Ecological Entomology (1994) 19, 1 1 1 - 120
The effects of host plant phenology on the demography
and population dynamics of the leaf-mining moth,
Cameraria hamadryadella (Lepidoptera: Gracillariidae)
EDWARD F. CONNOR, ROBERT H . ADAMS-MANSON,"
TIMOTHY G . C A R R t and M I C H A E L W . BECK*
Department of Environmental Sciences, Clark Hall, University of Virginia, Charlottesville, Virginia, and
Blandy Experimental Farm, Boyce, Virginia, U.S.A.
Abstract. 1. We examined the effects of variation in the timing of spring leaf
production and autumn leaf fall on the survival, mortality and abundance of
Cameraria hamadryadella on Quercus alba and Q.macrocarpu.
2. We monitored and manipulated the timing of foliation on field and potted
Q.alba trees and observed the abundance of C.hamadryadella on those trees.
We also monitored and manipulated the timing of leaf fall on Q.alba and
Q.macrocarpa trees in the field and observed its effects on survival, mortality
and abundance of C.hamadryadella.
3 . Variation in the timing of spring leaf production has no effect on C. hamudryadella abundance. However, a warm winter and spring in 1991 led to accelerated development and the imposition of a facultative third generation in one
out of ten years of observation.
4. In 1989, leaves fell relatively early and leaf fall in the autumn accounted for
more than SO% of the mortality of C.hamudryadella. in 1990 and 1991 leaves fell
relatively late and leaf fall induced mortality was substantially reduced and overwinter survival was markedly increased.
5. The abundance of C.hamadryadella remained constant in the spring and
summer of 1990 following the previous autumn's relatively early leaf fall, but
increased by 10-fold in the spring of 1991 following the relatively late leaf fall of
autumn 1990. The abundance of C. hamadryadella also increased 4-fold between
the summer of 1991 and the spring of 1992 after another autumn of relatively late
leaf fall. We attribute these increases in abundance in part to reduced mortality
because of later leaf fall.
6. Variation in the timing of autumn leaf fall may be responsible for initiating
outbreaks of C .hamadryadrlla.
Key words. Leaf-miner, oaks, Cameraria hamadryadella, host-plant phenology,
survival, mortality, population dynamics, Quercus, demography.
* Present address: Department of Biology, Nelson Biological
Labs, Rutgers University. Piscataway, NJ 08855. U . S . A .
Present address: Department of Biological Sciences, Northern Arizona University, Flagstaff, A Z 86011, U . S . A .
Present address: Department of Biological Sciences, Florida
State University, Tallahassee, FL 32306. U . S . A .
*
Correspondence: Dr E. F. Connor. Department of Environmental Sciences, Clark Hall, University of Virginia. Charlottcsvillc,
VA 22903, U . S . A .
Introduction
Leaf phenology has been suggested to play an important
role in the demography and population dynamics of herbivorous insects (Askew, 1962; Varley & Gradwell, 1958,
1963; Rockwood, 1974; Dixon, 1976; Holliday, 1977;
Oplcr, 1978; Owen, 1978; Witter & Waisanen, 1978; Faeth
e t a / . , 1981; Pritchard & James, 1984; Potter, 1985; West,
1985; Hunter, 1990, 1992). Apart from phenological effects
112
Edward F. Contior et al.
on ontogenetic changes in the chemistry, moisture content, toughness and pubescence of leaves and their potential effects on insect growth, survival, reproduction and
host selection, two distinct aspects of leaf-phenology have
been proposed to affect populations of herbivorous insects:
the timing of leaf production and the timing of leaf fall.
Variation in the timing of leaf production can be critical
for herbivorous insects whose emergence and persistence
is closely tied to the availability of suitable foliage (Rockwood, 1974; Opler, 1978; Auerbach & Simberloff, 1984).
Insects that emerge before bud burst, or after foliage has
matured, may experience high mortality or other more
subtle demographic effects. For example, after a 10-year
study of the univoltine winter moth, Operophtera brumata,
i n an oak forest, Varley & Gradwell (1958, 1963) concluded
that 'winter disappearance,' a combination of predation
and asynchrony between winter moth emergence and
leaf production, accounted for the marked variation in
abundance observed between years. Holliday (1977)
reached similar conclusions for winter moth populations
feeding on apple, and Dixon (1976) also implicated the
timing of leaf-production as an important factor determining the survival of newly hatched sycamore aphids,
Duepatiosiphum platunoides. On the other hand, Crawley
Kr Akhteruzzaman (1988) and Watt & MacFarlane (1991)
found no relationship between leaf production in oaks and
Sitka spruce and insect abundance. However, Hunter
( 1992)shows that the impact of variation in leaf production
phenology on insect populations can differ between sites
and years.
The importance of leaf abscission in the population
dynamics of insects was first recognized by Clark (1962,
1964) for psyllids, and later by Owen (1978) and Faeth
at al. (1981) for leaf-mining and other sessile insects.
Owen (1978) and Faeth et al. (1981) studied a number of
species of dipteran, lepidopteran and coleopteran leafminers whose development is restricted to a single leaf,
and reasoned that for leaf-mining insects early leaf fall will
most likely lead to mortality unless the larvae is near
pupation. o r has pupated (but see Kahn & Cornell, 1989,
for an alternative view). For leaf-miners that are not
restricted to a single leaf or other external feeding folivores,
larvae may be able to return to their host plant after leaf
fall. but experience a higher risk of mortality and an
energetic cost of locomotion while searching for their host
plant. Faeth rt ul. (1981) observed that as much as 39% of
the mortality of sonie species of leaf-mining insects could
h c attributed to 'early leaf abscission.' They defined 'early
l c d abscission' to be leaf fall that occurred prior to the
normal annual peak of leaf fall in the autumn. Williams &
Whithani (19%) also found early leaf abscission to account
for as much a s a 53% reduction in abundance of a gallforming aphid. I n a recent review, Stilling & Simberloff
(1989) illustrate that although the effect of early leaf
abscission on mortality in leaf-mining insects can be substantial, it varies considerably among species.
