Content uploaded by Silmary Alvim
Author content
All content in this area was uploaded by Silmary Alvim on Jun 18, 2018
Content may be subject to copyright.
69
BIOTROPICA 33(1): 69–77 2001
Leaf Gall Abundance on
Avicennia germinans
(Avicenniaceae) along
an Interstitial Salinity Gradient
1
Silmary J. Gonc¸alves-Alvim
2
Ecologia Evolutiva de Herbı´voros Tropicais/DBG, CP 486, ICB/Universidade Federal de Minas Gerais,
30161-970 Belo Horizonte, MG, Brazil
Ma´rcio C. F. Vaz dos Santos
Departamento de Oceanografia e Limnologia/UniversidadeFederal do Maranha˜o, Av. dos Portugueses s/n,
Campus Universita´rio do Bacanga, 65080-040 Sa˜o Luı´s, MA, Brazil
and
G. Wilson Fernandes
Ecologia Evolutiva de Herbı´voros Tropicais/DBG, CP 486, ICB/Universidade Federal de Minas Gerais,
30161-970 Belo Horizonte, MG, Brazil
ABSTRACT
We investigated the relationships among interstitial salinity, leaf sclerophylly, plant vigor, and population density for
the leaf galling insect Cecidomyia avicenniae (Diptera: Cecidomyiidae) on its host plant Avicennia germinans (Avicen-
niaceae). Sampling was done in six mangrove stands and in one varzea forest of Maranha˜o, northeast Brazil. At each
site, ten shoots were randomly taken on five A. germinans trees. From each shoot we counted the total number of
galls and recorded the shoot length (cm). We also recorded the average length, width, total area, and biomass of leaves
per shoot. Leaf sclerophylly was quantified by leaf biomass per unit area (g/cm
2
). Samples of interstitial water were
taken by a 1.3-cm PVC tube with 80 cm of depth, and salinity (ppt) was measured with a refractometer. Leaf
sclerophylly showed a positive relationship with interstitial salinity (R
2
5
0.77, P
,
0.05). We also observed positive
relationships between gall density per unit of leaf area (cm
2
) and salinity (r
5
0.36, P
,
0.05), and between gall
density and leaf sclerophylly (r
5
0.40, P
,
0.05). The salinity and the leaf sclerophylly together explained 22 percent
of the variation in gall density of C. avicenniae. We found a negative relationship between the number of galls per
centimeter and shoot length (R
2
5
0.50, P
,
0.05). Thus, longer shoots of A. germinans showed lower gall density.
Our results suggest that the gall density of C. avicenniae on A. germinans is affected by the salinity of host plant
habitat and by leaf sclerophylly along an interstitial salinity gradient.
RESUMO
Investigou-se a relac¸a˜o entre salinidade intersticial, esclerofilia da folha, vigor da planta e densidade de galhas provocadas
pelo inseto galhador foliar, Cecidomyia avicenniae (Diptera: Cecidomyiidae), em sua planta hospedeira Avicennia ger-
minans (Avicenniaceae). As coletas foram realizadas em seis mangues e em uma mata de va´rzea, no Maranha˜o, nordeste
do Brasil. Em cada local, dez ramos foram coletados aleatoriamente em cinco a´rvores de A. germinans. De cada ramo
foram obtidos o nu´mero total de galhas e o comprimento (cm). Me´dias do comprimento, largura, biomassa e a´rea
das folhas por ramo foram tambe´m registradas. A esclerofilia foliar foi quantificada atrave´s da biomassa por unidade
de a´rea foliar (g/cm
2
). Amostras da a´gua intersticial foram obtidas atrave´s de um tubo de PVC de 1,3 cm de diaˆmetro
a` uma profundidade de 80 cm, e a salinidade (ppm) medida com um refratoˆmetro. A esclerofilia das folhas apresentou
uma forte correlac¸a˜o positiva com a salinidade intersticial (R
2
5
0,77; P
,
0,05). Observou-se tambe´m correlac¸o˜es
entre a densidade de galhas por unidade de a´rea foliar (cm2) e a salinidade intersticial (r
5
0,36; P
,
0,05), e entre
densidade de galhas e a esclerofilia das folhas (r
5
0,40; P
,
0,05). Salinidade e esclerofilia juntas explicaram 22 por
cento da variac¸a˜o na densidade de galhas de C. avicenniae. Observou-se, ainda, uma relac¸a˜o negativa entre a densidade
de galhas por centı´metro e o comprimento do ramo (R
2
5
0,50; P
,
0,05). Portanto, ramos mais longos de A.
germinans apresentaram menor densidade de galhas. Nossos resultados sugerem que a densidade de galhas de C.
avicenniae em A. germinans e´ afetada tanto pela salinidade do habitat da planta hospedeira quanto pela esclerofilia ao
longo do gradiente de salinidade intersticial.
Key words: Avicennia germinans; black mangrove; Brazil; Cecidomyia avicenniae; herbivory; insect galls; plant stress;
plant vigor; saline stress.
1
Received 16 February 1999; revision accepted 1 February 2000.
2
Address for reprints.
