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Universidade Federal de São Carlos
Centro de Ciências Biológicas e da Saúde
Programa de Pós-Graduação em Ecologia e Recursos Naturais
Defesas contra herbivoria no cerrado: síndromes de defesa e
originalidades
Danilo Muniz da Silva
Orientador: Prof. Dr. Marco Antônio Batalha
São Carlos – SP
Fevereiro de 2010
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Universidade Federal de São Carlos
Centro de Ciências Biológicas e da Saúde
Programa de Pós-Graduação em Ecologia e Recursos Naturais
Defesas contra herbivoria no cerrado: síndromes de defesa e
originalidades
Danilo Muniz da Silva
Dissertação apresentada ao Programa de Pós-
Graduação em Ecologia e Recursos Naturais da
Universidade Federal de São Carlos, como parte dos
requisitos para a obtenção do título de mestre em
Ecologia e Recursos Naturais.
Orientador: Prof. Dr. Marco Antônio Batalha
São Carlos
2010
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Ficha catalográfica elaborada pelo DePT da
Biblioteca Comunitária da UFSCar
S586dc
Silva, Danilo Muniz da.
Defesas contra herbivoria no cerrado: síndromes de
defesa e originalidades / Danilo Muniz da Silva. -- São
Carlos : UFSCar, 2010.
61 f.
Dissertação (Mestrado) -- Universidade Federal de São
Carlos, 2010.
1. Ecologia vegetal. 2. Extinção (Biologia). 3. Filogenia. 4.
Herbivoria. 5. Síndromes. I. Título.
CDD: 581.5 (20
a
)
Danilo MunÍZ da Silva
Defesas contra herbivoria no cerrado: síndromes de defesa e originalidades
Dissertação apresentada à Universidade Federal de São Carlos, como parte dos
requisitos para obtenção do títu10de Mestre em Ecologia e Recursos Naturais.
Aprovada em 22 de fevereiro de 2010
BANCA EXAMINADORA
10Examinador
Presidente
20 Examinador
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,( . ,~: ""'-C:>G,,;::;L~ c~ {..r.~
Prof. Dr. Heraldo Luis Vasconcelos
UFUlUberlândia-MG
3
4
Agradecimentos
Agradecemos à Fapesp por auxílio financeiro e por bolsa concedida ao primeiro autor; ao
CNPq, por bolsa concedida aos autores; e a P. H. T. Silva, J. F. Silva, A. M. M. Silva, P. Loiola, V.
Dantas, A. Rangel, F. T. Hanashiro, C. C. Angelieri e C. Mizuno, por ajuda em campo; a M. I. S.
Lima e M. Imatomi, por ajuda nas análises químicas.
5
Sumário
Resumo 6
Abstract 7
Introdução Geral 8
Capítulo1
Defense syndromes against herbivory in cerrado plant community 10
Capítulo 2
Phylogenetic and phenotypic originalities in a cerrado plant community 37
Conclusão geral 61
6
Resumo
As plantas possuem traços contra herbivoria que podem ocorrer conjuntamente e
aumentar a eficiência da defesa. Testamos se há síndromes de defesa em uma comunidade de
plantas do cerrado e caso haja, se elas apresentam sinal filogenético. Medimos nove traços de
defesa em uma comunidade de cerrado sensu stricto no sudeste do Brasil. Testamos a
correlação entre todos os pares de traços e agrupamos as espécies em síndromes de defesa de
acordo com os traços. A maioria das correlações par a par dos traços foi complementar.
Plantas com menores áreas foliares específicas apresentaram também folhas duras, com
menos nitrogênio, com mais tricomas e com taninos. Encontramos cinco síndromes: duas com
baixos valores de defesa e alta qualidade nutricional, duas com altos valores de defesa e baixa
qualidade nutricional e uma com traços compensando uns aos outros. Houve duas estratégias
de defesa contra herbivoria predominantes no cerrado: as síndromes de “tolerância” e de
“baixa qualidade nutricional”. Filogenia não determinou o conjunto de traços que as espécies
apresentaram; então, postulamos que a herbivoria atua como um fator biótico selecionando
esses traços.
A complementaridade permite a coexistência das espécies e um uso mais eficiente do
nicho. Originalidade de uma espécie é o quanto aquela espécie contribui para a raridade de
traços. Testamos a relação entre abundância e as originalidades filogenética e fenotípica e
comparamos a extinção baseada na abundância com extinções aleatórias. A abundância não
esteve relacionada com as originalidades, que por sua vez, não estiveram relacionadas entre
si. Extinções baseadas na abundância não diferiram do acaso. Entretanto, as originalidades
estiveram concentradas em poucas espécies e quatro das mais originais estavam entre as
mais raras. Essas espécies contribuíram para a raridade de traços mais do que as espécies
comuns e podem contribuir para dinâmicas compensatórias e manutenção da estabilidade da
comunidade. Logo, a abundância das espécies pode não ser um fator predominante na
manutenção das funções no cerrado.
7
Abstract
Plants have traits against herbivory that may occur together and increase defense
efficiency. We tested whether there are defense syndromes in a cerrado community and, if so,
whether there is a phylogenetic signal in them. We measured nine defense traits from a
woodland cerrado community in southeastern Brazil. We tested the correlation between all
pairs of traits and grouped the species into defense syndromes according to their traits. Most
pairwise correlations of traits were complementary. Plants with lower specific leaf area also
presented tougher leaves, with low nitrogen, more trichomes, and tannins. We found five
syndromes: two with low defenses and high nutritional quality, two with high defenses and
low nutritional quality, and one with traits compensating each other. There were two
predominant strategies against herbivory in cerrado: “tolerance” and “low nutritional quality”
syndromes. Phylogeny was not determining the suite of traits species presented; so, herbivory
could be regarded as a biotic factor selecting these traits.
Complementarity allows species coexistence and more efficient use of niche. Originality of
a species is how much that species contributes to rarity of traits. Here we (1) tested the
relation between abundance and both phylogenetic and phenotypic originalities and (2)
compared abundance-based extinctions to random ones. We measured nine defense traits,
phylogenetic information and abundance from a woodland cerrado community in
southeastern Brazil. Abundance was not related to neither phylogenetic nor functional
originalities; phylogenetic and phenotypic originalities were not related. Abundance-based
extinctions were not different from random. However, the originalities were concentred in
few species and four of the more original species were among the rarest. These species
contribute to rarity of traits more than common ones and they may contribute to
compensatory dynamics and to maintenance of community stability. Thus, species abundance
may not be a predominant factor to the maintenance of functions in cerrado.
8
Introdução Geral
Conjuntos de traços de defesas contra tipos diversos de herbívoros tendem a ser
favorecidos, pois reduzem o custo da defesa, de modo que, respostas mais gerais devem estar
presentes em toda a comunidade (Núñez-Farfán et al. 2007). Por outro lado, defesas para
herbívoros específicos são mais custosas e podem reduzir a resistência a outros herbívoros e
patógenos, assim tendem a ser induzidas apenas na presença destes herbívoros (Núñez-
Farfán et al. 2007, Thaler et al. 1999, Fordyce & Malcom 2000). A presença de um
determinado traço de defesa nas espécies pode covariar com a presença de outros traços,
formando conjuntos de traços que se podem definir como “síndromes de defesa” (Agrawal &
Fishbein 2006). Como a pressão de seleção da comunidade de herbívoros está sendo exercida
sobre toda a comunidade vegetal, as mesmas síndromes de defesas devem ocorrer em várias
espécies. Como as plantas de cerrado estão crescendo em solos pobres (Haridasan 2000) a
reposição de folhas perdidas por herbivoria é mais custosa (Fine et al. 2006). Por isso, o dano
causado pela herbivoria no cerrado é reduzido devido tanto à fenologia – o período de
produção de novas folhas é distinto do pico de herbívoros – quanto a alguns traços das folhas,
como dureza, baixos teores de nitrogênio e água e alto teor de fenóis (Marquis et al. 2002). A
herbivoria possui um papel importante para o cerrado, tanto diretamente pela influência no
crescimento e reprodução das plantas, quanto pela interação com fatores abióticos (Marquis
et al. 2002). Esperamos, pois, que a herbivoria seja um filtro ambiental muito forte no cerrado,
selecionando espécies com grande investimento em traços de defesa.
No primeiro capítulo, testamos a correlação entre os traços de defesa contra herbivoria e
sua interação com a filogenia do componente arbóreo-arbustivo de uma área de cerrado
sensu stricto no estado de São Paulo. Procuramos responder as seguintes perguntas: (1) As
plantas do cerrado apresentam conjunto de traços similares que caracterizam síndromes de
9
defesa?; (2) Se sim, Quais são essas síndromes?; e (3) Há sinal filogenético nas síndromes de
defesa contra herbivoria?
