borghetti, 2003). Indeed, we found that clonal growth for Aechmea nudicaulis, a locally abundant species, reveals a directional movement from inside vegetation patches to
the outside, where these clones colonize an open area and, in turn,
generate a potential germination site for Clusia and other plant
species (Sampaio et al., 2004). Similarly, in Atlantic forest swamps
the tanks of N. procerum provide safe germination for a number of
tree species (Scarano et al., 1997; Scarano, 2006). It colonizes large
flooded areas via clonal growth and is highly competitive for space
(Freitas et al., 2003). Finally, F. itatiaiae behaves as a mat species on
rock outcrops at the high altitude zone of the Itatiaia plateau,
although locally it is less important in this respect than plant species belonging to other families (Medina et al., 2006).
3.2. Common features and differences between nurse plants
Table 2 provides a brief summary of main features of the nurse
plants described here. In addition to Clusias and bromeliads, we
have found other important nurse plants that are not canopy
plants in the rainforest. In the high altitude rock outcrops, the
mat species Pleurostima gounnelleana (Beauv.) N.L de Menezes
(Velloziaceae) and bryophytes nucleate the vegetation islands with
highest species richness (Medina et al., 2006), while in the restingas
the hemicryptophyte palm Allagoptera arenaria (Gomes) Kuntze is
one of the few pioneers on the bare sand and is a key starting point
for vegetation succession (Scarano, 2002). While the various nurse
plants listed here belong to phylogenetically distant groups, present different life-forms and habits, and not all of them have epiphytic forms in the rainforest, they seem to share some
interesting similarities. They are all locally abundant and they all
have good ecophysiological performance (Scarano et al., 1999,
2001, 2005a). These two traits are often treated as measures of fitness (e.g. Niklas, 1997; Lüttge and Scarano, 2007). Thus, a close
examination of fitness – i.e. an individual’s ability to contribute
to the gene pool of the next generation relative to that of other
individuals – is required.
Niklas (1997) argued that the various biological properties contributing to fitness can be grouped into two categories: those related to survival and those related to reproductive success. The
usual practise is to select a few traits to measure (often belonging
to one of the categories only) and assume that they provide a good
assessment of fitness. This is not necessarily a correct assumption.
The risks of assuming, for instance, a correlation between survival
and reproductive success are clear from the example given by Niklas (1997): one can easily imagine a long-living sterile plant and/or
a fecund ephemeral plant. Indeed, in the case of the nurse plants of
the habitats marginal to the Atlantic rain forest high abundance
and good ecophysiological performance are not necessarily correlated to Darwinian fitness, i.e. seed output.
Table 2
Sites (habitat type, location and climate) where most of the research reviewed here has been conducted. Proposed nurse plants for each site are given, along with evidences
regarding their Darwinian fitness and respective references.
Habitats
Location
Climate
Nurse plant species
Fitness-related evidences
References
High
altitude
rocky
outcrops
Itatiaia National Park
(20°250 S, 44°500 W;
2400 m a.s.l.)
Campylopus pilifer* and
Polytrichum commune*
Pleurostima gounelleana*
Fernseea itatiaiae*
Unavailable
Scarano et al. (2001),
Medina et al. (2006), and
Ribeiro et al. (2007)
Swamp
forest
Poço das Antas
Biological Reserve
(22°300 S, 42°150 W; sea
level)
Nidularium procerum**
Absence of new seedlings in
over 10 years of observation
period. Clonal growth only.
Scarano et al. (1997), Freitas
et al. (1998, 2003)
Open
restingas
Restinga de Jurubatiba
National Park (22°230 S,
41°450 W; sea level)
2273 mm rainfall concentrated in the
summer (November–February).
Winter (May–August): cold, dry, and
less. Summer daytime T °C
max = 23 °C; winter night-time
min = T °C 10 °C .
2053 mm rainfall well distributed
throughout the year; discrete dry
season (May–September) Annual
T °C: mean = 26 °C, max = 38 °C,
min = 14 °C.
Markedly seasonal. Annual rainfall of
1164 mm concentrated in the
summer (November–February).
Annual T °C: mean = 23 °C,
max = 30 °C, min = 20 °C.
Aechmea nudicaulis**
Absence of new seedlings in
over 10 years of observation
period. Clonal growth only.
Regular fruiting and
evidences of seed
regeneration
Low fruit set (often < 30%)
in most of nine sampling
sites along 4 years. Low fruit
and seed set in other two
sampling sites over 2 years.
Liebig et al. (2001), Sampaio
et al. (2004, 2005), Scarano
et al. (2004), Dias et al.
(2005), Faria et al. (2006),
Dias and Scarano (2007),
and Martins et al. (2007)
Allagoptera arenaria*
Clusia hilariana**
*
**
Are both pioneer and nurse plants.