70 Gonc¸alves-Alvim, Santos, and Fernandes
T
HE FACTORS THAT INFLUENCE THE DENSITIES OF HER
-
BIVORE INSECT POPULATIONS
include variation in host
plant quality, differential resistance, natural ene-
mies, and environmental variation that may act di-
rectly on herbivores or on their host plants (Stiling
1994). Studies on the role of plant quality on the
attack of herbivores have led to the development
of several hypotheses (White 1969, 1970; Feeny
1976; Bryant et al. 1983; Coley 1983; Coley et al.
1985; Bazzaz et al. 1987; Mattson & Haack 1987;
Price 1991).
White (1969) proposed the plant stress hy-
pothesis, which predicts that physiologically
stressed hosts are attacked more by herbivores than
are healthy hosts. The mechanism influencing this
pattern is said to be an increased level of amino
acids in plant tissue, which increases the chance of
offspring survival. In addition, stressed plants invest
less in secondary chemicals (e.g., tannin, resins, and
essential oils), making them more vulnerable to
herbivore attack (Rhoades 1979). Several studies
have corroborated this hypothesis (White 1970,
1976, 1984; Raffa & Berryman 1982; Rhoades
1983; Mattson & Haack 1987; Fernandes & Price
1988, 1991; De Bruyn 1995; Cobb et al. 1997).
The plant vigor hypothesis proposed by Price
(1991) states that insect herbivores having a larval
development which is associated with their host
plant growth processes should prefer to attack the
most vigorous plants or plant modules in which
subsequent larval performance is highest. Some
studies have corroborated the plant vigor hypoth-
esis (Price et al. 1987, 1990, 1997; Price 1991;
Hunter & Price 1992; Feller 1995; Preszler & Price
1995; Feller & Mathis 1997). Price (1991) also
indicated that these two hypotheses are not mu-
tually exclusive. Herbivores may perform better on
stressed plants or populations, but within an indi-
vidual plant, they may still prefer to feed on the
most vigorously growing plant parts; thus both hy-
potheses could be supported (Fernandes 1992,
Mopper & Whitham 1992).
Although it is necessary to test such hypotheses
to build general ecological theories, studies about
the role of vigor and stress on galling insect den-
sities in flooded forests are practically nonexistent.
Mangroves are important ecosystems due to their
ecological role and economic interests (Carmo et
al. 1995, Koch 1997); however, hypotheses ex-
plaining differences in herbivory have not been ex-
tensively tested in these ecosystems (Onuf et al.
1977, Lacerda et al. 1986, Feller 1995, Feller &
Mathis 1997).
In aquatic ecosystems, salt stress is restricted to
dry or seasonally dry climates. Its occurrence is due
to natural processes as well as to anthropogenic ac-
tivities (e.g., extraction and production of salt, hy-
droculture, and disturbances in the hydrology of
swamps). Salinity has been shown to affect primary
productivity, root/shoot ratios, leaf area, internode
length, leaf morphology, propagule size, and tree
structure in flooded forests (Barbour 1978, Lugo
et al. 1981, Santos 1989, Kathiresan & Thanga-
mara 1990, Lin & Sternberg 1992, Ghowail et al.
1993, Smith & Snedaker 1995). In addition, man-
grove forests that grow in salt stress are generally
considered oligotrophic ecosystems, and the adapt-
ed species have a characteristic physiognomy that
includes low stature, evergreen, and long-lived
scleromorphic leaves (Medina et al. 1990, Feller
1995).
Casual observation indicates that Avicennia ger-
minans (L.) Stearn. (Avicenniaceae) is frequently at-
tacked by a leaf galling insect, Cecidomyia avicen-
niae Cook (Diptera: Cecidomyiidae) in flooded
forests of Maranha˜o, Brazil. In this study, we in-
vestigated the effect of increased interstitial salinity
on leaf traits of A. germinans. We also considered
the following questions: (1) does an increase in in-
terstitial salinity increase the susceptibility of A. ger-
minans to attack by the galling insect C. avicen-
niae?; and (2) does the vigor of A. germinans shoots
influence the attack rates of C. avicenniae?
MATERIALS AND METHODS
S
TUDY SITES
.—The study was performed at seven
sites with flooded forests exposed to different saline
conditions that constituted an interstitial salinity
gradient. Sampling was done from August to No-
vember 1996 (dry season) in six mangrove stands
on Sa˜o Luı´s Island (2
8
32
9
S, 44
8
17
9
W) and Rosa´rio
(2
8
56
9
S, 44
8
15
9
W), and in one varzea forest at the
edge of the Munin River in Axixa´(2
8
51
9
S,
44
8
4
9
W) in Maranha˜o, northeast Brazil (Fig. 1).
The state of Maranha˜o has an equatorial climate,
with an average temperature of 25
8
C and 2000
mm annual average precipitation.