No segundo capítulo, utilizamos os traços de defesa contra herbivoria e as relações
filogenéticas das espécies do capítulo anterior. Com esses dados, determinamos as
originalidades filogenéticas e fenotípicas das espécies. Originalidade de uma espécie é uma
medida de quanto aquela espécie contribui para a raridade de traços na comunidade (Pavoine
et al. 2005). Espécies originais, devido a seus traços raros, são mais complementares às outras
espécies (Pavoine et al. 2005). Complementaridade permite a coexistência das espécies e o
uso mais eficiente do nicho (Petchey 2003). Nesse capítulo, testamos a relação entre a
abundância e a originalidade. Procuramos responder as seguintes perguntas: (1) As espécies
mais abundantes são filogeneticamente mais originais?; (2) As espécies mais abundantes são
fenotipicamente mais originais?; (3) As medidas de originalidade filogenética e fenotípica
estão relacionadas?; (4) Os valores de originalidades estão concentrados em poucas espécies?;
(5) Extinções simuladas das espécies baseadas nas suas abundâncias são diferentes do acaso?
10
Capítulo 1
Defense syndromes against herbivory in cerrado plant community
Danilo Muniz da Silva & Marco Antônio Batalha
Trabalho formatado nas normas da revista Plant Ecology.
11
Defense syndromes against herbivory in cerrado plant community
Danilo Muniz da Silva
1, 2
and Marco Antônio Batalha
1
1
Department of Botany, Federal University of São Carlos, P.O. Box 676, 13565-905
São Carlos, SP, Brazil
2
16 33518308
12
Defense syndromes against herbivory in cerrado plant community
Abstract
Plants have traits against herbivory that may occur together and increase defense efficiency.
We tested whether there are defense syndromes in a cerrado community and, if so, whether
there is a phylogenetic signal in them. We measured nine defense traits from a woodland
cerrado community in southeastern Brazil. We tested the correlation between all pairs of
traits and grouped the species into defense syndromes according to their traits. Most pairwise
correlations of traits were complementary. Plants with lower specific leaf area also presented
tougher leaves, with low nitrogen, more trichomes, and tannins. We found five syndromes:
two with low defenses and high nutritional quality, two with high defenses and low
nutritional quality, and one with traits compensating each other. There were two
predominant strategies against herbivory in cerrado: “tolerance” and “low nutritional quality”
syndromes. Phylogeny was not determining the suite of traits species presented; so, herbivory
could be regarded as a biotic factor selecting these traits.
Key-words: defense traits, herbivores, savanna, trade-off
Introduction
Plants have two defense strategies against herbivory: tolerance, the ability to maintain
fitness independently of herbivory damage, and resistance, the possession of traits that avoid
or deter herbivory (Mauricio 2000). It is difficult for plants growing in poor soils to replace
biomass lost to herbivores, so resistance should be the predominant defense strategy in such
situations (Fine et al. 2006). Defense traits can be structural (such as trichomes, spines, and
leaf toughness), chemical, or nutritional (Agrawal and Fishbein 2006, Hanley et al. 2007).
13
Structural defenses are morphological or anatomical traits that are advantageous to the plant
by avoiding that herbivores feed upon them, from protuberances to increased cell wall
toughness (Craine et al. 2003, Hanley et al. 2007). Nutritional defenses are traits that impose
difficulties for absorption of nutrients by herbivores, especially nitrogen, due to poor
nutritional materials (While 1993, Agrawal and Fishbein 2006). Chemical defenses are toxic
or repulsive compounds or enzyme inhibitors (Thaler et al. 1999, Craine et al. 2003).
Structural and chemical traits have investment costs along with defense benefits, and, thus,
are under selection (Craine et al. 2003, Hanley et al. 2007, Núñez-Farfán et al. 2007). These
traits may occur together and be complementary to each other, increasing defense efficiency;
for example, chemical and physical traits provide a greater level of defense when they occur
together (Berenbaum 1991). Thus, we expect some defense traits against herbivory to co-
occur in a given species.
Since suites of traits against several kinds of herbivores tend to be favored to reduce costs
associated to defense, general responses should be present in the whole community (Núñez-
Farfán et al. 2007). Moreover, defense against specific herbivores is more costly and can
reduce resistance against other herbivores and pathogens, defenses tend to be induced only in
the presence of the specific herbivore (Thaler et al. 1999, Fordyce and Malcon 2000, Núñez-
Farfán et al. 2007). Two or more traits may be positively correlated, resulting in suites of
covarying traits that may define “defense syndromes” (Agrawal and Fishbein 2006). As long
as the herbivore community implies selective pressure over the whole plant community, the
same defense syndromes should be present on most species.
Since cerrado (Brazilian savanna) plants grow in poor soils (Haridasan 2000), leaf
replacement demands more costs to them (Fine et al. 2006). Therefore, herbivory damage is
minimised in cerrado by both leaf phenology – that is, new leaves in periods distinct from
herbivore peaks – and leaf traits, such as toughness, low levels of nitrogen and water, and high
levels of phenolic compounds (Marquis et al. 2002). Herbivory has an important role in
14
cerrado ecology, either directly, by influencing plant growth and reproduction, or indirectly,
by the interaction with abiotic factors (Marquis et al. 2002). Herbivory restricts plant
distribution, acting as an environmental filter (Harley 2003). Environmental filters tend to
select species with similar traits that allow them to survive certain pressures (Fukami et al.
2005). We expect, then, herbivory to be a strong environmental filter in cerrado, selecting
species with high investment on defense traits.
Functional traits generally present phylogenetic conservatism on plant lineages (Ackerly
2003). If so, phylogenetic proximity allows two species to respond similarly to environmental
processes, due to traits inherited from common ancestry (Webb et al. 2002, Núñez-Farfán et
al. 2007). However, strong selection pressure can also lead two less related species to respond
similarly due to adaptative convergence (Webb et al. 2002, Núñez-Farfán et al. 2007). At
higher phylogenetic scales, defense traits seem to be more conserved, whereas, at lower
scales, they seem to be convergent (Agrawal and Fishbein 2006, Fine et al. 2006). For
example, different genera tend to present different suites of defense traits, indicating
phylogenetic clustering (Fine et al. 2006). However, in the genus Asclepias, defense traits are
not congruent to phylogeny, indicating “phylogenetic overdispersion” (Agrawal and Fishbein
2006). We expect, then, at community level, defense syndromes to be conserved.
Although there are studies on defense syndromes at genus level (Agrawal and Fishbein
2006, Becerra 2007) and among pairs of genera in forest communities (Fine et al. 2006), there
are no studies at community level. Particularly in the Brazilian cerrado, herbivory surveys are
restricted to only one species (e.g., Varanda and Pais 2006) or only a defense trait, such as
presence of extra-floral nectaries to ant association (e.g., Oliveira 1997, Oliveira and Freitas
2004) or latex presence (e.g., Diniz et al. 1999). Field mensurative experiments of defense
syndromes in cerrado plant communities could test the extrapolation of syndrome theory, as
well as relate defense traits to ecological and evolutionary constraints of savanna areas.
15
If defense syndromes are phylogenetically convergent, then one may suggest that
herbivory as a selective force is common and widespread; if, however, they are
phylogenetically conserved, then one may suggest that there is a phylogenetic signal and that
common ancestry can explain the association (Agrawal and Fishbein 2006). We expect
cerrado plants to present high investment in structural defenses, constituted primarily by
carbohydrates, and low investment in chemical defense, especially nitrogen compounds,
because the cerrado is a nutrient-limited community (Haridasan 2000, Craine et al. 2003).
The aim of this study was to test, in a cerrado disjunct site, the correlation of defense traits
and their interaction with phylogeny of woody plants. We addressed the following questions:
i) Do cerrado plant species present similar suites of traits that characterise defense
syndromes?; ii) If so, which are these syndromes?; and iii) Is there a phylogenetic signal in
defense syndromes against herbivory?
Methods
Study area and sampling
We carried out this study at the Federal University of São Carlos, southeastern Brazil
(21°58’05.3”S, 47°52‘10.1”W, 815-890 m a.s.l.; Santos et al. 1999). Regional climate is
seasonal, with dry winter and wet summer, defined as Cwa (Köppen 1931). The study site is
located at northeastern portion of the campus and is covered by woodland cerrado, a savanna
with dense tree cover (Sarmiento 1984, Santos et al. 1999). The study site presents poor soils,
with low pH, low content of organic matter and nitrogen, low cation exchange capacity, high
aluminum saturation and high proportion of sand (Table A1) and are classified as Oxisol
(Santos et al 1999).
We placed a 50 m x 50 m grid, with 100 5 m x 5 m contiguous plots, in which we sampled
16
all individuals belonging to the woody component, that is, woody individuals with stem
diameter at soil level equal to or higher than 3 cm (SMA 1997). We identified them to species
level, by using identification keys based on vegetative characters (Batalha and Mantovani
1999) and comparing vouchers to herbarium collections. We checked species names and
taxonomic information with Plantminer software (Carvalho et al. 2009). For each species in
the sample, we drew randomly ten individuals to measure the traits (Cornelissen et al. 2003).
When, for a given species, there were not ten individuals at the sample, we searched for
additional individuals nearby the plots, making an extra effort to reach ten individuals for
each species.