Variation in the timing of the period of peak leaf fall in
the autumn could also be important in the population
dynamics of herbivorous insects. If at the onset of leaf-fall
a substantial fraction of the insect population is composed
of life-history stages that are unable to enter the overwintering diapause, then leaf death and leaf fall will result
in high mortality rates and population declines. This
could be caused either by direct weather-induced insect
mortality associated with periods of leaf fall, or indirectly
via starvation brought on by early leaf death and leaf fall.
Dempster (1983) reviews a number of life-table studies
on Lepidoptera and implicates weather as an important
force that limits the length of time that food resources o r
oviposition sites are available, hence affecting subsequent
population change in a bottom-up manner (Hunter &
Price, 1992). Singer (1972) conclude that senescence of
Plantago erecta accounted for much of the mortality of
Euphydryas editha larvae because the host plant died
before the larvae could enter diapause. I n a study of the
population dynamics of the multi-voltine leaf-mining moth
Phylloitorycter (= Lithocolletis) hlaticardella on apple,
Pottinger & LeRoux (1971) found that a large fraction of
the larvae produced in the final generation of the growing
season fail to complete development and pupate. Barrett
& Brunner (1990) report similar observations for fhyllonorycter elmaella also feeding on apple, and conclude
that the onset of winter conditions results in direct mortality.
However, we suggest that mortality could also occur
because the leaves on which larvae feed, senesce and fall
before the larvae have gained sufficient mass to complete
development.
We performed a series of experiments to determine the
effects of variation in the timing of leaf production. leaf
fall and winter severity on the abundance, survival and
population dynamics of Cameraria hamadryadella on
oaks. We manipulated or observed the timing of leaf
production and leaf fall on potted oak saplings and o n
arboretum and forest trees, and exposed diapausing larvae
to different over-winter conditions.
Natural history of Cameraria hamadryadella
Cameraria hamadryadella (Clemens) (Lepidoptera:
Gracillariidae) is a bivoltine leaf-miner that feeds on oaks
in the subgenus Lepidobalanus (Hinckley, 1972; Maier &
Davis, 1989; Connor, 1991). Although populations of
C.hamadryadella are sparse, with densities usually less
than 0.1 mine per leaf, outbreak populations with densities
greater than twenty individuals per leaf are observed
(Solomon et al., 1980; Connor & Beck, 1993). ('.humudryadella over-winter as diapausing larvae within the leafmine in the leaf litter and emerge as adults i n the spring.
Host and leaf selection is accomplished by the ovipositing
female who cements eggs singly to the upper leaf surface.
Eggs hatch in 1-2 weeks, and the blotch mines of the first
generation appear between mid May and early June.
Development from egg to adult occurs on a single leaf,
and larvae feed for 4-6 weeks before pupating within the
mine. The first generation completes development and
mating and oviposition occur by late July or early August.
The second generation of leaf-mining larvae appears in
Host plant phenology and a leaf-mining moth
mid to late August and larvae feed until leaf senescence
and abscission occur, usually by the end of October.
Larvae enter diapause within their natal leaf to overwinter,
and to complete development, pupate, and emerge as
adults in the spring.
Methods
Overview of experimental design
To determine the effect of variation in the timing of leaf
production on the abundance of C.hamadryadella on white
oak, Quercus alba, we manipulated potted white oak trees
to either accelerate or delay leaf production. We also
observed the timing of bud break on field grown trees.
Potted trees and field grown trees were censused monthly
during the growing season to determine the abundance of
C.hamadryadella.
To determine the effects of variation in the timing of
leaf fall in the autumn on C.hamadryade1la. we marked
individual leaves with mines of C.hamadryadella on several
Q.alba and Q.macrocarpa trees and heated some trees
with orchard heaters in an attempt to extend leaf longevity.
The date of leaf fall and subsequent fate was recorded for
each leaf and leaf mine. We also removed a cohort of
mined leaves from the experimental trees each week to
simulate a wide range of dates of leaf fall.
To separate the effects of winter severity from the
effects of the timing of leaf fall on over-winter survival, we
over-wintered cohorts of leaves with mines of C.hamadryadella under ambient winter conditions and under two
experimentally imposed winter temperature regimes.
Leaf production experiments
Experiments with potted saplings. To determine if the
timing of leaf production affects the abundance of C.hamadryadella, we manipulated the time of leaf production on
potted saplings of Quercus alba L. Forty-five saplings each
approximately 1 m in height were potted in 13 litre pots in
the spring of 1981 and allowed to acclimate to the pots for
1 year. All plants were over-wintered in a common holding
area under ambient environmental conditions. Q.al6u bud
burst normally occurs in late April or early May. Fifteen
Q.alba plants were placed in a glasshouse heated at 20°C
on 18 March 1982 in order to accelerate leafing by raising
bud temperatures. Another group of fifteen plants were
kept out-of-doors and misted with water to evaporatively
cool the buds to delay leafing. These plants were misted
beginning on 14 April. An additional group of fifteen
plants were held out-of-doors and allowed to foliate at the
normal time. Plants brought into the glasshouse were in
full leaf by 15 April, unmanipulated plants were in full leaf
by 1 May, and misted plants were in full leaf by 15 May.
On 17 May 1982, prior to spring oviposition by C.hamadryadella, all plants were moved to a native oak forest at
the Ivy Creek Natural Area near Charlottesville, Virginia,
U.S.A. Plants were placed 3m apart in a 9 X 5 grid in a
113
region with an overstorey of predominantly Q.alba and
Q.rubra L. Plants from each treatment were assigned at
random to each location. Monthly from June to September
all leaves on each tree were counted and inspected for the
presence of C. hamadryadella. The abundance of C. hamadryadella was recorded as the number of mines per leaf. A
two-factor repeated measures ANOVA (time of foliation
and month of census) was performed on the data on
C.hamadryadella abundance. The data were assumed to
be multivariate normal, and the degrees of freedom of the
F tests were adjusted using the Huynh-Feldt epsilon (Winer
1971; O’Brien & Kaiser, 1985). One tree died during the
course of the experiment and several trees had abscised all
their foliage before the density estimates were made in
September, hence the degrees of freedom were reduced
commensurately.