S
TUDY SYSTEM
.—Eleven species of the genus Avicen-
nia are common along the tropical coasts. Two spe-
cies of Avicennia are found in the state of Maran-
ha˜o, where A. germinans (black mangrove) is the
dominant species (Santos 1989). Avicennia germi-
nans is able to grow under natural conditions in
several aquatic habitats and tolerates a wide range
of salt concentration (Santos 1989). This tolerance
derives from high phenotypic plasticity in response
Leaf Gall Abundance along an Interstitial Salinity Gradient 71
FIGURE 1. Map with location of sampling sites in Maranha˜o, Brazil: site 1
5
Axixa´, site 2
5
Rosa´rio, site 3
5
Iguaı´ba, site 4
5
Arac¸agy-II, site 5
5
Arac¸agy-I, site 6
5
Raposa-I, and site 7
5
Raposa-II.
to salt, as well as to physiological and structural
adaptations such as the exclusion of salt by roots,
the collection and secretion of salts by glands in
the leaves, and the accumulation of salt in intra-
cellular spaces of leaves and roots (Scholander et al.
1966, Flowers et al. 1977, Levitt 1980, Sua´rez et
al. 1998). Cecidomyia avicenniae induces spheroid
galls on the abaxial and adaxial leaf surfaces of the
host plant (Gagne´ 1994). Galls are yellow–green,
glabrous, and one-chambered.
S
AMPLING
.—At each site, ten shoots were collected
from each of five haphazardly selected trees. The
term ‘‘shoot’’ describes the terminal season of
growth on a stem without lateral ramifications.
These shoots were cut to separate the growth area
72 Gonc¸alves-Alvim, Santos, and Fernandes
of the previous season by difference in color and
were taken to the laboratory where we measured
shoot length (cm), number of galled and ungalled
leaves per shoot, and total number of galls per
shoot. To observe the galling insect abundance in
flooded forests, two methods were used. Gall den-
sity was measured as the average number of galls
per leaf area, and as the average number of galls
per centimeter of shoot length.
Because leaf condition is a sensitive indicator
of plant stress in mangrove forests (Carmo et al.
1995), the status of the A. germinans plants was
inferred from leaf traits (i.e., width, length, bio-
mass, and area). Leaves were removed from the
shoots and photocopied. These photocopies were
scanned and imported into an imaging computer
program by which total area (cm
2
) was quantified
(De Moraes et al. 1998). We also measured leaf
width (cm) and length (cm). To quantify sclero-
phylly, we measured leaf biomass per unit area (g/
cm
2
), which varied directly with hardness or tough-
ness of leaves (Feller 1995 and references therein).
To obtain dry biomass (g), leaves were dried in an
oven at 70
8
C for 72 h to reach constant weight
and were weighed.
Samples of pore water were obtained using a
syringe fitted with a probe and flexible tubing into
a PVC tube (1.3 cm diam.) and inserted into the
soil to a depth of 80 cm. The salinity of these water
samples was measured with a field refractometer
(ppt; Bertness & Hacker 1994). Sampling at 80
cm depth better reflected the salinity of water taken
up by the roots of the plant (Koch 1997).
S
TATISTICAL ANALYSES
.—All the variables were sub-
mitted previously to the Ryan-Joiner test for nor-
mality and Bartlett’s test of homogeneity of vari-
ances (
a5
0.05). Transformation using decimal
logarithm (x) or decimal logarithm (x
1
1) were
used for better data adjustment to the normal dis-
tribution.
Differences in measurements of leaf traits per
plant and gall density per square centimeter (cm
2
)
of leaf area among sampling sites were compared
through a one-way analysis of variance (ANOVA)
or the nonparametric Mood median test. One-way
multiple comparisons-Tukey test was also per-
formed. Regression analysis was done by using leaf
sclerophylly as the dependent variable and intersti-
tial salinity as the independent variable. The rela-
tionships between gall density per unit of leaf area
(cm
2
) versus leaf sclerophylly and interstitial salin-
ity were tested through correlation and multiple
regression analyses (Zar 1996).
Shoot length was used as an indication of plant
vigor to facilitate comparisons with previous studies
on the plant vigor hypothesis. To assess how galling
insects respond to vigor, shoots were divided into
3.51-cm intervals. Correlation and linear regression
analyses were performed using the midpoint of
each of the length classes as the independent vari-
able and galling insect density as the dependent
variable (Price et al. 1987, Price 1991).
RESULTS
S
ALINE STRESS IN
A.
GERMINANS.
—We found a neg-
ative relationship between interstitial salinity and
the performance of A. germinans, as indicated by
our leaf measurements (Table 1). There was a de-
crease in leaf size (i.e., width, length, and area) for
A. germinans with increasing salinity (Table 1). The
largest lengths of A. germinans leaves were found
in stands near Axixa´ (in the varzea forest with 0
ppt salt concentration), while the smallest were in
mangrove stands sampled at Raposa (67 ppt; Table
1). We also observed smaller values of leaf sclero-
phylly on plants along the Munim River in Axixa´
(one-way ANOVA: F
6, 34
5
15.89, P
,
0.05; Tu-
key-test: P
,
0.05; Table 1). Additionally, leaf
sclerophylly showed a strong positive relationship
with salinity (R
2
5
0.77, F
1, 32
5
101.62, y
5
2
2.06
1
0.00682x, P
,
0.05; Fig. 2).
A
TTACK OF THE INSECT GALLING ON
A.