Defense traits
From each sampled individual, we collected mature leaves, that is, fully expanded and
hardened leaves, with as less damage as possible (Cornelisen et al. 2003). We kept the leaves
in a cooler to avoid water loss or deterioration, and took them as soon as possible to the
laboratory, where we measured the following traits: nutritional quality, specific leaf area,
water content, latex content, trichome density, toughness, presence of alkaloids, terpenoids,
and tannins (Agrawal and Fishbein 2006).
We measured carbon (C) and nitrogen (N) concentration in leaves and calculated C:N ratio
as an indicator of plant nutritional quality. We collected leaf samples from five replicates from
each species. Analyses were conducted at University of São Paulo, using an elemental CHNS-O
analyser (CE Instruments/EA 1110) to determine carbon and nitrogen concentration.
Nutritional quality may influence herbivore attacks to plant tissue; that is, an elevated C:N
ratio imposes difficulties for nitrogen acquisition by herbivores (Agrawal and Fishbein 2006).
In some cases, herbivores avoid plants with low nutritional quality, whereas, in others, they
increase herbivory rates to compensate for low nitrogen (Mattson 1980).
17
Specific leaf area is positively related to growth rate and to maximum photosynthetic rate
(Cornelissen et al. 2003). Low values of specific leaf area are related to high investments on
structural leaf defenses (Cornelissen et al. 2003), whereas high values indicate fast growing
and high palatability (Agrawal and Fishbein 2006). Similarly, leaf water content increases
palatability, and so a leaf with less water should be more resistant to herbivory (Agrawal and
Fishbein 2006). To measure specific leaf area and water content, we collected two leaves from
each individual, kept them in a cooler and weighted their fresh masses. We scanned the leaves
and determined leaf area using the ImageJ 1.33 software (Rasband 2004). Then, we oven-
dried them at 75°C during 72 h to obtain dry mass. Dividing leaf area by dry mass, we
obtained specific leaf area (Cornelissen et al. 2003). We assigned leaf water content by the
difference between fresh and dry mass, divided by leaf area (Agrawal and Fishbein 2006).
Latex is an important physical defense strategy against herbivory (Agrawal and Fishbein
2006). To measure latex content, we cut a leaf at the base and collected the latex with a filter
paper until the flow stopped. We oven-dried the samples at 75°C during 24 h, then we
weighted them. Trichomes are also important structural defenses (Agrawal and Fishbein
2006). We assigned trichome density by counting the number of trichomes in a 28 mm
2
circle,
delimited near the leaf tip, on both top and bottom, with a dissecting microscope (Agrawal
and Fishbein 2006). Toughness is related to defense and nutritional constituents, and should
influence herbivore activities (Agrawal and Fishbein 2006). We used a penetrometer
(dynamometer DFE 010, Chatilon, with a cone tip) to measure leaf toughness. We pushed the
probe of the penetrometer through the leaf and recorded the maximum force required to
penetrate it. We measured the toughness at each side of the mid-rib and used the mean as a
single data point per plant (Agrawal and Fishbein 2006).
We determined presence of chemical compounds in leaves following Falkenberg et al.
(2003). We assigned the presence of alkaloids, terpenoids, and tannins, which are chemical
compounds frequently found in Brazilian plants that may work as defense against herbivores
18
(Lima 2000). We oven-dried the leaves, extracting them with methanol and filtering the
extract after 48 h (Falkenberg et al. 2003). To alkaloids tests, we mixed 2 ml of hydrogen
chloride and 2 ml of the methanol extract; we then heated the mixture for 10 minutes, waited
until it cooled off and filtered it again (Falkenberg et al. 2003). After that, we used a series of
three assays, Mayer, Dragendorff, and Wagner reactions, to determine the presence of
alkaloids and, then, we considered as positive those samples that reacted to at least two out of
the three (Falkenberg et al. 2003). To terpenoids tests, we first evaporated 2 ml of the
methanol extract and to the residue we added 5 ml of chloroform. Then we used Liebermann-
Burchard and Salkowisk reactions to test the presence of terpenoids (Falkenberg et al. 2003).
To tannin tests, we first evaporated 5 ml of the methanol extract and to the residue we added
10 ml of distillated water. Then we used a ferric chloride reaction to determine the presence
of tannins (Falkenberg et al. 2003).
We constructed a matrix with the mean of each continuous trait and presence or absence of
binary traits for each species; when necessary, we log-transformed the variables to achieve
normality; we standardised all defense traits to zero mean and unit variance. We also
constructed a matrix with the phylogenetic independent contrast (PIC) of traits, which
corrects each variable for phylogenetic dependence, by scaling its contrasts by its standard
deviation related to phylogenetic distances, assuming a Brownian model of evolution
(Felsenstein 1985). We applied a correlation test with Spearman’s coefficient to all pairs of
traits and to all pairs of phylogenetic independent contrast of traits.
We constructed an Euclidean distance matrix based on average values for the species. We
then used K-means multivariate clustering (Legendre and Legendre 1998) to group the
species into defense syndromes, such that species within each syndrome would have defense
traits more similar to one another than to species in the other groups. We searched for species
clustering from two to five groups, and we selected the best clustering number with the
pseudo-statistics F (Calinski-Harabasz 1974). We did a principal component analysis and
19
constructed an ordination diagram to view the groups in relation to the traits (Legendre and
Legendre 1998). We carried out all analyses in R (R Core Development Team 2008).
Phylogenetic analysis
We constructed a phylogenetic tree for the species in the sample using the Phylomatic
software (Webb and Donoghue 2005). The lengths of the branches were estimated from
maximum ages determined for genus, families, orders, and superior clades (Davies et al.
2004). We fixed the root and all dated nodes, and then we extrapolated branches length
placing the non-dated nodes evenly between dated nodes or between dated nodes and
terminals (species), using the Bladj algorithm in the Phylomatic software (Webb and
Donoghue 2005). We calculated phylogenetic distances among all pairs of species using the
Phylocom 4.01b software (Webb et al. 2008). We did a Mantel correlogram with 999
randomisations, correlating the trait matrix to the phylogenetic distance matrix. We
calculated Mantel statistic for each distance class and we tested for significance by
permutations, using Bonferroni’s correction to test for the global significance (Legendre and
Fortim 1989).
Results
We found 2,062 individuals, belonging to 61 species and 29 families, obtaining defense
traits for each species (tables 1 and 2). Spearman’s coefficient between the pairs of traits and
between PICs were low, with the highest values around 0.6 (table 3). We found significant
negative correlations between: C:N and specific leaf area; specific leaf area and water; specific
leaf area and trichomes; specific leaf area and toughness; specific leaf area and tannins; and
latex and trichomes (table 3). We found significant positive correlations between C:N and
20
toughness, water and latex, and water and toughness (table 3). We found the same pattern for
PICs, except that the correlations of latex were not significant, tannins were correlated to
alkaloids and not to specific leaf area, and C:N and trichomes were positively correlated (table
3).
We found five groups of defense traits (table 2, figure 1). The first group was related to
latex; the second group was more related to high values of specific leaf area and low ratios of
C:N; the third group was related to low trichome densities and C:N ratios; and the fifth group
was related to high values of trichomes and alkaloids; the fourth group was more related to
low values of specific leaf area, to high values of C:N, and to the presence of chemical defenses
(figure 1). The number of species varied among the groups (2, 28, 4, 26, and 1, respectively).
We did not find relationships between trait distances and phylogenetic distances (figure 2).
Discussion
Most pairwise correlations of traits were complementary. For instance, plants with lower
specific leaf area also presented tougher leaves, lower nitrogen content, more trichomes, and
tannins. These traits are probably acting together to defend the plant against herbivory, as
predicted by syndrome theory (Agrawal & Fishbein 2006). Nevertheless, there were also
some trade-offs. Leaves with more water content were tougher and had lower specific leaf
area. Although two correlations with latex and one with alkaloids also indicated trade-offs,
there were only two species with latex and one with alkaloids. Relationships among traits are
usually synergistic or present no trade-off (Steward & Keeler 1988, Agrawal & Fishbein
2006). Leaf trait relationships may suffer constraints by morphometry, that is, the range a
given trait can assume depends on the variation on other traits. However, herbivory might
also press selection over traits with multiple functions (Steward & Keeler 1988). Even if a trait
21
is related or evolved in response to other functions, it might contribute to anti-herbivore
resistance of a given syndrome (Agrawal & Fishbein 2006).
We found the three types of syndromes proposed by the “defense syndrome triangle”
theory (Agrawal & Fishbein 2006). Two syndromes found here (groups 2 and 3)
corresponded to the “tolerance” syndrome. Species within these syndromes had low values of
all defense traits and high values of nutritional quality. Leaves with low levels of defense are
more consumed both in field and in laboratory conditions (Pérez-Harguindeguy et al. 2003).