Observations on forest trees. To determine if the timing
of leaf production affects the abundance of C.hamadryadella we observed the timing of foliation of a large
group of Q.alba trees at the Ivy Creek Natural Area
during the spring of 1982. From this large group of trees
we selected fifteen trees of approximately equal diameter
(75-85cm, D.B.H.) and height (20-25m), five from each
of three foliation classes: early (predominately foliated
prior to 1 May), normal (partially foliated by 1 May) and
late (buds predominantly closed on 1 May).
Monthly from June to August we estimated the abundance of C.hamadryadella by removing five branches each
with approximately twenty-five leaves from a height of
10m on each tree. The five branches removed from each
tree were pooled and each leaf was counted and inspected
for the presence of C. hamadryadella. Abundance was
calculated as the number of mines per leaf. A two-factor
repeated measures ANOVA (time of foliation and month
of census) was performed on the data on C.hamadryadella
abundance. as described above.
Leaf fall experiments
To determine the effects of the timing of leaf fall in the
autumn on the survival of C. hamadryadella, we monitored
and manipulated the time of leaf fall on a series of trees
located in the Orland E. White Arboretum at Blandy
Experimental Farm (see Connor & Beck, 1993, fordescription of site). The fates met by second-generation (overwintering) larvae were estimated using cohorts of marked
leaves in 1989, 1990 and 1991. During 1989, 300 leaves
with mines of C.hamadryadellu were marked at the commencement of the second generation on four individual
Q.alba and four Q.rnacrocarpa Michaux trees. A portion
of these leaves were bagged with fine mesh bags (0.5 mm)
so that survival and mortality caused by leaf fall could be
estimated without the confounding influence of natural
enemies. During the subsequent autumn, the ground
around each experimental tree was searched weekly and
fallen, marked leaves were collected. Of the 300 marked
leaves, 257 were recovered. I n 1990 and 1991, similar
cohorts of leaves with C.hamadryadella mines distributed
I14
Edward F. Connor et a/.
across five Q.alha and six Q.macrocurpa were individually
marked at the commencement of the second generation.
A portion of these leaves were bagged with fine mesh
hags. In 1990,567 leaves were recovered, and in 1991,335
leaves were recovered.
In 1989 all recovered marked leaves were over-wintered
under refrigeration at 3°C. In 1990 and 1991, recovered
marked leavcs were over-wintered in the field in wire
cages ( 1 cni mesh). In each year, leaves were brought into
the laboratory in early spring to allow C.hamadryadella
larvae to complete development. All mines were dissected
to determine the fate of each individual C.hamadryadella.
Each individual was classified as meeting one of four fates
(survived, parasitized, preyed upon, or died due to other
causes). A detailed description of the evidence used to
infer thcse fates is presented in Connor (1991) and Connor
& Beck (1993). Death by other causes could include
mortality due to a ‘hypersensitive’ response of the host
plant (Anderson etal. , 1989; Cappuccino, 1992), parasitoid
stinging without egg laying, leaf fall induced death, and
mortality caused by wintering conditions. However, we
believe that parasitoid stinging without egg laying is a
minor component of this mortality (Connor & Beck, 1993).
Data obtained from the cohorts of leaves without bags on
both host species were used to estimated the distribution
of fates met by second generation C.hamadryadella. Differences in survival and mortality rates between years
were examined using analysis of variance on the angularly
transformed proportions (Sokal & Rohlf, 1981; Auerbach,
1991). We applied logistic regression to determine if survival or death by other causes is affected by the timing of
leaf fall (Hosmer & Lemeshow, 1989). Only mines from
hagged leaves were used in this analysis, to remove the
confounding influence of natural enemies.
I n 1990 we manipulated the timing of leaf fall using two
approaches. First, we attempted to delay leaf death and
lcaf fall o n Q.mucrocarpa trees by heating each tree with
orchard heaters. On evenings when temperatures were
forecast to fall below freezing, heaters were lit and allowed
t o burn through the entire night. We marked leaves with
early-instar second-generation mines of C. hamadryadella,
and we bagged these leaves with fine mesh cloth (0.5 mm
mesh) t o protect larvae from natural enemies. A total of
210 leaves were bagged on six trees, with a minimum of
twenty leaves per tree. Three trees were heated with two
orchard heaters each and three trees served as controls.
The date of leaf fall was recorded for each marked leaf
recovered from the ground. Secondly, we removed five
unhiigged leaves with late-instar mines of C,hamadryadella
from each of six Q.macrocarpa trees during each week
froin 16 October to 19 November 1990 for a total of 150
leaves. These leaves provided a sample of larvae whose
dates of leaf fall were known precisely. All leaves were
over-wintered in the field and dissected to determine
survival and mortality rates the following spring.
Leaf fall phenology was estimated using cohorts of
marked leaves i n I989 and leaf collection baskets in 1990
and 1991. The distribution of dates of recovery of the
cohorts of marked leaves was used to estimate the phenology
of leaf fall in 1989. However, in 1990 and 1991, two 0.5 m2
baskets were placed under each Q.alba and Q.macrocarpa
tree to estimate the timing of leaf fall. Baskets were
emptied approximately every 8 days and the numbers of
Q.alba or Q.macrocarpa leaves were recorded.
The abundance of C.hamadryadella on Q.alha in the
arboretum was estimated in each generation by counting
the number of mines on each leaf on at least three twigs
containing twenty-five to fifty leaves on each of three
or more trees of each species. Density estimates were
obtained beginning with the second generation in 1989 and
continuing through the first generation of 1992.