GERMINANS
.—
Along the salinity gradient, the incidence of C. av-
icenniae galls on shoots varied from 62 to 88 per-
cent (Fig. 3). We found positive relationships be-
tween gall density per unit of leaf area (cm
2
) and
leaf sclerophylly (r
5
0.40, P
5
0.018; Fig. 4), and
with salinity (r
5
0.36, P
5
0.032; Fig. 4). Inter-
stitial salinity (x
1
) and leaf sclerophylly (x
2
) togeth-
er explained 22 percent of the variation in gall den-
sity (R
2
5
0.22, F
2, 33
5
4.41, y
5
1.15
1
0.00279x
1
1
0.0427x
2
,P
,
0.05).
We observed a negative relationship between
the gall density (i.e., number of galls per centimeter
of length) and shoot length (R
2
5
0.50, F
1, 17
5
15.66, y
5
0.213
2
0.00251x, P
,
0.05; Fig. 5).
Therefore, galling insects were more abundant on
smaller shoots.
DISCUSSION
In contrast to other mangrove species (e.g., Rhizo-
phora mangle L., Rhizophoraceae) that have their
development limited by soil salinities
.
65 ppt
(Cı´ntron et al. 1978), A. germinans can support
Leaf Gall Abundance along an Interstitial Salinity Gradient 73
TABLE 1. Interstitial salinity, leaf measurements, and gall density (x¯
6
SE) of A. germinans (N
5
35) in seven sampling sites, and results of statistical analyses (
L
logarithmic decimal
transformation [x];
S
logarithmic decimal [x
1
1] transformation; * Mood median test and ** one-way ANOVA). Different letters represent statistically significant differences
(Tukey’s test, P
,
0.05).
Sampling
sites
Salinity
(ppt)
Leaf dry
biomass (g)**
Leaf area
(cm
2
)
L
**
Leaf length
(cm)*
Leaf width
(cm)*
Leaf sclerophylly
(g/cm
2
)
L
**
Gall density
(cm
2
)
S
**
Axixa´
Rosa´rio
Iguaı´ba
Arac¸agy-II
Arac¸agy-I
Raposa-I
Raposa-II
P
0
20
30
35
40
42
67
0.39
6
0.04
a
0.62
6
0.02
b
0.52
6
0.04
ab
0.44
6
0.04
a
0.35
6
0.03
a
0.37
6
0.03
a
0.31
6
0.05
a
,
0.05
47.10
6
3.50
a
51.15
6
3.60
a
41.89
6
2.98
a
26.56
6
1.95
b
21.07
6
2.92
bc
16.79
6
0.89
c
16.37
6
2.46
c
,
0.05
14.04
6
0.29
a
12.67
6
0.30
a
13.13
6
0.34
ab
9.44
6
0.34
bc
8.24
6
0.55
bc
7.84
6
0.48
c
7.25
6
0.18
c
,
0.05
5.33
6
0.21
a
5.64
6
0.22
a
4.84
6
0.18
a
3.92
6
0.28
b
3.66
6
0.30
bc
3.20
6
0.07
bc
3.13
6
0.18
c
,
0.05
0.008
6
0.0006
a
0.012
6
0.0006
b
0.012
6
0.0004
b
0.016
6
0.0009
bc
0.017
6
0.0012
bc
0.022
6
0.0028
c
0.020
6
0.0021
c
,
0.05
1.98
6
0.47
ab
1.44
6
0.31
ab
0.60
6
0.21
a
1.71
6
0.56
ab
4.54
6
0.89
b
2.77
6
0.64
b
4.04
6
0.64
b
,
0.05
FIGURE 2. Relationships between leaf sclerophylly
and interstitial salinity (ppt
5
parts per thousand).
FIGURE 3. Proportion of Avicennia germinans shoots
attacked by Cecidomyia avicenniae along an interstitial sa-
linity gradient.
and develop in hypersaline conditions through salt
exclusion and excretion processes. This fact was
confirmed by Su´arez et al. (1998), who observed
that A. germinans seedlings were adapted to high
hypersaline soils through increasing solute concen-
tration and cell elasticity.
Differences in sclerophylly of mangroves, how-
ever, have been attributed to a salinity gradient
(Feller 1995). Sclerophyllous leaves in hypersaline
mangroves have indicated marked drought and nu-
trient stress resistance (Camilleri & Ribi 1983), as
in the case of A. germinans trees. Thus, the better
performance of A. germinans in less saline sites may
be due to the great demand for energy necessary
to maintain physiological activities in hypersaline
mangroves, where only a small stock of available
energy remains for growth and development (Lugo
& Snedaker 1974).
Conversely, Feller (1995) found that sclero-
phylly was significantly affected by a nutrient treat-
ment in R. mangle (red mangrove) trees, and the
presence of dwarf forms was directly related to
74 Gonc¸alves-Alvim, Santos, and Fernandes
FIGURE 4. Relationships between gall density per
cm
2
on leaves of Avicennia germinans and (A) leaf scler-
ophylly, and (B) interstitial salinity. Logarithmic decimal
(x) or logarithmic decimal (x
1
1, where x
5
gall abun-
dance) transformation was used for better data adjust-
ment to the normal distribution.
