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) E D W A R D F . C O N N O R , R O B E R T H . A D A M S - M A N S O N , " TIMOTHY G . C A R R t and MICHAEL 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. hamu- dryadella abundance. However, a warm winter and spring in 1991 led to accel- erated 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 over- winter 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

Present address: Department of Biological Sciences, Nor-

* Present address: Department of Biological Sciences, Florida

Correspondence: Dr E. F. Connor. Department of Environ- mental Sciences, Clark Hall, University of Virginia. Charlottcsvillc, VA 22903, U.S.A.

Labs, Rutgers University. Piscataway, NJ 08855. U . S . A .

thern Arizona University, Flagstaff, A Z 86011, U.S.A.

State University, Tallahassee, FL 32306. U . S . A .

Introduction

Leaf phenology has been suggested to play an important role in the demography and population dynamics of her- bivorous 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 con- tent, toughness and pubescence of leaves and their poten- tial 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 (Rock- wood, 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 deter- mining 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 leaf- miners 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 hc 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 gall- forming 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 sub- stantial, i t 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. I f 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 over- wintering 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 fhyllo- norycter 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). ('.humu- dryadella over-winter as diapausing larvae within the leaf- mine 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 113

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.hama- dryadella 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.hama- dryadella, 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.hama- dryadella, 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

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. hama- dryadella 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.hama- dryadella 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 abun- dance 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, fordescrip- tion of site). The fates met by second-generation (over- wintering) 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 com- mencement 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. Dif- ferences 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 sur- vival 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 to 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.hamu- dryadella on potted trees was 0.0023 2 0.0WY individuals per leaf and on forest trees it was 0.0012 * 0.0006 indi- viduals 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.hama- dryadella among trees with different dates of leaf pro- duction 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 115

0.0 1

0.006

n - June July Augurt September

Mines/Leaf 0.012

0.0 1 I

! I 0.008

0.000

0.004

" June July Auguet

Month

Fig. 1. Abundance of Cameraria hamadryadella on trees with differing leaf production phenologies: (A) potted trees and (B) 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.macro- carpa 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.

0.35

0.3

0.25

0.2

0.15

0.1

0.05

ProDortion of Leaf Fall 0. alba

A

0.3

0.25

0.2

0.15

0.1

0.05

0

Prooortion of Leaf Fall

0. macrocarpa

B

0. alba

Sep 14 Sep 28 Oct 12 Oct 28 Nov

Q. macrocarpa

Nov 23

Proportion of Leaf Fall

iM Q. macrocarpa

Sep14 Sep 28 Oct 12 Oct 26 Nov 9 Nov 23

Fig. 2. Timing of leaf fall from Quercus alba and Quercus macro- carpa from the Orland E. White Arboretum at Blandy Exper- imcntal 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.hama- dryadella 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). How- ever, survival rates were significantly higher on Q.macro- carpa 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 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 on 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.

I A I 0.6

0.4

0.2

n

Variable B X 2 df P

1989 Survival

Species -0.0120 Datc 0.0395

Death by other causes Species -0.1481 Date -0.0525

Paras1 tlsm Predat Ion Other Survival

Proportion

B 0.6 -

I

O.(X)3 6.278

0.9580 0 .o 122

1 1

0.851 19.73

0.3562 0.0001

0.4

0.2

n

1990 Survival

Species - 0.0707 Datc -0.0022

Death by other causes Species -0.1117 Datc 0.0138

0.370 0 . 109

1 1

0.4915 0.7417

0.624 2.947

0.4295 0.0861

" 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.

1991 Survival

Species -0.0907 Date 0.0093 Treatment 0.1510"

Death by other causcs Species 0.1081 Date -0.0083 Trcatment -0.0895"

0.934 4.563 4.498

1 1 2

0.3339 0.0327 0.1055

3.824 3.262 1.566

1 1 2

0.0505 0.0709 0.4571

Furthermore, the probability of dying due to other causes was inversely related to the date of leaf fall in 1989 and 1991; i t 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 (x2 = 16.25, df = 6, P < 0.05), and death by other causes was inversely related to the date of leaf fall (x' = 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 prob- ability of dying due to other causes was strongly and inver- sely 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) .

* 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 B X 2 df P

Survival Date 0.0465 8.33 1 0.0039

Death by other causes Date -0.056 9.2bb I 0.0023

Winter severity experiment

Approximately equal proportions of larvae survived in each of the over-wintering treatments (x' = 1.76, df = 2, P >0.4). In fact, the highest rate of survival occurred among larvae exposed to a period of freezing conditions

HOSI plant phenology arid a leaf-mitiing moth 117

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 x2 = 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).

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 pro- duction 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 Phyllo- norycter 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.hama- dryadella 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

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 leaf- mining 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 accel- erated leafing on C. hamadryadella demography. How- ever, 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 or 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. Com- bined 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 i t i 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 popu- lation 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 119

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patterns, causes of mortality, and abundance, will allow us to determine how often outbreaks of Cameraria huma- dryadella 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.

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Accepted 18 January 1994