Maximum and minimum temperatures and precipitation
were recorded daily at a weather station 0.5 km from
the experimental trees. The passage of storm fronts and
their associated winds were compiled from the monthly
climatological summaries for the nearest permanent
weather station prepared by the U.S. National Oceanic
and Atmospheric Administration.
Winter severity experiment
In order to determine if winter severity rather than the
timing of autumn leaf fall is responsible for variation in
over-winter survival, a portion of the leaves marked in
1991 were exposed to a period of refrigeration (3°C) or
freezing (-l0OC) from 15 February to 21 March 1992.
Leaves were randomly partitioned among over-winter
treatments for each leaf fall date to ensure that the effects
of the timing of leaf fall and winter severity could be
estimated. Mines were dissected and fates determined for
each larva as described above. A total of 370 over-wintering
larvae were examined in this experiment. We applied
logistic regression to determine if survival was related to
timing of leaf fall or over-winter treatment, and compared
the survival rates among over wintering treatments using a
x2 test for independence.
Results
Leaf production experiments
C.hamadryadella were observed at very low abundances
on both potted trees and forest trees in 1082 at the Ivy
Creek Natural Area. The average abundance of C.hamudryadella on potted trees was 0.0023 2 0.0WY individuals
per leaf and on forest trees it was 0.0012 0.0006 individuals per leaf (Fig. 1). These are among the lowest
densities reported for C .hamadryadella (Connor & Beck,
1993). The observation that densities were higher on
potted trees than on field trees on the first sampling date
indicates that the potted trees were placed i n the field prior
to oviposition by over-wintering females. The abundance
of C .hamadryadella generally increased over the growing
season, but no difference in the abundance of C.hamadryadella among trees with different dates of leaf production was detected (potted trees: F2,33 = 0.09, f = 0.9 12;
forest trees: F2.12= 1.19, P = 0.337). The higher average
*
Host plant phenology and a leaf-mining moth
0.35
115
ProDortion of Leaf Fall
0. alba
0. macrocarpa
A
0.3
0.25
0.0 1
0.2
0.15
0.006
0.1
-
0.05
n
0.012
0.0 1
0.008
0.000
0.004
June
July
Augurt
September
Mines/Leaf
I
!
0.3
Prooortion of Leaf Fall
Q. macrocarpa
B
0.25
I
0.2
0.15
0.alba
0.1
"
June
July
Auguet
0.05
Month
Fig. 1. Abundance of Cameraria hamadryadella on trees with
differing leaf production phenologies: (A) potted trees and (B)
0
Sep 14
Sep 28
Oct 12
Oct 28
Nov
Nov 23
Oct 26
Nov 9
Nov 23
Proportion of Leaf Fall
field trees. Wide bars depict average densities and narrow bars
depict one standard error.
abundance of C.hamadryadella on potted trees is consistent
with observations of higher densities lower in the crown of
host trees (E. F. Connor, personal observation).
Leaf fall experiments
During the autumn of 1989, more than half of all Q.alba
leaves had fallen by 18 October whereas the median date
of leaf fall for Q.macrocarpa was not until 4 November
(Fig. 2A). During the autumn of 1990 the median date of
leaf fall for Q.alba was 29 October and for Q.rnacrocarpa
it was 12 November (Fig. 2B). In 1991 the median date of
leaf fall for Q.alba was 31 October and for Q.macrocarpa
it was 29 November. In every year, leaf fall from Q.macrocarpa occurred later than from Q.alba. Furthermore, the
median date of leaf fall was at least 8 days later in 1990 and
1991 than in 1989 for both species. The average date
of abscission for the marked leaves on the heated and
unheated Q.macrocarpa trees did not differ ( I = 1.57,
df = 4, P = 0.192).
Examination of the local temperature and precipitation
data, and the regional data on winds, yields no striking
differences between years that could easily explain the
differences in leaf fall patterns. The date of first frost was
9, 20 and 14 October respectively during 1989, 1990 and
1991. In 1989 the period between 1 September and 15
October had more days with precipitation (events of
greater than 2cm of rain) and strong winds (gusts greater
than 48kph) than did 1990 and 1991.
i
M Q. macrocarpa
Sep14
Sep 28
Oct 12
Fig. 2. Timing of leaf fall from Quercus alba and Quercus macrocarpa from the Orland E. White Arboretum at Blandy Experimcntal Farm in (A) 1989, (B) 1990 and ( C ) 1991. Data represent
the percentage of leaf fall occurring in each time period. Arrows
mark the median dates of leaf fall for each specics.
On both Q.alba and Q.macrocarpa, significantly higher
proportions of second-generation C.hamadryadella died
due to other causes in 1989 than in 1990 (F1,,s= 6.32,
P < 0.03), and 10 times more second-generation C.hamadryadella survived in 1990 than in 1989 (F1,15=71.35,
P < 0.0001, Fig. 3). In 1991, over-winter survival rates for
C .hamadryadella declined somewhat relative to the values
observed in 1990, but remained significantly higher than
those estimated in 1989 (F,,ls = 16.15, P < 0.003). However, survival rates were significantly higher on Q.macrocarpa than on Q.alba in 1991 (Fl,h=9.48, P<O.03).
Mortality due to other causes in 1991 was similar to the
high levels observed in 1989 ( F I . =~ 0.617,
~
P > 0.4).
Logistic regression indicated that the probability of
survival was directly related to the date of leaf fall in 1989
and 1991, but not related to the date of leaf fall in in 1990.
116
Edward F. Connor et al.
ProDortion
I A
0.6
I
Table 1. Summary of the logistic regression examining the effect
of datc of leaf fall on survival and 'death by other causes' [or
Qucrcus alba and Quercus macrocarpa in 1989 ( n = 174). IW0
( n = 385) and 1991 ( n = 459). All leaves were bagged i n ordcr to
estimate the cffects of timing of leaf fall o n mortality without the
confounding influence of parasitism and predation. The treatment
effect in 1991 is the means of over wintering the Icavcs. B =
regression coefficient, x2 = change in deviance x2 statistic, df =
degrees of freedom, and P = significance level.