FIGURE 5. Relationship between gall density per cen-
timeter of shoot and shoot length class (cm) on Avicennia
germinans. Logarithmic decimal (x
1
1) transformation
was used for better data adjustment to the normal distri-
bution.
phosphorous deficiency rather than salinity and
physiological drought; however, soil nutrient avail-
ability can be altered by hypersalinity (e.g.,Bow-
dish & Stiling 1998), which affects the perfor-
mance of mangrove trees. Also, nutrient limitation
is relative to soil type and plant species (Feller
1995). Experiments with A. germinans are needed
to develop a better understanding of the impact of
salinity and nutrient limitation on this species. Fu-
ture studies will focus on this question.
The high density of the galling insect on A.
germinans in hypersaline mangroves may reflect the
occurrence of more vulnerable plants under high
saline conditions, supporting the prediction of
White (1969, 1970, 1984). Similar results were ob-
tained in other studies (De Bruyn 1995, Cobb et
al. 1997, Bowdish & Stiling 1998). De Bruyn
(1995) observed a negative correlation between the
density of galls and shoot diameter of Phragmites
australis (Cav.) Trin. ex Steud (Poaceae); shoot di-
ameter decreased with increasing environmental
stress. Cobb et al. (1997) verified both in the field
and experimentally that the larvae of Dioryctria al-
bovitella Hulst (Lepidoptera: Pryralidae) preferen-
tially attacked stressed populations of Pinus edulis
Engelm. (Pinaceae), both at a local and regional
level.
Scleromorphic vegetation develops certain
traits, such as long-lived leaves, reduced probability
of abscission, low nutrition, and high concentra-
tion of chemical defenses in response of nutrient-
poor soil (Fernandes & Price 1988, 1991; Fernan-
des et al. 1994; Price et al. 1998). In opposition to
free-feeding herbivores, galling insects are com-
monly associated with scleromorphic vegetation
(Fernandes & Price 1988, Fernandes et al. 1994).
Sclerophyllous plants provide favorable and safe
sites for colonization that benefit galling insects
against environmental pressures (Price et al. 1998).
So, our results support the hypothesis that the
abundance of galling insects increases with plant
stress gradient and leaf sclerophylly (Fernandes &
Price 1988, 1991; Fernandes 1992; Price et al.
1998).
Contrary to our findings, some authors (New-
berry 1980, Farnsworth & Ellison 1991) have sug-
gested that salt solution on the leaf surface of Av-
icennia spp. could discourage establishment of in-
sect herbivores on leaves. Soto and Jimenez (1982)
observed low herbivore damage in mangroves oc-
curring in areas of high salinity, where mangrove
species attain higher internal salt concentrations;
however, J. Martel (pers. comm.) found that plants
of Solidago altissima L. (Asteraceae) growing in soil
of high salinity had a small effect on the gall-in-
ducing larvae of Epiblema scudderiana Clemens
(Lepidoptera: Tortricidae). Despite poor plant per-
formance, increasing soil salinity did not cause lar-
Leaf Gall Abundance along an Interstitial Salinity Gradient 75
val mortality or retard instar development, and gall
nitrogen concentrations were always much higher
when compared to that of stems.
Several studies with leaf miners and galling in-
sects have shown that some species select larger
leaves or shoots over smaller ones (Whitham 1978,
Mopper et al. 1984, Craig et al. 1989, Larsson
1989, Price 1991, Woods et al. 1996, Price et al.
1997). Whitham (1978) observed that females of
the leaf-galling aphid Pemphigus betae Doane (Ho-
moptera: Eriosomatidae) search out, colonize, and
defend larger leaves. Mopper et al. (1984) found
that leaf area was positively correlated with the den-
sity of the microlepidopteran leaf miner Stilbosis
quadricustella (Chambers) (Lepidoptera: Cosmop-
terigidae) on Quercus germinata Small. (Fagaceae).
Given that in saline forests the number of galls was
high on A. germinans plants despite smaller leaf
area, our results suggest that the indirect effect of
salt concentration appears to be stronger than the
direct effect of leaf area on the attack rate of the
galling insect.
Although there are some sampling limitations
in observational studies of tropical vegetation
whereby many trees do not flush synchronously
and some shoots may be available to attack while
others may have no suitable leaves and are unat-
tacked (P. W. Price, pers. comm.), our results in
this system do not provide support for the plant
vigor hypothesis (Cornelissen et al. 1997, Madeira
et al. 1997, Gonc¸alves-Alvim et al. 1999). We also
observed that the salinity of host plant habitat and
leaf sclerophylly affected the density of C. avicen-
niae galls on A. germinans. Because salinity and leaf
sclerophylly together explained only 22 percent of
the attack rate on A. germinans, we believe that
other factors, such as the variation in resistance
within species (e.g., plant genotype effect; Stiling
1994) and biotic factors, such as parasites and
predators, could also influence the population den-
sity of this galling herbivore.