Thus, although we did not measure the amount of damage caused by herbivores, these species
are expected to have tolerance to herbivory. Two other syndromes (groups 4 and 5)
corresponded to the “low nutritional quality” syndrome. They had traits that deter herbivory
and offer little nutrients. Species with these characteristics are expected to be less attacked by
herbivores (Pérez-Harguindeguy et al. 2003). A last syndrome could correspond to the
“nutrition and defense” syndrome, with tougher leaves and latex compensating high water
content and absence of trichomes. Species in this syndrome should be attacked only by few
herbivores that can overcome specific (latex) barriers and should be avoided by generalist
herbivores (Pérez-Harguindeguy et al. 2003). Three of the syndromes presented one or few
species and differed one from other by one trait (presence of alkaloids, absence of tannins, or
presence of latex). Thus, there were basically two predominant strategies of defense against
herbivory in the cerrado woody species we sampled.
As long as we did not find a phylogenetic signal, phylogeny was not determining the suite
of traits the species presented and so herbivory could be regarded as a biotic factor selecting
for these traits (Agrawal & Fishbein 2006). Furthermore, as the two predominant strategies
were present in most species, these suites of traits are expected to respond well to several
herbivores (Núñez-Farfán et al. 2007). Suites of diverse herbivores from different
phylogenetic groups and guilds attack the same phenotypic hosts (Maddox & Root 1990).
Since the selective pressure by herbivory is caused by suites of high diverse herbivores, the
22
response evolved against a species can act against another (Maddox & Root 1990). Moreover,
the community of herbivores is expected to be generalist, acting on the whole plant
community and not only on some phylogenetic groups (Agrawal & Fishbein 2006).
We should be careful to extrapolate these results to other savannas, because predominant
herbivores in cerrado are leaf-cutter ants and other insects, whereas in other savannas they
are large mammals living in big herds (Costa et al. 2008). Nevertheless, herbivory in cerrado
is greater than or comparable to other terrestrial communities (Costa et al. 2008). It can
decrease reproductive fitness or even lead to mortality of plants (Mundim 2009). Although
almost half of species presented tolerance syndrome, the impact of herbivory, together with
the nutrient-poor soils, makes tolerance strategy something unexpected as a defense against
herbivory for cerrado species (Fine et al. 2006). Tolerance strategy can have evolved as a
response to fire, which removes leaves less selectively than herbivores (Bond and Keeley
2005). Furthermore, cerrado plants may adjust their leaf phenology to escape in time from
insects attack (Marquis et al. 2001). The few strategies we found may be the result from series
of environmental filters, reducing the species pool sequentially, only to remain those with
phenotypic conditions to survive all of them, that is, drought, fire, poor soils, and, finally,
herbivory.
Acknowledgments
We are grateful to Fapesp, for financial support and for the scholarship granted to the first
author; to CNPq, for the scholarship granted to the second author; to P. Loiola, V. Dantas, I. A.
Silva, A. Rangel, F. T. Hanashiro, C. C. Angelieri and C. Mizuno, for valuable help in field.; to M. I.
S. Lima and M. Imatomi, for help in chemical analyses.
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28
Table 1 Numbers of sampled individuals of woody species in cerrado sensu stricto at Federal
University of São Carlos (21°58’05.3”S, 47°52‘10.1”W). In parenthesis the number of
individuals sampled outside of the plots (see Methods).
Family Species
Individuals
Anacardiaceae Tapirira guianensis Aubl.
10 (9)
Annonaceae
Ann
ona coriacea Mart.
10 (8)
Annonaceae
Annona crassiflora
Mart.
10 (9)
Annonaceae
Xylopia frutescens
Aubl.
10 (8)
Araliaceae Schefflera macrocarpa (Cham. & Schltdl.) Frodin
10 (6)
Araliaceae Schefflera vinosa (Cham. & Schltdl.) Frodin & Fiaschi
10 (0)
Asteraceae Gochnatia pulchra Cabrera
10 (0)
Asteraceae Piptocarpha rotundifolia (Less.) Baker
10 (0)
Bignoniaceae Tabebuia ochracea (Cham.) Standl.
10 (0)
Celastraceae Plenckia populnea Reissek
10 (0)
Clusiaceae Kielmeyera coriacea Mart. & Zucc.
10 (1)
Clusiaceae Kielmeyera grandiflora (Wawra) Saddi
10 (0)
Connaraceae Connarus suberosus Planch.
10 (9)
Dilleniaceae Davilla elliptica A. St.-Hil.
10 (6)
Dilleniaceae Davilla rugosa Poir.
10 (9)
Ebenaceae Diospyros hispida A. DC.
10 (0)
Erythroxylaceae Erythroxylum cuneifolium (Mart.) O.E. Schulz
10 (4)
Erythroxylaceae Erythroxylum suberosum A. St.-Hil.
10 (0)
Erythroxylaceae Erythroxylum tortuosum Mart.
10 (0)
Euphorbiaceae Pera glabrata (Schott) Poepp. ex Baill.
10 (1)
Fabaceae
Acosmium dasycarpum
(Vogel) Yakovlev
10 (0)
Fabaceae
Acosmium subelegans
(Mohlenbr.) Yakovlev
10 (6)
Fabaceae Bauhinia rufa (Bong.) Steud.
10 (0)
Fabaceae Dalbergia miscolobium Benth.
10 (0)
Fabaceae Dimorphandra mollis Benth.
10 (3)
Fabaceae Machaerium acutifolium Vogel
10 (6)
Fabaceae Stryphnodendron adstringens (Mart.) Coville
10 (0)
Fabaceae Stryphnodendron obovatum Benth.
10 (1)
Lacistemataceae Lacistema sp. Sw.
10 (9)
Lauraceae Ocotea pulchella (Nees) Mez
10 (0)
Malpighiaceae Banisteriopsis megaphylla (A. Juss.) B. Gates
10 (9)
Malpighiaceae Byrsonima coccolobifolia Kunth
10 (0)
Malpighiaceae Byrsonima verbascifolia (L.) DC.
2 (0)
Malpighiaceae Heteropterys umbellata A. Juss.
10 (6)
Melastomataceae Leandra lacunosa Cogn.
10 (7)
Melastomataceae Miconia albicans (Sw.) Triana
10 (0)
Melastomataceae Miconia ligustroides (DC.) Naudin
10 (0)
Melastomataceae Miconia rubiginosa (Bonpl.) DC.
10 (9)
Myrsinaceae Myrsine coriacea (Sw.) R. Br. ex Roem. & Schult.
10 (4)
Myrsinaceae Myrsine umbellata Mart.
10 (0)
Myrtaceae Campomanesia adamantium (Cambess.) O.Berg
10 (0)
Myrtaceae Myrcia bella Cambess.
10 (0)
Myrtaceae Myrcia guianensis (Aubl.) DC.
10 (0)
29
Family Species
Individuals
Myrtaceae Myrcia sp. DC. ex Guill
10 (6)
Myrtaceae Myrcia splendens (Sw.) DC.
10 (3)
Myrtaceae Myrcia tomentosa (Aubl.) DC.
10 (6)
Myrtaceae Psidium laurotteanum Cambess. in A.St.-Hil.
9 (7)
Nyctaginaceae Guapira noxia (Netto) Lundell
10 (7)
Nyctaginaceae Guapira opposita (Vell.) Reitz
10 (7)
Ochnaceae Ouratea spectabilis (Mart. ex Engl.) Engl.
10 (7)
Phyllanthaceae Phyllanthus acuminatus Vahl
10 (8)
Rubiaceae Palicourea coriacea (Cham.) K.Schum.
10 (8)
Rubiaceae Rudgea viburnoides (Cham.) Benth.
10 (0)
Rubiaceae Tocoyena formosa (Cham. & Schltdl.) K.Schum.
10 (0)
Rutaceae Fagara rhoifolia (Lam.) Engl. 10
(7)
Salicaceae Casearia sylvestris Sw.
10 (4)
Styracaceae Styrax ferrugineus Nees & Mart.
10 (1)
Thymelaeaceae Daphnopsis sp. Mart.
10 (6)
Verbenaceae
Aegiphila lhotskiana
Cham.
10 (0)
Verbenaceae Lippia velutina Schauer
10 (9)
Vochysiaceae Vochysia tucanorum Mart.
10 (0)
30
Table 2 Defense traits (mean ± sd, presence/absence for chemical defenses) for sampled species in cerrado sensu stricto at Federal University
of São Carlos (21°58’05.3”S, 47°52‘10.1”W). Group = group from K-means partitioning, Water = water content (mg cm
-2
), SLA = specific leaf
area (cm
2
g
-1
), Toughness (N), Trichomes = trichome density (trichomes cm
-2
), Latex (mg), C:N = carbon:nitrogen ratio.