0.4
0.2
Variable
n
Paras1tlsm
Predat Ion
Other
Survival
Proportion
0.6 -
B
I
0.4
n
Parasltlsm
Prsdatlon
Other
Survival
Fate
Fig. 3. Fatcs met by second-generation Carncraria harnudryadella
on ( A ) Querrui alba and (B) @.macrocarpa during 1989, 1990
and 1991. Wide bars depict average proportion of cohort meeting
each fate on each trcc: narrow vertical bars depict one standard
error.
X2
Survival
Species
Datc
-0.0120
0.0395
O.(X)3
6.278
Death by other causes
Species
-0.1481
Date
-0.0525
0.851
19.73
-0.0707
(x2
(x'
P
1
1
0.9580
0 .o122
0.3562
0.0001
1
0.370
0 . 109
-0.0022
Death by other causes
-0.1117
Species
Datc
0.0138
1
0.624
2.947
0.4915
0.7417
0.4295
0.0861
1991
Survival
Species
Date
Treatment
-0.0907
0.0093
0.1510"
Death by other causcs
0.1081
Species
Date
-0.0083
Trcatment
-0.0895"
Furthermore, the probability of dying due to other causes
was inversely related to the date of leaf fall in 1989 and
1991; it was independent of the date of leaf fall in 1990
(Table I ) . However, combining probabilities using Fisher's
method indicates that over the 3 years of study, survival
rates were directly related
= 16.25, df = 6, P < 0.05),
and death by other causes was inversely related to the date
of leaf fall
= 28.62, df = 6, P < O.OO()S, Sokal & Rohlf,
1981). The probability of survival was unrelated to host
species in all years, and death by other causes was related
to host species only in 1YY1 (Table 1). For the cohort of
larvae on Q.rnucrocarpu leaves removed by hand on
specific dates throughout the autumn of 1990, the probability of dying due to other causes was strongly and inversely related to the date of leaf removal and the probability
of surviving was strongly and directly related to the date of
leaf removal (Table 2).
Density estimates of C. humadryadellu on Q.alba made
in each generation between the second generation of 1989
and the second generation of 1992 show that densities
increased by an order of magnitude between the second
generation of I990 and the first generation of 1991, and
4-fold between the second generatim of 1991 and the first
generation of 1902 (Fig. 4).
df
1989
1990
Survival
Species
Datc
0.2
"
B
0.934
4.563
4.498
1
1
2
0.3339
0.0327
0.1055
3.824
3.262
1.566
1
0.0505
0.0709
0.4571
1
2
* Rcgrcssion coefficents averaged across categorics.
Table 2. Summary of the logistic regression examining the ef-
fect of datc of leaf fall on survival and 'death by other causes'
for leaves removed by hand from Querru,r rnarrorarpa in l"0
(n = 148), B = regression coefficient. x2 = change in deviance x2
statistic, df = degrees of freedom, and P = significance levcl.
Variable
Survival
Date
B
0.0465
Death by other causes
-0.056
Date
X2
df
P
8.33
1
0.0039
9.2bb
I
0.0023
Winter severity experiment
Approximately equal proportions of larvae survived in
each of the over-wintering treatments
= 1.76, df = 2,
P >0.4). In fact, the highest rate of survival occurred
among larvae exposed to a period of freezing conditions
(x'
HOSIplant phenology arid a leaf-mitiing moth
Mines/Leaf
t
First Generation
Second Generation
_. .
1989
1990
1991
1992
Year
Fig. 4. Density of Cameraria hamadryadella o n Querrus alba in
the Orland E. White Arboretum between 1989 and 1992. Broad
vertical bars depict average densities on sample trees, and narrow
vertical bars depict one standard error.
(45%), whereas 37% of larvae over-wintered in the field
or at 3°C survived. Logistic regression analysis indicated
that the probability of survival was inversely related to the
date of leaf fall (change in deviance
= 4.106, df = 1,
P < 0.05), but not related to over-wintering treatment
(change in deviance x2 = 1.91, df = 2, P > 0.35).
x2
Discussion
Effects of leaf production phenology on C .hamadryadella
Our observations on the abundance of C.hamadryadella
on Q.alba trees with different bud-break phenologies
suggests that variation in the timing of spring leaf production is largely unimportant to the demography or
population dynamics of C.hamadryadella. We found no
relationship between date of foliation and C.hamadryadella
abundance for either indigenous field trees o r manipulated
potted saplings whose foliation dates differed by as much
as 1 month. Our result is consistent with the results of
similar phenological manipulation experiments performed
on birch, Betula pendula, by Fowler 8 Lawton (1984).
They found no effect of accelerating or delaying foliation
on the abundance of birch leaf-miners. However, Auerbach
(1991) found that the timing of bud burst was critical
in determining the abundance of the leaf-miner Phyllonorycter sulicifolieila which preferentially oviposits on
yound leaves of aspen (Populus sp.).
The lack of a relationship between date of foliation
and C.hamadryadella abundance was not completely
unexpected. Upon bud-break the developing leaves of
Q.alba are supple and covered by a dense pubescence on
both the upper and lower leaf surface. As leaves expand to
their mature size, the pubescence is shed, particularly
from the upper surface. While spring emergence of C.hamadryadella is coincident with bud burst (we observed adults
in early May), oviposition is slightly delayed relative to
leafing so that females encounter expanded leaves with
less pubescence to interfere with oviposition. Leaves on
117
trees with later dates of bud-break appear to mature
rapidly, reaching maturity at the same time as trees that
leaf earlier probably because they experience higher
ambient air temperatures. West (1985) suggests that the
delayed emergence of leaf mining insects attacking oaks is
an evolved response to avoid competition with spring
defoliating macrolepidoptera. However, since many leafmining insects cement their eggs to the leaf surface, we
suggest that delayed oviposition may be an adaptation
to ensure that eggs can be securely attached to the leaf
surface, rather than a mechanism to avoid competition.