ACKNOWLEDGMENTS
We thank L. Silva and V. Oliveira for field assistance, and
K. Floate, P. W. Price, R. Dirzo, E. Marques, D. Yanega,
and an anonymous reviewer for their comments, which
improved the manuscript. This study was done in partial
fulfillment for the specialist’s degree of S. J. Gonc¸alves-
Alvim in tropical ecology from Universidade Federal do
Maranha˜o and was supported by CAPES, CNPq
(521772/95–8), and FAPEMIG (1950/95).
LITERATURE CITED
B
ARBOUR
, M. G. 1978. The effect of competition and salinity on the growth of a salt marsh plant species. Oecologia
37: 93–99.
B
AZZAZ
, F. A., N. R. C
HIARIELLO
,P.D.C
OLEY
,
AND
L. F. P
ITELKA
. 1987. Allocating resources to reproduction and
defense. BioScience 37: 58–67.
B
ERTNESS
,M.D.,
AND
S. D. H
ACKER
. 1994. Physical stress and positive associations among marsh plants. Am. Nat.
144: 363–372.
B
OWDISH
,T.I.,
AND
P. S
TILING
. 1998. The influence of salt and nitrogen on herbivore abundance: direct and indirect
effects. Oecologia 113: 400–405.
B
RYANT
,J.P.,T.P.C
LAUSEN
,P.B.R
EICHARDT
,M.C.M
C
C
ARTHY
,
AND
R. A W
ERNER
. 1983. Carbon/nutrient balance
of boreal plants in relation to herbivory. Oikos 40: 357–386.
C
AMILLERI
,J.C.,
AND
G. R
IBI
. 1983. Leaf thickness of mangroves (Rhizophora mangle) growing in different salinities.
Biotropica 15: 139–141.
C
ARMO
, T. M., M. G. B
RITO
-A
BAURRE
,R.M.S.M
ELO
,S.Z
ANNOTTI
-X
AVIER
,M.B.
DA
C
OSTA
,
AND
M. M. M. H
ORTA
.
1995. Os manguenzais da baı´a norte de Vito´ria, Espı´rito Santo: um ecossistema ameac¸ado. Rev. Bras. Biol.
55: 801–818.
Cı´
NTRON
, G., A. E. L
UGO
,D.J.P
OOL
,
AND
G. M
ORRIS
. 1978. Mangroves of arid environments in Puerto Rico and
adjacent islands. Biotropica 10: 110–121.
C
OBB
, N. S., S. M
OPPER
,C.A.G
EHRING
,K.C
HRISTENSEN
,
AND
T. G. W
HITHAM
. 1997. Increased moth herbivory
associated with environmental stress of pinyon pine at local and regional levels. Oecologia 109: 389–397.
C
OLEY
, P. D. 1983. Herbivore and defensive characteristics of tree species in a lowland tropical forest. Ecol. Monogr.
53: 209–233.
,J.P.B
RYANT
,
AND
F.SC
HAPIN
III. 1985. Resource availability and plant antiherbivore defense. Science 230:
895–899.
C
ORNELISSEN
, T. G., B. G. M
ADEIRA
,L.R.A
LLAIN
,A.C.F.L
ARA
,L.M.A
RAU
´JO
,
AND
G. W. F
ERNANDES
. 1997.
Multiple responses of insect herbivores to plant vigor. Cieˆnc. Cult. 49: 285–288.
C
RAIG
, T. P., J. K. I
TAMI
,
AND
P. W. P
RICE
. 1989. A strong relationship between oviposition preference and larval
performance in a shoot-galling sawfly. Ecology 70: 1691–1699.
D
E
B
RUYN
, L. 1995. Plant stress and larval performance of a dipterous gall former. Oecologia 101: 461–466.
D
E
M
ORAES
, C. M., W. J. L
EWIS
,P.W.P
ARE
´
,H.T.A
LBORN
,
AND
J. H. T
UMLINSON
. 1998. Herbivore-infested plants
selectively attract parasitoids. Nature 393: 570–573.
76 Gonc¸alves-Alvim, Santos, and Fernandes
F
ARNSWORTH
,J.W.,
AND
A. M. E
LLISON
. 1991. Patterns of herbivory in Belizean mangrove swamps. Biotropica 23:
55–67.
F
EENY
, P. 1976. Plant apparency and the diversity of phytophagous insects. Rec. Adv. Phytochem. 10: 1–22.
F
ELLER
, I. 1995. Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle).
Ecol. Monogr. 65: 477–505.
,
AND
W. N. M
ATHIS
. 1997. Primary herbivory by wood–boring insects along an architectural gradient on
Rhizophora mangle. Biotropica 29: 440–451.
F
ERNANDES
, G. W. 1992. Adaptive distribution of gall-forming insects: patterns and mechanisms. Ph.D. dissertation.,
Northern Arizona University, Flagstaff, Arizona. 99 pp.
,C.F.L.L
ARA
,
AND
P. W. P
RICE
. 1994. The geography of galling insects and the mechanisms that result in
patterns. In P. W. Price, W. J. Mattson, and Y. Barranchikov (Eds.). The ecology and evolution of gall-forming
insects, pp 42–48. USDA For. Serv., St. Paul, Minnesota.