Are nurse plants but not pioneers.
F.R. Scarano / Biological Conservation 142 (2009) 1201–1208
C. hilariana was also the most studied nurse plant in this respect.
High abundance (Pimentel et al., 2007) and good ecophysiological
performance via the conservative strategy of CAM (Scarano et al.,
2005b) do not seem to match an often low fruit and seed output
(Faria et al., 2006). We have hypothesized that local abundance
may have been achieved by a substantial contribution of asexual
reproduction and/or high success of sexual reproduction in odd
years (Martins et al., 2007). Asexual regeneration is not often accounted for in fitness measures and might help explain such lack
of correlation. In the case of the bromeliads, seed-originated regenerants of Aechmea nudicaulis in the restingas and N. procerum in the
swamp forest have hardly been ever found in over 10 years of
observations. Clonal growth maintains the high abundance of these
species and provides advantages in the competition for space with
other species (Freitas et al., 1998, 2003; Sampaio et al., 2004,
2005).
Indeed, particularly in the restinga habitat, clonal growth and
asexual reproduction do seem to be relevant to overall performance of plants. Matallana et al. (2005) speculated that the exceptionally high proportion of dioecious plants (37%) found among
the 27 most abundant species in the open restingas of northern
Rio de Janeiro (including dominant C. hilariana and P. icicariba) is
correlated to clonal growth or resprouting capacity. Dioecy abundance was rather unexpected given that the flora of this geologically young habitat is predominantly originated from the
neighbouring rainforest. Since dioecious plants demand vectors
for cross-pollination, it appeared unlikely that pollinators would
follow the migration of plant species from a mesic environment
to a harsh coastal environment. Dioecy, however, is often associated with fleshy fruit formation (Weller and Sakai, 1999; Vamosi
et al., 2003; Vamosi and Vamosi, 2004), including for these restingas (Matallana et al., 2005) and, consequently, long distance dispersal by birds (for a local example, see Gonzaga et al., 2000). If
dioecy and asexual reproduction in the restingas are correlated,
the former could explain arrival via long distance dispersal and
the latter maintenance, particularly in a scenario of low Darwinian
fitness, as seems to be the case for Clusia (Matallana et al., 2005;
Faria et al., 2006).
Despite all the similarities shared by the nurse plants at the
habitats peripheral to the Atlantic forest complex, from a conservation viewpoint one important variation is in regard to their
geographic distribution patterns. While all nurse plants discussed
are highly abundant at their local habitats, some of them are
endemics (e.g. F. itatiaiae, Pleurostima gounnelleana) and others
are widespread (e.g. Aechmea nudicaulis, Allagoptera arenaria).
Although Simberloff (2003) lists some keystone species that are
rare in nature or locally, there are clearly more reports of abundant species playing such a role. However, as he points out, keystone species were originally defined to be species whose
importance to the rest of the community and the ecosystem is
disproportionate given its abundance. Irrespective of the controversies around the keystone species concept, fact is that if (a)
nurse plants play key roles related to community biodiversity
and ecosystem function at this rainforest periphery and elsewhere, and (b) nurse plants in our case are often locally abundant
and at least regionally widespread, it follows that such plants,
irrespective of commonality or rarity, should be targeted by conservation initiatives. Indeed, Lindenmayer et al. (2008) have recently argued that one often detects the functional relevance of
a keystone species after damage is done to the ecosystem where
it occurs. It is also well known that lower levels of functional
redundancy, as in ecosystems that rely on one or a few keystone
species, imply in higher fragility (e.g. Simberloff, 2003; Scarano,
2006). Thus, Lindenmayer et al. (2008) proposed that keystone
species should be as much of a priority as rare species in a checklist for ecological management of landscapes for conservation.
1205
Rodrigues et al. (2009) further argued that such species should
be targeted for restoration initiatives in the Atlantic forest.
4. Rarity and plasticity
While one intuitively associates rarity to fragility, this is not
necessarily so. We have seen, for instance, that even abundant
nurse plants may face problems with sexual reproduction. I now
focus on distinct cases of species that fit the labels of rare, endemic
or threatened and share features that reflect vigour and plasticity
in face of environmental variation or change.
F. itatiaiae, the bromeliad that form mats on rocks at high altitude areas and nurse other plant species, is the only case we have
examined of a rare nurse plant. It is endemic to the Itatiaia plateau
where, however, it has a highly abundant population (Medina
et al., 2006). Perhaps more interestingly, this local dominant plant
is also highly plastic as regards its ecophysiology, particularly of
nitrogen use, which might explain its high abundance and vigour
(Scarano et al., 2001). Locally, neighbouring plants of this species
displayed one of the highest intraspecific variations of nitrogen isotope signatures (4.3‰ variation) reported in the literature, which is
related to root system functioning. This plant is often associated to
bryophyte mats, which vary in depth, before reaching bare rock.