The only leaf-miners known to attack expanding leaves on
oaks are members of the Eriocraniidae (Lepidoptera).
Species in this family have piercing ovipositors and insert
eggs within leaves rather than cement them to the surface
(Opler, 1974; Connor, 1979).
Our experiments also failed to show any affect of accelerated leafing on C .hamadryadella demography. However, this may arise in part because our experiment only
manipulated the timing of leafing and not the emergence
date of C .hamadryadella. A warm winter and early spring
would not only accelerate leafing, but also accelerate the
development and emergence of C.hamadryadelu. In
response to an unusually warm winter and spring in 1991,
we observed bud break and emergence of C .hamadryadella
10-14 days earlier than on average, and this allowed
between 4% and 8% of the population of C.hamadryadella
in the arboretum to enter a facultative third generation in
late summer of 1991. Hence the effects of accelerated
leafing and emergence in the spring are manifested by
earlier development of each summer generation, and the
potential for a facultative third generation. In 10 years of
study in the arboretum, C .hamadryadella has only entered
a third generation in one year.
Effects of iea,f fall phetioiogy on C .hamadryadella
In 1989 C.hamudryadella feeding on leaves that fell in
early autumn tended to die due to other causes, while
larvae feeding on leaves that fell in late autumn tended to
survive. Death due to other causes accounted for over
50% of niortality of second-generation C.hamadryadella
on both Q.alba and Q.macrocarpa, and only 5% of the
population survived to emerge in 1990. In the following
spring the density of first-generation C.hamadryadella was
no different than in the second generation of 1989.
In the autumn of 1990 the chances of surviving o r of
dying due to other causes were unrelated to the timing of
leaf fall on unmanipulated leaves. However, when leaves
were removed by hand to ensure a wide range of leaf fall
dates, the chances of surviving or dying due to other
causes was strongly related t o date of leaf removal. Combined with our experiment demonstrating that winter
severity per SC has no effect on over-wintering survival,
our results argues that leaf fall is the proximal cause of
death ‘due to other causes’ in autumn-feeding larvae. This
is in spite of the fact that some insect specics experience
significant over-winter mortality even when exposed to
118
Edward F. Connor et al.
winter temperatures substantially above the super-cooling
point (Bale, 1987, 1991).
Death due to other causes accounted for only 22% and
36‘26 mortality on Q.alba and Q.macrocarpa in 1990,
respectively, and more than 50% of second-generation
C.hutnadryadella survived to emerge in 1991. In 1990 the
median date of leaf fall for both Q.alba and Q.macrocarpa
was at least 8 days later than in 1989, and early-instar
second-generation mines appeared 10 days earlier than
in 1989. In the following spring of 1991 the density of
C .hamadryadella on both host species increased by an
order of magnitude relative to the densities observed in
1989 and 1990. We interpret these results to indicate that
the timing of leaf fall in the autumn can have enormous
consequences to the demography and population dynamics
of C .hamadryadella.
The timing of leaf death and leaf fall in the autumn is
determined ultimately by the response of the host plant
to photoperiod (Addicott, 1982). However, the more
proximal causes of leaf fall appear to be related to the
onset of sub-freezing temperatures and to wind and rain.
The early autumn of 1989 was characterized by early
frosts, more rainfall, and higher winds than 1990, which
in turn was higher in these attributes than 1991. These
observations are consistent with the observation that
median dates of leaf fall for both Q.alba and Q.macrocarpa
were earliest in 1989 and latest in 1991.
The data on timing of leaf fall and the mortality caused
by other causes in 1991 is at first examination puzzling, but
appears to be related to death due to early leaf fall in the
facultative third generation which can occur in years with
long growing seasons. The median date of leaf-fall was
later for both Q.alba and Q.macrocarpa in 1991 than in
1990, but death by other causes accounted for as much
mortality in 1991 as it did in the early leaf fall year of 1989.
Survival rates remained higher in 1991 than in 1989, but
were substantially reduced compared to 1990. Given the
late leaf fall in 1991, we would normally have expected
high survival rates and low rates of death by other causes.
However, because of the imposition of a facultative third
generation in 1991, many early-instar third-generation
larvae remained when leaves fell and hence were killed by
‘death due to other causes.’ The higher survival rates and
later leaf fall on Q.macrocarpa than on Q.alba in 1991 and
the ‘species’effect on ‘death by other causes’ in the logistic
regression for 1991 are also consistent with this observation.
Changes
iti
abutidatice of C .hamadryadella
We interpret the 10-fold increase in abundance observed
between the autumn of 1990 and the spring of 1991 to arise
largely because of reduced mortality due to later leaf fall
in 1990. I n the spring following the autumn of 1989 in
which early leaf fall was the major source of mortality, the
abundance of C.hamadryadella was unchanged. However,
densities increased markedly in the spring of 1991 following
an autumn in which leaves fell later, and mortality caused
by leaf fall was substantially lower.
Early leaf fall may not be entirely responsible for the
lower survival rates and higher mortality due to other
causes observed in 1989. Other factors affecting the rates
of development of C .hamadryadella may indirectly affect
mortality rates associated with leaf fall. In both 1989 and
1990 early-instar first-generation mines of C.hamadryadella
were first observed between 1 and 5 June, and average
daily temperatures for June, July and August were similar
in both years. Still, early-instar second-generation mines
of C .hamadryadella appeared approximately 10 years later
in 1989 than in 1990. Whatever the cause, delayed hatching
of second generation eggs could increase the probability
that larvae will not gain sufficient mass to enter diapause
when leaves fall.