,
AND
P. W. P
RICE
. 1988. Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia
76: 161–167.
,
AND
. 1991. Comparisons of tropical and temperate galling species richness: the roles of environmental
harshness and plant nutrient status. In P. W. Price, T. M. Lewinsohn, G. W. Fernandes, and W. W. Benson
(Eds.). Plant-animal interactions: evolutionary ecology in tropical and temperate regions, pp. 91–115. John
Wiley and Sons, New York, New York.
F
LOWERS
, T. J., P. F. T
ROKE
,
AND
A. R. Y
EO
. 1977. The mechanism of salt tolerance in halophytes. Annu. Rev. Plant
Physiol. 28: 89–121.
G
AGNE
´
, R. J. 1994. The gall midges of the Neotropical region. Cornell University, Ithaca, New York.
G
HOWAIL
, S. I., A. M. A
BDEL
-M
ONEM
,W.M.E
L
-G
HAMRY
,
AND
N. E. S
ABER
. 1993. Preliminary studies on effect of
different salinity levels on germination, growth, and anatomy of mangrove (Avicennia marina). In H. Leith
and A. L. Masoom (Eds.). Towards the rational use of high-salinity tolerant plants, pp. 237–244. Kluwer
Academic, Dordrecht, The Netherlands.
G
ONC¸ ALVES
-A
LVIM
, S. J., M. L. F
ARIA
,
AND
G. W. F
ERNANDES
. 1999. Preference of four Neotropical species of galling
insects to shoot vigor. Ann. Soc. Entomol. Bras. 28: 147–155.
H
UNTER
,M.D.,
AND
P. W. P
RICE
. 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-
up and top-down forces in natural communities. Ecology 73: 724–732.
K
ATHIRESAN
, K.,
AND
T. S. T
HANGAMARA
. 1990. A note on the effects of salinity and pH on the growth of Rhizophora
seedlings. Ind. For. 116: 243–244.
K
OCH
, M. S. 1997. Rhizophora mangle L. seedling development into the sapling stage across resource and stress
gradients in subtropical Florida. Biotropica 29: 427–439.
L
ACERDA
,L.D.
DE
,D.V.J
OSE
´
,C.E.
DE
R
ESENDE
,M.C.F.F
RANCISCO
,J.C.W
ASSERMAN
,
AND
J. C. M
ARTINS
. 1986.
Leaf chemical characteristics affecting herbivory in a New World mangrove forest. Biotropica 18: 250–255.
L
ARSSON
, S. 1989. Stressful times for the plant stress-insect performance hypothesis. Oikos 56: 277–283.
L
EVITT
, J. 1980. Response of plants to environmental stress. Vol. II. Water, radiation, salt, and other stresses. Academic
Press, New York, New York.
L
IN
, G.,
AND
L. S
TERNBERG
. 1992. Effect of growth form, salinity, nutrient, and sulfide on photosynthesis, carbon
isotope discrimination, and growth of red mangrove (Rhizophora mangle L.). Aust. J. Plant Physiol. 19: 509–
517.
L
UGO
, A., G. C
INTRON
,
AND
C. G
OENAGA
. 1981. Mangrove ecosystems under stress. In G. W. Barret, and R. Rou-
senburg (Eds.). Stress effects on natural ecosystems, pp. 129–153. John Wiley and Sons, New York, New
York .
,
AND
C. S
NEDAKER
. 1974. The ecology of mangroves. Annu. Rev. Ecol. Syst. 5: 39–64.
M
ADEIRA
, B. G., T. G. C
ORNELISSEN
,M.L.F
ARIA
,
AND
G. W. F
ERNANDES
. 1997. Insect herbivore preference for plant
sex and modules in Baccharis concinna Barroso (Asteraceae). In A. Raman (Ed.). Ecology and evolution of
plant-feeding insects in natural and man-made environments, pp. 135–143. International Scientific, New
Delhi, India.
M
ATTSON
, W. J.,
AND
R. A. H
AACK
. 1987. The role of drought stress in provoking outbreaks of phytophagous insects.
In P. Barbosa and J. C. Schultz (Eds.). Insect outbreaks: ecological and evolutionary perspectives, pp. 365–
394. Academic Press, Orlando, Florida.
M
EDINA
, E., V. G
ARCIA
,
AND
E. C
UERVAS
. 1990. Sclerophylly and oligotrophic environments: relationship between leaf
structure, mineral nutrient content, and drought resistance in tropical rain forests of the upper Rio Negro
region. Biotropica 22: 51–64.
M
OPPER
,S,S.H.F
AETH
,W.J.B
OECKLEN
,
AND
D. S. S
IMBERLOFF
. 1984. Host-specific variation in leaf miner population
dynamics: effects on density, natural enemies, and behavior of Stilbosis quadricustella (Lepidoptera: Cosmop-
terigidae). Ecol. Entomol. 9: 169–177.
,
AND
T.G. W
HITHAM
. 1992. The stress paradox: effects on pinyon sawfly sex ratios and fecundity. Ecology
73: 515–525.