Araucaria angustifolia (Bertol.) Kuntze (at high altitudes in Rio
de Janeiro) and Caesalpinia echinata Lam. (at dry coastal forests)
are present in any list of Brazilian species threatened of extinction,
however they are locally highly abundant in their habitats in Rio de
Janeiro and, in regard to ecophysiological performance, highly vigorous in the case of the former (e.g. high electron transport rates;
Franco et al., 2005) or strongly conservative as in the case of the
latter (e.g. slow growth, high proline accumulation; Gebler et al.,
2005b). Moreover, Araucaria shows high within-population genetic
diversity at the study site (Souza et al., 2005). Caesalpinia shows a
similar pattern locally, but it has been shown that the species has
higher between-population than within-population genetic diversity (Cardoso et al., 1998). High abundance, good ecophysiological
performance and high genetic diversity can hardly be seen as indicators of fragility. Although in the case of the two threatened trees
past and present economic use are obviously serious hurdles they
have to face, at least in the case of Araucaria, forecasts that adequate management of planted forests could contribute to Atlantic
forest conservation in southern Brazil are highly encouraging
(Fonseca et al., 2009).
The legume tree Andira legalis (Vell.) Toledo is another curious
case that deserves examination. It is restricted to isolated, often
small populations, sparsely occurring in coastal vegetation from
southeast to northeast Brazil (Mattos, 1979), in both exposed (open
shrubby vegetation in the restingas) and shaded environments (in
coastal or low montane forests). Contrasting with the majority of
the species in the genus, it has big fruits that are probably dispersed
by large rodents (Pennington and Gemeinholzer, 2000). Such as in
the case of the nurse bromeliads, although some fruit production
has taken place, seedlings of this species have not been found in
our study sites since 1996. However, upon disturbance such as fire,
this species shows pronounced clonal growth (Cirne and Scarano,
2001) to an extent that it out-competes other local plants and densely covers restinga areas subjected to this manmade impact (Cirne
et al., 2003). This nitrogen-fixing plant (Scarano et al., 2001; Gebler
et al., 2005a) has an understorey often bare of other plant species in
restinga sites, and the occurrence of allelopathy in closely related
Andira humilis Mart. ex Benth. (Periotto et al., 2004) raises the suspicion that Andira legalis might behave likewise.
Thus, this small set of rare, endemic and/or threatened species
occurring at marginal rainforest habitats indicate how plastic and
ecologically versatile these plants can be in face of environmental
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F.R. Scarano / Biological Conservation 142 (2009) 1201–1208
change and/or disturbance. Intrinsic fragility is, therefore, discarded (see also Scarano et al., 2001, 2005a).
5. Biogeography and the taxonomic bottleneck
We have seen so far that common plants might perform key
ecological functions and that rare plants are not necessarily more
fragile biologically than common plants, and that evidences for
both arguments emerge from examples studied at habitats marginal to the Atlantic rain forest sensu stricto. The third possible flaw
related to the use of species rarity as an indicator for conservation
priority is related to taxonomic imprecision. This problem, still
common to many tropical plant groups, is two-fold.
First, for some plant groups there might be more actual species
than species names, i.e. one given species, poorly delimited taxonomically, might comprise several hidden species. Thus, if for instance the current taxonomic entity has a broad geographic
distribution, further taxonomic investigation might prove that this
entity actually hides several natural species, some of which might
be rare. The case of a bromeliad from the restingas is an example
pertinent to the subject matter of this paper. Aechmea bromeliifolia
(Rudge) Baker was the name given to a tank-bromeliad that occurred as a terrestrial, rupicolous or epiphyte plant, from sea level
to 1585 m of altitude, from Central America to Argentina and
throughout most Brazilian states (Smith and Downs, 1979), in vegetation as distinct as rain forests, savannas, dunes, marshes and
swamps. In Scarano et al. (2002) we have studied its impressive
morpho-physiological and ecological plasticity along four neighbouring habitats, which were located within walking distance from
each other in a restinga site, and varied largely as regards to light
and flooding regime. In all of these habitats we found seedlings
of various plant species inside these bromeliad tanks (unpublished
data), which based on the evidences described for other restingas
and swamp forests is likely to be a relevant trait to ensure diversity
in this location. Recently, a detailed study of the systematics of a
group within the Aechmea showed that what we then called Aechmea bromeliifolia is actually Aechmea maasii Gouda & W. Till. (Faria,
2006) which is geographically restricted to restingas and coastal
forests at northern Rio de Janeiro and Espírito Santo.