In addition to the marked drop in death due to other
causes between the second generation in 1989 and 1990,
all remaining mortality rates also fell between 1989 and
1990. This is particularly true for rates of parasitism on
Q.macrocarpa which dropped from 38% in 1989 to 15% in
1990. Whether or not these differences are related to
the differences between years in the timing of initiation
of second-generation mines or to leaf longevities is not
known. The fact that leaves were allowed to abscise
naturally in 1989 and removed by hand in 1990 from
Q.macrocarpa could also explain the higher estimate
of mortality due to other causes and lower estimate of
parasitism on Q.macrocarpa than on Q.alba in 1990.
Hand-removed leaves were detached earlier than naturally
abscised leaves and therefore should display a higher rate
of mortality due to other causes.
In the spring of 1992 the abundance of C .hamadryadella
increased again by a factor of 4 compared to the previous
year. Leaf fall occurred even later in 1991 than in 1990,
especially on Q.macrocarpa. However, leaf fall induced
death by other causes was as high in 1991 as in 1989, partly
because of high rates of larval mortality in the facultative
third generation. However, the fact that between 4% and
8% of second-generation individuals matured early enough
to emerge and attempt a third generation in late summer,
suggests that a large percentage of second-generation
larvae gained sufficient mass to enter the larval diapause
and successfully overwinter. Thus, late leaf fall, combined
with earlier completion of development and lower rates of
mortality from natural enemies, accounts for the population increase between 1991 and 1992.
Other studies have shown that early leaf abscission prior
to the autumn peak of leaf fall can have substantial effects
on survival (Faeth el al., 1981; Pritchard & James, 1984;
Potter, 1985; Williams & Whitham, 1986; Connor, 1988;
Stiling & Simberloff, 1989; Auerbach, 1991). Our results
and those of Pottinger & LeRoux (1971) and Barrett &
Brunner (1990) suggest that the timing of autumn leaf fall
may be equally or more important. The observation of a
10-fold increase in survival and a subsequent 10-fold
increase in abundance following a year with relatively late
leaf fall in comparison to a year with relatively early leaf
fall, argues that autumn leaf fall phenology has important
effects on the demography and population dynamics of
C.hamadryadella. Only continued monitoring of leaf fall
Host pluiit pheriology arid a leaf-mining moth
patterns, causes of mortality, and abundance, will allow
us to determine how often outbreaks of Cameraria humadryadella are caused by the timing of autumn leaf-fall.
Acknowledgments
We thank R. Arnold, K. Connor, J. Dooley, J. Everett,
G. McQuate and R. Wrubel for their assistance with
the field work. We thank the Board of the Ivy Creek
Foundation for permission to use forests at the Ivy Creek
Natural Area, and Mr and Mrs Bedford Moore for providing
access to our field sites. The manuscript benefited from
careful reviews by M. Bowers, J. Dooley, J. Hjalten, S.
Matter, M. Nuckols, P. Price, H. Roininen, C. Sacchi, M.
Taverner, G. Turner, E. English, and two anonymous
reviewers. This research was supported in part by NSF
grants DEB80-21779, BSR 88-12989 and BBS 91-12013.
119
of Camerariu hamadryadella (Lcpidoptera: Gracillariidac)
on four species of host plants. Ecological Entomolog.~, 16.
315 -322.
Connor. E.F. & Beck, M. (1993) Density-related mortality in
Cameraria humudryade//a (Lcpidoptera: Gracillariidae) at
epidemic and cndcmic densities. Oikos. 66, 515-525.
Crawlcy, M.J. & Akhteruzzaman, M. (1988) Individual variation
in the phcnology of oak trccs and its consequcnccs for herbivorous insects. Functional Ecology, 2, 409-415.
Dcmpstcr, J.P. (1983) Thc natural control of populations of
butterflies and moths. Biological Reviews, 58. 461-481.
Dixon, A.F.G. (1976) Timing of egg hatch and viability of the
sycamore aphid, Drepanosiphum platanoides (Schr.), at bud
burst of sycamore, Acer pseudoplatanus L. Journal of Animal
Ecology. 45. 593.
Facth, S.H., Connor, E.F. &i Simberloff, D. (1981) Early leaf
abscission: a iicglcctccl source of mortality for folivores.
American Naturalist. 117, 409-415.
Fowler, S . V . & Lawton, J.H. (1984) Foliage preference of birch
herbivores: a ticld manipulation cxpcriment, Oikos. 42.
230-248.
References
Addicott, F.T. (1982) Abscission. University of California Press,
Berkeley, California.
Anderson. S.S., McCrea. K.D., Abrahamson, W.G. & Hartzel,
L.M. (1989) Host genotype choice by the ball gallmaker Eurosta
solidaginis (Diptera: Tephritidae). Ecology, 70, 1048- 1054.
Askew, R.R. (1962) The distribution of galls of Neuroterus
(Hymcnoptera: Cynipidae) on oak. Jounral of Animal Ecology,
31, 439-455.
Auerbach, M. (1991) Relative impact of interactions within and
between trophic levels during an insect outbreak. Ecology. 72,
1599- 1608.
Auerbach, M. & Simberloff, D. (1984) Responses of leaf miners
to atypical lcaf production patterns. Ecological Entomology, 9.
361-367.
Bale, J.S. (1987) Inscct cold hardiness: freezing and supercooling:
an ecophysiological perspective. Journal of Insect Physiology,
33, 899-908.
Bale, J.S. (1991) Insects at low ternperaturc: a predictable relationship? Functional Ecology, 5, 2Y 1-298.
Barrctt, B.A. & Brunner, J.F. (1990) Temporal distribution of
Phyllonorycter elmaella (Lepidoptera: Gacillariidac) and its
major parasitoid, Pnigalio flavipes (Hymenoptcra: Eulophidae),
in Washington apple orchards. Environmental Entomology, 19,
362 -369.
Cappuccino, N . (1992) The nature of population stability in
Eurosta solidaginis, a nonoutbrcaking herbivore of goldenrold.
Ecology. 73, 1792-1801.
Clark, L. R. (1962) The gencral biology of Cardiaspitia albitexfuru
(Psyllidac) and its abundance in relation to weather and parasitism. Australian Journal of Zoology, 10, 537-586.