Group
Species C:N SLA Water Latex Trichomes Toughness Alkaloids
Terpenoids
Tanins
1
Kielmeyera coriacea Mart. & Zucc. 28 ± 5 77 ± 13 31 ± 3 5 ± 5 1 ± 1 1.1 ± 0.2 0 1 1
1
Kielmeyera grandiflora (Wawra) Saddi 34 ± 9 77 ± 13 41 ± 9 9 ± 3 0 ± 0 1.9 ± 0.4 0 0 1
2
Acosmium subelegans (Mohlenbr.) Yakovlev 17 ± 3 82 ± 14 17 ± 5 0 ± 0 56 ± 123 1.0 ± 0.2 0 1 1
2
Aegiphila lhotskiana Cham. 15 ± 2 104 ± 15 27 ± 5 0 ± 0 841 ± 193 0.7 ± 0.2 0 1 1
2
Banisteriopsis megaphylla (A. Juss.) B. Gates 15 ± 3 127 ± 28 18 ± 6 0 ± 0 617 ± 331 0.4 ± 0.2 0 0 1
2
Byrsonima coccolobifolia Kunth 22 ± 3 97 ± 16 20 ± 0 0 ± 0 14 ± 12 0.8 ± 0.1 0 0 1
2
Casearia sylvestris Sw. 16 ± 3 124 ± 20 10 ± 0 0 ± 0 143 ± 114 0.7 ± 0.2 0 0 1
2
Dalbergia miscolobium Benth. 18 ± 3 76 ± 10 20 ± 0 0 ± 0 11 ± 10 0.8 ± 0.3 0 0 1
2
Daphnopsis sp. Mart. 24 ± 6 132 ± 44 17 ± 5 0 ± 0 1 ± 1 1.2 ± 0.2 0 0 1
2
Davilla elliptica A. St.-Hil. 29 ± 3 129 ± 43 16 ± 5 0 ± 0 216 ± 158 0.9 ± 0.3 0 0 1
2
Davilla rugosa Poir. 28 ± 3 188 ± 40 11 ± 3 0 ± 0 228 ± 134 0.8 ± 0.3 0 0 1
2
Dimorphandra mollis Benth. 13 ± 1 102 ± 15 12 ± 4 0 ± 0 623 ± 173 0.3 ± 0.1 0 0 1
2
Erythroxylum cuneifolium (Mart.) O.E. Schulz 18 ± 2 160 ± 42 11 ± 3 0 ± 0 1 ± 2 0.4 ± 0.2 0 1 1
2
Erythroxylum suberosum A. St.-Hil. 18 ± 3 90 ± 13 19 ± 3 0 ± 0 0 ± 1 1.3 ± 0.4 0 1 1
2
Erythroxylum tortuosum Mart. 20 ± 1 91 ± 14 20 ± 0 0 ± 0 2 ± 1 0.9 ± 0.4 0 0 1
2
Fagara rhoifolia (Lam.) Engl. 17 ± 3 106 ± 15 13 ± 5 0 ± 0 247 ± 101 0.5 ± 0.2 0 1 1
2
Gochnatia pulchra Cabrera 21 ± 6 103 ± 23 10 ± 0 0 ± 0 2700 ± 803 0.8 ± 0.1 0 1 1
2
Guapira noxia (Netto) Lundell 10 ± 1 104 ± 24 31 ± 7 0 ± 0 17 ± 25 0.9 ± 0.2 0 1 1
2
Guapira opposita (Vell.) Reitz 11 ± 1 120 ± 28 19 ± 7 0 ± 0 38 ± 55 0.8 ± 0.2 0 1 1
2
Heteropterys umbellata A. Juss. 17 ± 4 118 ± 22 11 ± 3 0 ± 0 27 ± 45 0.4 ± 0.1 0 0 1
2
Lacistema sp. Sw. 28 ± 8 157 ± 43 10 ± 0 0 ± 0 519 ± 86 0.6 ± 0.2 0 0 1
2
Leandra lacunosa Cogn. 29 ± 3 126 ± 26 22 ± 4 0 ± 0 257 ± 35 0.8 ± 0.3 0 0 1
2
Machaerium acutifolium Vogel 11 ± 2 92 ± 11 14 ± 5 0 ± 0 214 ± 123 0.9 ± 0.2 0 0 1
2
Miconia ligustroides (DC.) Naudin 27 ± 3 97 ± 22 19 ± 3 0 ± 0 5 ± 7 0.6 ± 0.1 0 0 1
2
Myrsine coriacea (Sw.) R. Br. ex Roem. & Schult. 20 ± 1 126 ± 21 12 ± 4 0 ± 0 308 ± 93 0.5 ± 0.1 0 1 1
2
Phyllanthus acuminatus Vahl 28 ± 1 207 ± 41 10 ± 0 0 ± 0 0 ± 0 0.3 ± 0.1 0 0 1
2
Plenckia populnea Reissek 21 ± 5 106 ± 12 12 ± 4 0 ± 0 0 ± 0 0.7 ± 0.2 0 1 1
2
Stryphnodendron adstringens (Mart.) Coville 18 ± 1 81 ± 15 22 ± 4 0 ± 0 24 ± 48 0.7 ± 0.1 0 0 1
2
Stryphnodendron obovatum Benth. 18 ± 3 121 ± 30 17 ± 7 0 ± 0 5 ± 2 0.4 ± 0.1 0 0 1
31
Group
Species C:N SLA Water Latex Trichomes Toughness Alkaloids
Terpenoids
Tanins
2
Xylopia frutescens Aubl. 21 ± 2 197 ± 34 10 ± 0 0 ± 0 140 ± 131 0.4 ± 0.1 0 1 1
3
Annona crassiflora Mart. 25 ± 5 117 ± 25 20 ± 0 0 ± 0 380 ± 82 0.7 ± 0.1 0 0 0
3
Lippia velutina Schauer 17 ± 3 164 ± 60 14 ± 5 0 ± 0 926 ± 130 0.5 ± 0.1 0 0 0
3
Palicourea coriacea (Cham.) K.Schum. 18 ± 5 112 ± 21 29 ± 5 0 ± 0 2 ± 4 0.9 ± 0.4 0 1 0
3
Vochysia tucanorum Mart. 21 ± 3 107 ± 16 24 ± 5 0 ± 0 9 ± 14 1.2 ± 0.2 0 1 0
4
Acosmium dasycarpum (Vogel) Yakovlev 17 ± 3 79 ± 9 20 ± 5 0 ± 0 1040 ± 334 1.2 ± 0.2 0 0 1
4
Annona coriacea Mart. 28 ± 4 86 ± 17 27 ± 7 0 ± 0 204 ± 72 2.1 ± 0.5 0 0 1
4
Bauhinia rufa (Bong.) Steud. 19 ± 2 67 ± 5 16 ± 5 0 ± 0 954 ± 227 1.1 ± 0.2 0 1 1
4
Byrsonima verbascifolia (L.) DC. 40 ± 7 74 ± 7 25 ± 7 0 ± 0 2056 ± 793 0.7 ± 0.1 0 0 1
4
Campomanesia adamantium (Cambess.) O.Berg 28 ± 3 81 ± 14 13 ± 5 0 ± 0 604 ± 401 1.1 ± 0.2 0 1 1
4
Connarus suberosus Planch. 30 ± 6 65 ± 6 20 ± 0 0 ± 0 1403 ± 561 1.4 ± 0.2 0 1 1
4
Diospyros hispida A. DC. 33 ± 5 62 ± 7 23 ± 5 0 ± 0 708 ± 278 1.0 ± 0.3 0 1 1
4
Miconia albicans (Sw.) Triana 31 ± 7 91 ± 17 17 ± 5 0 ± 0 65100
a
0.7 ± 0.2 0 0 1
4
Miconia rubiginosa (Bonpl.) DC. 38 ± 4 64 ± 7 20 ± 0 0 ± 0 281 ± 52 0.7 ± 0.1 0 0 1
4
Myrcia bella Cambess. 33 ± 6 89 ± 12 17 ± 5 0 ± 0 1020 ± 308 1.2 ± 0.2 0 1 1
4
Myrcia guianensis (Aubl.) DC. 29 ± 4 64 ± 8 20 ± 0 0 ± 0 661 ± 370 1.3 ± 0.3 0 0 1
4
Myrcia sp. DC. ex Guill 28 ± 2 78 ± 8 12 ± 5 0 ± 0 1095 ± 504 0.9 ± 0.2 0 0 1
4
Myrcia splendens (Sw.) DC. 39 ± 5 104 ± 24 10 ± 0 0 ± 0 1067 ± 385 0.8 ± 0.1 0 0 1
4
Myrcia tomentosa (Aubl.) DC. 25 ± 3 87 ± 13 16 ± 5 0 ± 0 419 ± 138 1.1 ± 0.3 0 1 1
4
Myrsine umbellata Mart. 31 ± 3 84 ± 20 20 ± 0 0 ± 0 0 ± 0 1.1 ± 0.3 0 0 1
4
Ocotea pulchella (Nees) Mez 30 ± 6 70 ± 12 14 ± 5 0 ± 0 1445 ± 710 1.4 ± 0.2 0 1 1
4
Ouratea spectabilis (Mart. ex Engl.) Engl. 32 ± 7 63 ± 12 22 ± 5 0 ± 0 0 ± 0 2.3 ± 0.5 0 1 1
4
Pera glabrata (Schott) Poepp. ex Baill. 31 ± 2 74 ± 9 20 ± 0 0 ± 0 0 ± 0 0.9 ± 0.2 0 0 1
4
Piptocarpha rotundifolia (Less.) Baker 28 ± 8 96 ± 22 20 ± 0 0 ± 0 1304 ± 419 1.1 ± 0.3 0 1 1
4
Psidium laurotteanum Cambess. in A.St.-Hil. 38 ± 6 74 ± 14 18 ± 4 0 ± 0 1583 ± 133 1.3 ± 0.1 0 1 1
4
Rudgea viburnoides (Cham.) Benth. 25 ± 4 81 ± 14 33 ± 5 0 ± 0 687 ± 258 1.2 ± 0.2 0 0 1
4
Schefflera macrocarpa (Cham. & Schltdl.) Frodin 31 ± 5 52 ± 17 36 ± 11 0 ± 0 2392 ± 450 1.0 ± 0.3 0 0 1
4
Schefflera vinosa (Cham. & Schltdl.) Frodin & Fiaschi 27 ± 5 62 ± 5 28 ± 6 0 ± 0 1572 ± 1038 0.9 ± 0.2 0 1 1
4
Styrax ferrugineus Nees & Mart. 36 ± 4 70 ± 19 20 ± 5 0 ± 0 437 ± 12 1.5 ± 0.3 0 1 1
4
Tabebuia ochracea (Cham.) Standl. 20 ± 3 77 ± 13 21 ± 3 0 ± 0 620 ± 148 1.3 ± 0.4 0 0 1
4
Tapirira guianensis Aubl. 34 ± 4 75 ± 11 20 ± 0 0 ± 0 18 ± 31 0.7 ± 0.1 0 0 1
5
Tocoyena formosa (Cham. & Schltdl.) K.Schum. 27 ± 6 86 ± 11 20 ± 5 0 ± 0 1627 ± 959 0.8 ± 0.3 1 1 1
a
measure without standard deviation, because it was based on a single leaf due to elevated number of trichomes
32
Table 3 Pairwise correlations of defense traits among cerrado species at Federal University of
São Carlos (21°58’05.3”S, 47°52‘10.1”W). SLA = Specific leaf area. Lower diagonal are
based on raw data, upper diagonal are phylogenetic independent contrast (PIC).