N
EWBERRY
,D.M
C
C. 1980. Infestation of the coccid Icerya seychellarum (Westw.) on the mangrove Avicennia marina
(Forsk.) Vierh. on Aldabra Atoll, with special reference to tree age. Oecologia 45: 325–330.
O
NUF
, C. P. D., J. M. T
EAL
,
AND
I. V
ALIELA
. 1977. Interactions of nutrients, plant growth, and herbivory in a mangrove
ecosystem. Ecology 58: 514–526.
P
RESZLER
,R.W.,
AND
P. W. P
RICE
. 1995. A test of plant-stress and plant-genotype effects on leaf-miner oviposition
and performance. Oikos 74: 485–492.
Leaf Gall Abundance along an Interstitial Salinity Gradient 77
P
RICE
, P. 1991. Plant vigor hypotheses and herbivore attack. Oikos 62: 244–251.
,N.C
OBB
,T.P.C
RAIG
,G.W.F
ERNANDES
,J.K.I
TAMI
,S.M
OPPER
,
AND
W. H. P
RESZLER
. 1990. Insect herbivore
population dynamics on trees and shrubs: view approaches relevant to latent and eruptive species and life
table development. In E. A. Bernays (Ed.). Insect-plant interactions, pp. 1–38. CRC, Boca Raton, Florida.
,G.W.F
ERNANDES
,A.C.F.L
ARA
,J.B
RAWN
,H.
BARRIOS
,M.G.W
RIGHT
,S.P.R
IBEIRO
,
AND
N. R
OTHCLIFF
.
1998. Global patterns in local number of insect galling species. J. Biogeogr. 25: 581–591.
,G.W.F
ERNANDES
,
AND
G. L. W
ARING
. 1987. Adaptive nature of insect galls. Environ. Entomol. 16:
15–24.
,H.R
OININEN
,
AND
J. T
AHVANAINEN
. 1997.Willow tree shoot module length and the attack and survival
pattern of a shoot-galling sawfly, Euura atra (Hymenoptera: Tenthredinidae). Entomol. Fenn. 8: 113–119.
R
AFFA
,K.F.,
AND
A. A. B
ERRYMAN
. 1982. Physiological differences between lodgepole pines resistant and susceptible
to the mountain pine beetle and associated microorganisms. Environ. Entomol. 11: 486–492.
R
HOADES
, D. F. 1979. Evolution of plant chemical defense against herbivores. In G. A. Rosenthal and D. H. Janzen
(Eds). Herbivores: their interactions with secondary plant metabolites, pp. 3–54. Academic Press, New York,
New York.
. 1983. Herbivore population dynamics and plant chemistry. In R. F. Denno and M. S. McClure (Eds.).
Variable plants and herbivores in natural and managed systems, pp. 155–220. Academic Press, New York,
New York.
S
ANTOS
, M. C. F. V. 1989. Structural patterns of hypersalinity stressed mangrove forests in the state of Maranha˜o,
northern Brazil. M.S. thesis. Colorado School of Mines, Golden, Colorado. 164 pp.
S
CHOLANDER
, P. F., E. D. B
RADSTREET
,H.T.H
AMMEL
,
AND
E. A. H
EMMINGSEN
. 1966. Sap concentrations in halophytes
and some other plants. Plant Physiol. 41: 529–532.
S
MITH
,S.M.,
AND
S. C. S
NEDAKER
. 1995. Salinity responses in two populations of viviparous Rhizophora mangle L.
seedlings. Biotropica 27: 435–440.
S
OTO
, R.,
AND
J. A. J
IMENEZ
. 1982. Ana´lisis fisiono´mico estructural del manglar de Puerto Soley, La Cruz, Guanacaste,
Costa Rica. Rev. Biol. Trop. 30: 158–161.
S
TILING
, P. 1994. Coastal insect herbivore populations are strongly influenced by environmental variation. Ecol.
Entomol. 19: 39–44.
S
UA
´REZ
, N., M. A. S
OBRADO
,
AND
E. M
EDINA
. 1998. Salinity effects on the leaf water relations components and ion
accumulation patterns in Avicennia germinans (L.) L. seedlings. Oecologia 114: 299–304.
W
HITE
, T. C. R. 1969. An index to measure weather-induced stress of trees associated with outbreaks of psyllids in
Australia. Ecology 50: 905–909.
. 1970. The nymphal stage of Cardiaspina densitexta (Homoptera: Psyllidae) on leaves of Eucalyptus fasciculosa.
Aust. J. Zool. 18: 273–293.
. 1976. Weather, food, and plagues of locusts. Oecologia 22: 119–134.
. 1984. The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food
plants. Oecologia 63: 90–105.
W
HITHAM
, T. G. 1978. Habitat selection by Pemphigus aphids in response to resource limitation and competition.
Ecology 59: 1164–1176.
W
OODS
, J. O., T. G. C
ARR
,P.W.P
RICE
,L.E.S
TEVENS
,
AND
N. S. C
OBB
. 1996. Growth of coyote willow and the
attack and survival of a mid-rib galling sawfly, Euura sp. Oecologia 108: 714–722.
Z
AR
, J. H. 1996. Biostatistical analysis. Prentice-Hall, Upper Saddle River, New Jersey.