Second, and in opposition to the case above, for some plant
groups there might be more species names than actual species,
i.e. several rare species might be altogether one species only. Curiously, the bromeliads also provide a good example of this case. The
evolution of this plant family is fairly recent and many sources of
biological novelty are still available, which often posed difficulties
to species classification, such as natural hybridization (Wendt et al.,
2001, 2002), phenotypic plasticity (Freitas et al., 1998; Scarano
et al., 2002) and possibly high rates of somatic mutation (e.g. Duval
et al., 2003). Leme (2003), for instance, discussed nominal extinction of species, i.e. the designation of incorrect synonyms at the
specific or infraspecific level. He uses the example of the Bromeliaceae family in Brazil to argue that nominal extinction of species
might hinder conservation initiatives and that taxonomists should
be cautious when applying synonymies. His argument is built upon
two examples: (a) Smith (1955) designated Vriesea botafogensis
Mez a synonym of Vriesea saundersii (Carrière) E. Morren ex
Mez.; then Leme and Costa (1994) reinstated V. botafogensis; and
(b) Wendt (1997) designated Aechmea cariocae L.B. Sm. a synonym
of Aechmea squarrosa Baker; then Leme and Rezende (2002) reinstated Aechmea cariocae. He claims that the action of reinstating
these two species serves a practical goal of conserving them, given
that they are both endemic and rare, and invokes the use of the
precautionary principle of the United Nations (‘‘when there are
threats of serious or irreversible damage from a given activity, and if
full scientific certainty is not attained, this activity should be avoided
or strictly controlled”). Although well-intended, this argument is
incoherent because the two studies that he picked as examples
of poor taxonomy, and qualified as ‘‘irresponsible” based on his
opinion of what conservation should be, were published in wellknown peer-reviewed journals with significant impact factors,
whereas his counter-arguments were published in journals with
local and/or small circulation. Irrespective of whether his taxonomic opinion is correct or incorrect, the proliferation of vehicles
publishing descriptions of purportedly new species poses a risk
of creating fuzziness around species determination and possibly
generating more names than actual species. While species are
poorly delimited, perhaps species-groups or complex should be a
more functional conservation unit than species alone.
These two types of taxonomic problems that occur in the Bromeliaceae family can also be verified for the genus Clusia, as we
have recently admitted (Araujo and Scarano, 2007). C. hilariana, a
species that is central to our working hypothesis, was believed,
based on herbaria specimens, to be a widespread species common
to northern and southern states at coastal Brazil, and also to eastern states. Since rainforest specimens originally designated as C.
hilariana were recently revised and identified as Clusia aemygdioi
Gomes da Silva & Weinberg, there is a growing suspicion that the
former might be a strictly restinga species. If so, C. hilariana might
be an example of a recently originated Clusia species, which became dominant in the restingas studied here and instead of a widespread species would rather be an endemic.
6. Final remarks
Despite all obvious merits, biodiversity hotspot classification
(Myers et al., 2000) and other initiatives that establish rarity as
an indicator of conservation priority might be biased if they disregard important evolutionary and adaptive processes taking place in
lower diversity communities and/or ecotones (Smith et al., 2001;
Scarano, 2002) as the ones discussed here or comprehensively reviewed recently by Crawford (2008). In the case of the Atlantic rain
forest complex, the data reviewed here reinforces the thesis that
from a conservation viewpoint it should be treated as the rain forest plus its marginal habitats collectively. Marginal habitats are
extensions of the core rain forest and also a buffer zone to it, as
seen by the floristic relations discussed here and also by cases of
animal transit between these distinct vegetation types despite
fragmentation. This recommendation is in harmony with the notion that landscape history affects the present distribution pattern
of species in fragmented landscapes and therefore should be considered for conservation planning (Metzger et al., 2009).
The point here is that commonness may comprise species with
important ecological attributes related to ecosystem function and,
therefore, deserves equal attention as recently suggested by Lindenmayer et al. (2008). In the case discussed in this paper, some
of such common species play key roles in processes that result in
the high diversity of the marginal habitats where, curiously, the
species composition strongly consists of rainforest migrants. However, this is not to say that rarity does not deserve attention of conservation initiatives in the Atlantic forest complex or elsewhere.
Rarity remains relevant to conserve particularly because, as shown
by Grime (1998), they are an important pool for the future in an
ever changing planet. He has argued that if environmental changes
turned rare species abundant, they would then participate substantially in the transformation of energy and matter, thus becoming regulators of the ecosystem function.
Acknowledgements
I thank J.P. Metzger for critical reading and for kindly giving me
the opportunity to synthesize the ideas presented here, L.S. Duarte,
T. Wendt, an anonymous referee and my students A.T.C. Dias, M. L.
F.R. Scarano / Biological Conservation 142 (2009) 1201–1208
Garbin and R.B. Zandavalli for critical comments on the manuscript, and CNPq and FAPERJ for productivity grants.
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