C:N SLA Water Latex Trichomes
Toughness Alkaloids Terpenoids
Tanins
C:N -0.41** 0.21 0.15 0.26* 0.38** 0.01 -0.19 0.14
SLA -0.47***
-0.54***
-0.01 -0.09 -0.60*** -0.11 -0.05 -0.15
Water 0.20 -0.53***
0.23 -0.16 0.57*** 0.11 -0.13 -0.19
Latex 0.16 -0.15 0.30* -0.12 0.13 0.00 -0.06 0.19
Trichomes 0.22 -0.28* -0.05 -0.26*
-0.15 0.10 -0.09 -0.05
Toughness 0.39** -0.61***
0.49*** 0.22 0.08 -0.06 0.05 0.07
Alkaloids 0.02 -0.04 0.06 -0.02 0.19 -0.04 0.07 -0.28*
Terpenoids
-0.09 -0.12 0.01 0.02 0.10 0.23 0.14 0.03
Tanins 0.17 -0.26* -0.15 0.05 0.06 0.07 0.03 -0.03
*P < 0.05, **P <0.01, ***P <0.001
33
Fig. 1 Biplot of principal component analysis with defense traits of species in
cerrado sensu stricto at the Federal University of São Carlos (21°58’05.3”S,
47°52‘10.1”W). Each species is represented by the number of its group. Water =
water content (mg cm
-2
), SLA = specific leaf area (cm
2
g
-1
), Toughness (N),
Trichomes = trichome density (trichomes cm
-2
), Latex (mg), C:N =
carbon:nitrogen ratio
Fig. 2 Mantel correlogram between the trait and the phylogenetic distances
matrices for cerrado species. No correlation was significant at α’ = 0.004
(Bonferroni correction)
34
-1 0 1 2
-1 0 1 2
PC1
PC2
CN
SLA
Water
Latex
Trichomes
Toughness
Alkaloids
Terpenoids
Tanins
4
22
4
3
2
4
2
4
4
2
4
2
2
2
2
2
4
2
2
2
2
2
2
2
2
1
1
2
2
3
2
4
2
4
4
4
4
4
4
2
4
4
4
3
4
2
4
2
4
4
4
4
2
2
4
4
4
5
3
2
Fig. 1
35
50 100 150 200 250
-0.10 -0.05 0.00 0.05
Phylogenetic distance
Mantel r
Fig. 2
36
Appendix
Table A1 Soil features (mean ± sd) in cerrado sensu stricto at Federal University of
São Carlos (21°58’05.3”S, 47°52‘10.1”W). OM = organic matter (g kg
-1
), P=
available phosphorus (mg kg
-1
), N= total nitrogen concentration (mg kg
-1
), K=
exchangeable K
+
(mmol kg
-1
), Ca= exchangeable Ca
2+
(mmol kg
-1
), Mg=
exchangeable Mg
2+
(mmol kg
-1
), Al= exchangeable Al
3+
(mmol kg
-1
) , SB= sum of
bases (mmol kg
-1
), CEC= cation exchange capacity (mmol kg
-1
), V= base
saturation (%), m= aluminum saturation (%), Sand, Silt and Clay (%)
Soil feature mean ± sd
pH 3.6 ± 0.1
OM 43 ± 8
P 5 ± 2
N 1740 ± 294
K 1.3 ± 0.4
Ca 3 ± 1
Mg 2 ± 1
Al 17 ± 4
SB 6.6 ± 2.0
CEC 87 ± 17
V 8 ± 3
M 72 ± 8
Sand 68 ± 2
Silt 4 ± 1
Clay 28 ± 2
37
Capítulo 2
Phylogenetic and phenotypic originalities in a cerrado plant community
Danilo Muniz da Silva, Igor Aurélio Silva & Marco Antônio Batalha
Trabalho formatado nas normas da revista Austral Ecology.
38
Phylogenetic and phenotypic originalities in a cerrado plant community
Danilo Muniz da Silva
1, 2
, Igor Aurélio Silva
1
and Marco Antônio Batalha
1
1
Department of Botany, Federal University of São Carlos, P.O. Box 676, 13565-
905 São Carlos, SP, Brazil
2
(55) 16 33518308
Short running title: Originality in cerrado plants
39
Phylogenetic and phenotypic originalities in a cerrado plant community
Abstract
Complementarity allows species coexistence and more efficient use of niche.
Originality of a species is how much that species contributes to rarity of traits.
Here we (1) tested the relation between abundance and both phylogenetic and
phenotypic originalities and (2) compared abundance-based extinctions to random
ones. We measured nine defense traits, phylogenetic information and abundance
from a woodland cerrado community in southeastern Brazil. Abundance was not
related to neither phylogenetic nor functional originalities; phylogenetic and
phenotypic originalities were not related. Abundance-based extinctions were not
different from random. However, the originalities were concentred in few species
and four of the more original species were among the rarest. These species
contribute to rarity of traits more than common ones and they may contribute to
compensatory dynamics and to maintenance of community stability. Thus, species
abundance may not be a predominant factor to the maintenance of functions in
cerrado.
Key words: complementarity, functionality, savanna, simulated extinction,
species abundance.
40
Introduction
Complementarity allows species coexistence, and more efficient use of niche
(Petchey 2003). Resource use efficiency depends on how much a community can
make use of the available niche, that is, if the niche is plentiful filled, more ways of
resource use will result in higher values of functioning (Petchey 2003).
Complementarity also plays a role in stability in space or time, when
complementary species have different functions acting at different periods or local
conditions (Questad & Foster 2008; Gonzalez & Loreau 2009). As the traits of a
species correspond to functions it performs and conditions it needs (Cornelissen et
al. 2003), differences in traits will establish niche partition and functioning
divergence (Mason et al. 2008; Questad & Foster 2008). Species with uncommon
traits may use different niches, increasing the probability of coexistence and even
increasing the conditions for the growth of other species in a process of facilitation
(Quintana-Ascencio & Menges 2000; Lyons et al. 2005). The frequency of traits
ranges from exclusive traits, present in one species only, to very common traits,
present in most species (Pavoine et al. 2005). Some species may have a very rare
trait or an amount of rare and uncommon traits; these species can thus perform
original functions and they are called “original species” (Pavoine et al. 2005; 2008).
Because of its rare traits, original species are more complementary to other species
(Pavoine et al. 2005).
Originality is usually measured as an average value of difference in traits among
a given species and all other species (Pavoine et al. 2005; 2008). The originality of
a species is how much that species contribute to rarity of traits in a community
(Pavoine et al. 2005). If many species contribute with specific traits each, then the
41
originality will be well distributed (Pavoine et al. 2005). If the opposite, few
species with many rare traits, the originality will be concentred into few species
and all the others will have low originality (Pavoine et al. 2005). Functionally
diverse communities in heterogeneous habitats present high spatial turnover due
to trait variation among species for exploiting environmental heterogeneity
(Questad & Foster 2008). Original species could be more abundant if they occupy
different portions of the niche, or less abundant if they need specific and rare
environmental conditions at small scale (Pavoine et al. 2005; Petchey et al. 2007).