Clark, L.R. (1964) Thc population dynamics of Cardimpinu
albitextura (Psyllidac). Australian Journal of Zoology, 12,
362 -380.
Connor, E.F. (1979) Population and community ccology of
lcaf-mining insccts on oak. Ph.D. dissertation, Florida Statc
University, Tallahassee, Florida.
Connor. E.F. (1988) Cohort and death asscmblagc cstimatcs
of thc survival and mortality of Rrachys ovatus (Wcbcr)
(Colcoptera: Buprestidac). American Midlund Naturalist. 120.
150- 155.
Connor. E.F. (1991) Colonization, survival, and causcs of mortality
Hincklcy. A.D. (1972) Comparativc ecology o f two leafminers o n
white oak. Environmental Entomology, I , 258-261.
Holliday. N.J. (1977) Population ccology of wintcr moth (Operophteru brirmutu) on apple i n relation to larval dispersal and the
time of bud burst. Journal of’Applied Ecology, 14, 800-813.
Hosmcr. D.W. & Lcmeshow, S. (1989) Applied Logistic Regression. John Wilcy and Sons, Ncw York.
Hunter, M.D. (1990) Differcntial susccptihility to variablc plant
phcnology and its role in competition bctween two insect
herbivorcs on oak. Ecologicul Entomology, 12, 373-382.
Hunter, M.D. (1902) A variable insect-plant interaction: thc
relationship bctwecn tree budburst phenology and population
levels of insect herbivores among trccs. Ecological Entomology.
17, 91 -95.
Huntcr, M.D. &i Price, P.W. (1992) Playing chutes and ladders:
heterogeneity and the relative roles of bottom-up and top-down
forces in natural communities. Eco1og.y. 73. 724-732.
Kahn, D.M. & Corncll, H.V. (1989) Lcafmincrs, early lcaf
abscission, and parasitoids: a tritrophic interaction. Ecology,
70. 1219- 1226.
Maicr, C.T. & Davis, D.R. (1989) Southern Ncw England host
and distributional records of Lithocolletinc Gracillariidae
(Lcpidoptera). Miscellaneous Publications of the Entomological
Sociqy of’America, 70.
O’Bricn. R.G. & Kaiser. M.K. (198s) MANOVA methods for
analyzing rcpcatcd measurcs designs: an cxtcnsive primer.
Psychological Bulletin, 97. 3 16-333.
Oplcr, P.A. (1974) Biology. ccology, and host spcciticity of
microlcpidoptcra associated with Quercus agrifolia (Fagaccac).
University of California Publications in Entomolog.v, 75, 1-X3.
Oplcr, P.A. (1978) Interaction of plant lifc history components
as rclatcd to arboreal hcrbivory. The Ecology of Arboreal
Folivores (cd. by G. G. Montgomery). pp. 23-31. Smithsonian
Institution Press, Washing ton, D .C .
Owcn. D.F. (1078) The effect of a consumcr Phyorn.vza ilicis
o n scasonal Icaf-fall in thc holly 1L.u ar~uijolium.Oikos, 31.
268-271.
Pottcr. D.A. (IYX.5) Population rcgulation of thc nativc holly lcaC
;~
Locw (Diptcra: Agromyzidac), on
miner, P h v t o r n ~ ~ilicicola
American holly. Oecologia, 66.499-505.
Pottingcr. R.P. & LcRoux, E.J. (1971) The biology and dynamics
of Lithocolletis hlaricardellu (Lcpidoptcra: Gracillariidac) on
applc i n Qucbcc. Memoirs of rlrr Enrornologicul Societv of’
Canada. 77. 1-437.
120
Edward F. C o n n o r et al.
Pritchard, I.M. & James, R. (1984) Leaf fall as a source of leaf
miner mortality. Oecologia, 64, 140-141.
Rockwood. L.L. (1974) Seasonal changes in the susceptibility
of Cresentia d a t a leaves to the flea beetle, Oedionychus sp.
E d o g y , 55, 142-148.
Singer, M.C. (1972) Complex components of habitat suitability
within a butterfly colony. Science, 176, 75-77.
Sokal, R.R. & Rohlf, F.J. (1981) Biometry, 2nd edn. W. H.
Freeman and Company, New York.
Solomon, J.D., Mecracken, F.I., Anderson, R.L., Lewis, R., Jr,
Olivera. F.L., Filer, T.H. & Barry, P.J. (1980) Oak pests: a
guide to major insects, diseases, air pollution, and chemical
injury. U.S. Department of Agriculture, Forest Service General
Report SA-GR-11.
Stilling, P.D. & Simberloff, D. (1989) Leaf abscission: induced
defense against pests or response to damage? Oikos, 55,
43-49.
Varlcy, G.C. & Gradwell, G.R. (1958) Oak defoliators in England.
Proceedings of the Xth International Congress of Entomology,
4, 33-36.
Varley, G.C. & Gradwell, G.R. (1963) The interpretation of
insect population changes. Proceedings Ceylon Association for
the Advancement of Science D, 19, 142- 156.
Watt, A.D. & MacFarlane, A.M. (1991) Winter moth on Sitka
spruce: synchrony of egg hatch and budburst. and its effect on
larval survival. Ecological Entomology, 16, 387-390.
West, C. (1985) Factors underlying the late seasonal appearance
of the lepidopterous leaf-mining guild on oak. Ecological
Entomology, 10, 111-120.
Williams, A.G. & Whitham, T.G. (1986)Prematurc leaf abscission:
an induced plant defense against aphid galls. Ecology, 67,
1619- 1627.
Winer, B.J. (1971) Statistical Principles in Experimental Design,
2nd edn. McGraw-Hill, New York.
Witter, J.A. & Waisanen, L.A. (1978) The effect of differential
flushing times among trembling aspen clones on Tortricid
caterpillar populations. Environmental Eniomo1og.y. 7 , 139- 143.
Accepted 18 January 1994