If common species are the more original ones, there is niche partitioning by
narrowing species niches to distinct portions. Otherwise, if biotic factors act as
environmental filters, favouring species with similar traits (Webb et al. 2002),
common species would be the less original ones, presenting common traits.
Moreover, if original species, with key traits, are rare, there would be implications
for conservation. The role of rare species on functioning is underestimated and
needs more studies, because rare species are at higher risk of extinction (Pruvis et
al. 2000; Lyons et al. 2005). Thus, relationships between originality and abundance
may allow us to infer ecological process and establish conservation priorities.
The comparison between originality based on phylogenetic distances and
originality based on phenotypic distances may allow us to relate evolutionary
history to traits: phylogenetic distances represent time of divergence, which is a
period of isolated evolution and possibility of evolving new traits, whereas
phenotypic distances represent a divergence in traits themselves (Pavoine et al.
2005; Mouliott et al. 2008). In addition, it is possible to infer about functional
redundancy when comparing phenotypic originality to phylogenetic originality.
Species may have similar traits, or share similar phylogenetic history, or both.
42
Nonetheless, the real condition of functionally similar species to become
redundant is when their abilities to survive to different perturbations are different
from each other (Laliberté et al. 2009). Then, if the measures of phenotypic and
phylogenetic originality are not related, there may be insurance by redundancy.
That is, species with different resistances – for example, defences against
herbivory – share evolutionary history and may have the same functions. Thus, if
one species is lost, other could play the same role (Lyons et al. 2005; Laliberté et al.
2009). Probability of traits shared by related plants due to common ancestor
decreases with their phylogenetic distance (Pavoine et al. 2005). Also, some traits
may converge occurring in non-related plants, especially if they allow species to
survive to a given environmental filter (Webb et al. 2002). We expect, as a rule of
thumb, the traits to be conserved in the phylogeny and, consequently, the two
measures to be related. However, if traits are convergent, the two measures will
not be related.
Species extinctions are not random (Pruvis et al. 2000; Vamosi & Wilson 2008).
They are based on traits and may be biased on phylogeny (Pruvis et al. 2000;
Pruvis 2008). Thus, the loss of some species may result in greater loss of
functionality or evolutionary history than others, particularly if endangered
species have relatives also at risk (Vamosi & Wilson 2008). Moreover, how much
the loss of a given number of species results on loss of traits, depends on which
species are lost: loss of evolutionary distinct species or of phylogenetic clumps
results in greater loss of traits and evolutionary history (Isaac et al. 2007; Vamosi
& Wilson 2008). Originality can be used to identify priority species for
conservation and to maximise conservation actions (Pavoine et al. 2005). It is
difficult to determine the exact minimum viable size of populations (Brook et al.
43
2006), but it is assumed that species with lower abundances have higher risk of
extinction (Lyons et al. 2005). To assess the effect of extinctions on traits, we could
compare the loss of originality in abundance-based extinction trajectory to random
species loss.
The aim of this study was to test the relation of abundance and originality. We
addressed the following questions: (1) Are species abundance and phylogenetic
originality related?; (2) Are species abundance and phenotypic originality related?;
(3) Are the phylogenetic originality and phenotypic originality related?; (4) Are
phylogenetic and phenotypic originalities concentrated in few species?; (5) Are
simulated extinction of species based on their abundances different from random?
Methods
Study area and sampling
We carried out this study at the Federal University of São Carlos, southeastern
Brazil (21°58’05.3”S, 47°52‘10.1”W, 815-890 m a.s.l.; Santos et al. 1999). Regional
climate is seasonal, with dry winter and wet summer, defined as Cwa (Köppen
1931). The study site is located at the northeastern portion of the campus and is
covered by woodland cerrado, on Oxisol (Santos et al. 1999). In this area, there is a
permanent 50 m x 50 m grid, with 100 5 m x 5 m contiguous plots, in which all
individuals belonging to the woody component were identified. We considered a
list of leaf traits related to defence against herbivory: nutritional quality, specific
leaf area, water content, latex content, trichome density, toughness, presence of
alkaloids, presence of terpenoids, and presence of tannins.
44
We used an elemental CHNS-O analyser (CE Instruments/EA 1110) to
determine carbon and nitrogen concentration, with which we calculated C:N ratio
as an indicator of plant nutritional quality. We divided leaf area by dry mass, to
obtain specific leaf area (Cornelissen et al. 2003). We assigned leaf water content
by the difference between fresh and dry mass, divided by leaf area (Agrawal &
Fishbein 2006). To measure latex content, we cut a leaf at the base and collected
the latex with a filter paper. We oven-dried the samples at 75°C during 24 h, then
we weighted them. We assigned trichome density by counting the number of
trichomes in a 28 mm
2
circle, delimited near the leaf tip, on both top and bottom,
with a dissecting microscope (Agrawal & Fishbein 2006). We used a penetrometer
(dynamometer DFE 010, Chatilon, with a cone tip) to measure leaf toughness. We
pushed the probe of the penetrometer through the leaf and recorded the maximum
force required to penetrate it. We determined the presence of alkaloids,
terpenoids, and tannins in leaves following Falkenberg et al. (2003). We also
determined species abundances by counting the number of individuals for each
species in the plots.
Originality
We constructed a phylogenetic dendrogram for the species using the Phylomatic
software (Webb & Donoghue 2005). The lengths of the branches were estimated
from maximum ages determined for genus, families, orders, and superior clades
according to Davies et al. (2004). We fixed the root and all dated nodes, and then
we extrapolated branch lengths, placing the non-dated nodes evenly between
dated nodes or between dated nodes and terminals (species), using the Bladj
45
algorithm in the Phylomatic software (Webb & Donoghue 2005). We also
constructed a functional dendrogram using the defence traits. We did a
hierarchical clustering of species based on the traits, using Euclidean distance and
average method (Legendre & Legendre 1998).
For both dendrograms, we calculated the originality of each species following
the procedures proposed by Pavoine et al. (2005). First, we calculated the distance
of each pair of species, by summing the branches necessary to link the pairs into
the dendrograms. Then, we measured originalities as the frequency distribution
that maximises quadratic entropy (QE-based index, Pavoine et al. 2005). In this
way, we obtained two originality indices: phylogenetic originality, based on the
phylogenetic dendrogram, and phenotypic originality, based on the functional
dendrogram. We carried out all analyses in R (R Core Development Team 2009)
with the package “ade4” (Dray & Dufour 2007).
Statistical analyses
To test whether the originality of a species was related to its abundance, we
used a parametric Pearson correlation tests between abundances and both
phylogenetic and phenotypic originalities. We also tested for correlation between
both originality indices. We determine the number of species and individuals
necessary to achieve at least 50% of the whole originality for both originality
measures.
We ordered species by their abundances and then we simulated extinctions,
excluding species from the less to the most abundant. At each step, we summed up
the originality of remaining species. Then, we did 1,000 randomisations, excluding
46
species at random and summing up the originality of the remaining species at each
step. We then calculated the mean and 95% confidence intervals of the
randomisations. We carried out all analyses in R (R Core Development Team
2009).
Results
We did not find significant correlation between abundance and phylogenetic
originality (r = -0.028, P = 0.83), between abundance and phenotypic originality (r
= -0.001, P = 0.99), and between phylogenetic and phenotypic originalities (r = -
0.047, P = 0.72). Nine species comprised 52% of the phylogenetic originality,
accounting for 4.75% of total abundance, whereas other three species comprised
54% of the phenotypic originality, accounting for 6.11% of total abundance (Table
1). The common species (58% of total abundance) comprised only 7.5 and 4.9% of
the phylogenetic and phenotypic originalities, respectively (Table 2). Four species,
that is, Xylopia frutescens, Annona coriacea, Annona crassiflora, and Davilla rugosa
were among the nine species with higher phylogenetic originality and also were
among the rare species, with one or two individuals in the plots. Species with
higher phenotypic originality were among neither the less nor the most abundant
species.
The extinctions following abundance were not different from random
extinctions, when considering the trajectory of loss of either phylogenetic
originality (Fig. 1a) or phenotypic originality (Fig. 1b).
Discussion
47
There was a degree of redundancy among species, since the phenotypic and
phylogenetic originalities were not related. Most of the originalities were
concentred in a few rare species, indicating that these species present a higher
susceptibility to extinctions. The loss of the originalities was not different from
random and so species abundance may not be a predominant variable to the
maintenance of functions in cerrado.
The rare species were the more phylogenetically original ones. Although there
was no relation between abundance and phylogenetic originality, four of the most
original species were the less abundant ones. Rare species are usually
underestimated, although in some communities they perform keystone process in
the functioning (Lyons et al. 2005). As these rare species were isolated in the
phylogenetic tree, they may have a series of phylogenetic related traits
contributing more than common species to the rarity of traits (Pavoine et al. 2005).
More distinct species are expected to compensate the reduction of the population
size of the dominant species caused by environmental changes, because they may
be adapted to different conditions (Gonzalez & Loureau 2009). Besides, rare
species may have populations increased after disturbances or catastrophes, with
higher survival and growth rates, recolonising open areas and stabilising the
environmental conditions until populations of superior competitors stabilise
(Quintana-Ascencio & Menges 2000; Lyons et al. 2005). We know little about the
role rare species play in communities, and given that they are at high risk of
extinction, they should have a special conservation attention (Lyons et al. 2005).
The loss of one of these phylogenetically original species implies great loss of
48
genetic information, and, consequently, decreases possible responses to
environmental changes in cerrado.
Only three species encompassed more than half of the phenotypic originality,
implying that few species contributed to rarity of traits, even though these species
were not the most abundant and represented only about 6% of the total
abundance. Similar results were found in a fish community, in which five fish
species comprised 52% of the phenotypic originality (Moulliot et al. 2008) and in a
carnivore phylogeny, in which 12 out of 70 carnivore species comprised 50% of
the phylogenetic originality (Pavoine et al. 2005). If this pattern is maintained in
many community types, one may postulate that originality is concentrated in a
small number of species and, probably, of individuals. The concentration of traits
in species with low abundances indicates a degree of susceptibility of the
community to stochastic extinctions. If these few species were lost, there would be
loss of many functions in the community.
As long as we used defence traits against herbivory to estimate the phenotypic
originality, this measure was related to specific capacities to resist against
herbivores. In this context, more original species could be expected to have specific
defences and, consequently, specific herbivores. Variations in plant traits represent
a multidimensional resource map with discontinuities to which herbivores have to
adapt (Nyman 2009). As each plant lineage will inherit most of its traits from its
immediate ancestor, herbivores will have to overcome smaller differences, and in a
smaller number of traits, to attack related plants (Nyman 2009). Thus, common
and widespread plants with many relatives tend to have more associated
herbivores than rare, taxonomically isolated ones (Nyman 2009). Likewise,
phenotypic dissimilarities among species (for example, morphological features,
49
concentrations of nutrients, and presence of chemical defensive compounds)
correspond to herbivores tolerance to dietary variation, which is determined by its
physiological capabilities (Nyman 2009). Thus, less original species – clumped in
the phenotypic dendrogram – should share herbivores, whereas more original
species – isolated in the phenotypic dendrogram – should have specialist
herbivores.
Most of the relative abundance was concentrated in few species. This pattern, in
which there are few common and many rare species, is found worldwide in many
types of communities (Stohlgren et al. 2005). Common species contribute more to
biomass and, consequently, to stock function, but rare species may contribute to
nutrient use efficiency and regulatory functions disproportionally to their
abundances (Lyons et al. 2005). In communities that experience environmental
changes in time, less abundant species are important to compensatory dynamics,
especially if they have traits that allow them to survive different perturbations
(Gonzalez & Loreau 2009). This is the case in the Brazilian cerrado, which presents
many seasonal perturbations, such as fire and drought, which modify the structure
of the vegetation and increment light, nutrient, and the availability of open patches
(Gottsberger & Silberbauer-Gottsberger 2006). Moreover, the spatial variation of
rarity and dominance highlights the importance of rare species, with their unique
traits, to the maintenance of the community stability (Stohlgren et al. 2005).
Since the two originality indices were not related, the species isolated in the
phylogenetic tree had defence traits similar to the average of other species and
some species had rare traits, which were not present in their relatives. For a given
group of phylogenetic related plants, there were different resistance strategies
against herbivory; hence, functions performed by this group could be kept under
50
different herbivory pressures. If some less abundant species were functionally
similar to some dominant species, but with different requirements and tolerances,
they could increase the resilience of the community under perturbations, such as
an increasing herbivory (Lyons et al. 2005). This resilience may occur in the
cerrado, because the most abundant species were less original ones, being similar
to many species, and their phenotypic originality was not related to their
phylogenetic originality.
The simulated extinction based on abundances showed that the loss of
originality was not different from random, because most species had very low
originalities and their abundances did not predict their originalities. The most
phenotypically original species were generally neither the most abundant nor the
less abundant species, implying that the extinctions expected for rare species
would have low effect on the trait diversity. Besides, the general low levels of
originality and independence from the abundance indicated, to a certain extent, a
high functional similarity among rare and common species. Thus, the decline in
abundance of common species could be compensated by the increase of rare
competitor species adapted to different conditions (Gonzalez & Loreau 2009). For
each lost species, there will be a loss of originality: if species were extinct by their
abundance, the loss of phylogenetic originality would be predictable and
phenotypic originality would experience a great loss with a high number of extinct
species.
Acknowledgements
51
We are grateful to Fapesp, for financial support and for the scholarship granted
to the first author; to CNPq, for the scholarship granted to the authors; and to C. C.
Angelieri, V. Dantas, F. T. Hanashiro, C. Mizuno, P. Loiola, and A. Rangel, for
valuable help in field.
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Table 1 Woody species with higher values of phylogenetic and phenotypic
originalities, cumulative proportion of originality (f), and cumulative proportion
of abundance (n) in a woodland cerrado at Federal University of São Carlos
(approximately, 21°58’05.3”S, 47°52‘10.1”W)
Phylogenetic originality f (%) n (%)
Ocotea pulchella (Nees) Mez 0.160 16 1.99
Xylopia frutescens Aubl. 0.087 25 2.09
Annona coriacea Mart. 0.057 31 2.13
Annona crassiflora Mart. 0.057 36 2.23
Davilla elliptica A. St.-Hil. 0.033 40 2.28
Davilla rugosa Poir. 0.033 43 2.47
Diospyros hispida A. DC. 0.030 46 4.17
Styrax ferrugineus Nees & Mart. 0.030 49 4.61
Guapira opposita (Vell.) Reitz 0.029 52 4.75
Phenotypic originality
Tocoyena formosa (Cham. & Schltdl.) K.Schum. 0.273 27 1.99
Kielmeyera coriacea Mart. & Zucc. 0.134 41 3.54
Kielmeyera grandiflora (Wawra) Saddi 0.135 54 6.11
56
Table 2 Most abundant species, cumulative proportion of abundance (n),
cumulative proportion of phylogenetic originality, and cumulative proportion of
phenotypic originality in a woodland cerrado at Federal University of São Carlos
(approximately, 21°58’05.3”S, 47°52‘10.1”W)
n (%) Phylogenetic
originality
(%)
Phenotypic
originality
(%)
Myrsine umbellata Mart. 28 1.6 0.2
Vochysia tucanorum Mart. 36 3.2 3.4
Myrcia guianensis (Aubl.) DC. 42 3.5 3.9
Miconia albicans (Sw.) Triana 48 4.0 4.5
Piptocarpha rotundifolia (Less.) Baker 53 6.0 4.6
Tabebuia ochracea (Cham.) Standl. 58 7.5 4.9
57
Fig. 1 Effects of abundance-based extinctions on (a) phylogenetic originality and
(b) phenotypic originality in a woodland cerrado at Federal University of São
Carlos (approximately, 21°58’05.3”S, 47°52‘10.1”W). Open circles show
extinction trajectory following abundance, black circles show mean and 95%
confidence intervals of 1,000 random extinction trajectory, and gray circles
show the worst case (lower line) and best case (upper line) scenarios
58
0 10 20 30 40 50 60
0.0 0.2 0.4 0.6 0.8 1.0
phylogenetic originality
a
0 10 20 30 40 50 60
0.0 0.2 0.4 0.6 0.8 1.0
number of extinct species
phenotypic originality
b
59
Supplementary material
Fig. S 1 Dispersion diagram between (a) abundance and phylogenetic originality,
(b) abundance and phenotypic originality and (c) phylogenetic originality and
phenotypic originality in a woodland cerrado at Federal University of São Carlos
(approximately, 21°58’05.3”S, 47°52‘10.1”W).
60
0 50 100 150 200
0.00 0.04 0.08
abundance
phylogenetic originality
a
0 50 100 150 200
0.00 0.04 0.08
abundance
phenotypic originality
b
0.00 0.02 0.04 0.06 0.08 0.10
0.00 0.04 0.08
phylogenetic originality
phenotypic originality
c
61
Conclusão geral
Houve basicamente duas estratégias predominantes de defesa contra a
herbivoria nas espécies arbóreas de cerrado: “tolerância”, espécies com baixos
valores de defesa e altos valores nutricionais; e “baixa qualidade nutricional”,
espécies com altos valores de defesa e com baixos valores nutricionais. Como nós
não encontramos um sinal filogenético, a filogenia não foi o fator determinando o
conjunto de traços que as espécies apresentaram, logo, a herbivoria pode ser o
fator selecionando tais traços. As poucas estratégias que encontramos podem ser
resultado de uma série de filtros ambientais, reduzindo o banco de espécies
sequencialmente, entre eles a herbivoria.
Houve um grau de redundância na comunidade vegetal de cerrado, já que a
originalidade filogenética e originalidade fenotípica não estiveram relacionadas. A
maior proporção de originalidade esteve concentrada em poucas espécies,
indicando um grau de suscetibilidade a perda dessas poucas espécies. A
abundância não foi o fator predominante para a manutenção das funções no
cerrado.
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