© 2007 The Authors

Journal compilation © 2007 The Royal Entomological Society

Agricultural and Forest Entomology (2007), 9, 141–158 DOI:10.1111/j.1461-9563.2007.00327.x

Introduction

Subsequent to its discovery in Macedonia in 1984 ( Deschka & Dimic, 1986 ), the horse-chestnut leaf miner Cameraria ohridella Deschka & Dimic has spread very rapidly all over Europe and was first observed in Switzerland in 1998 ( Kenis & Forster, 1998 ). In all invaded regions, the leaf miner reaches outbreak densities, causing severe damage to horse-

chestnut Aesculus hippocastanum L. an important ornamen-tal tree throughout most of Europe. Despite yearly fluctuations in population densities, no outbreak has ever collapsed, a phenomenon rarely encountered in insects ( Berryman, 1987 ). To understand the mechanisms that allow this insect to build and maintain outbreak densities, and potentially to develop sustainable control methods, it is es-sential to assess all mortality factors and other population traits acting on the host through all of its developmental stages. Surprisingly, very little is known about the different mortality factors affecting C. ohridella , with the notable exception of parasitism. The latter has been the focus of

Factors favouring the development and maintenance of outbreaks in an invasive leaf miner Cameraria ohridella (Lepidoptera: Gracillariidae): a life table study

Sandrine Girardoz * † , Donald L. J . Quicke † ‡ § and Marc Kenis * * CABI Switzerland Centre, 1, rue des Grillons, 2800 Delémont, Switzerland , † Division of Biology, Imperial College London, Silwood Park Campus, Ascot, Berks SL5 7PY, U.K. , ‡ Centre for Population Biology, Silwood Park, Ascot, Berks SL5 7PY, U.K. and § Department of Entomology, Natural History Museum, London SW7 5BD, U.K.

Abstract 1 Life tables were constructed for seven generations of the invasive horse-chestnut leaf miner Cameraria ohridella in Switzerland, to assess the factors allowing the moth to build and maintain outbreak densities and to identify ‘gaps’ among their mortality factors that could be targeted by new control methods. The fecundity of females was calculated and the mortality factors affecting all developmental stages determined.

2 Females contained 106.6 eggs. In captivity, the mean number of eggs laid per fe-male varied between 34 and 82 eggs, with a maximum of 184 eggs. Egg mortal-ity was 18 – 75% and was mostly due to unknown factors.

3 The main mortality factors affecting larvae and pupae in the leaves were preda-tion by birds and arthropods in all generation and leaf senescence in the autumn generation. Parasitoids killed less than 5% of the population.

4 Nearly 90% of overwintering pupae died in dead leaves, the majority of them be-ing killed by earthworms and other leaf decomposers. As a result, the overwinter-ing generations were the only ones showing a net rate of increase less than one. Non-overwintering generations had net rates of increase between four and 11, al-lowing populations to build up from spring to autumn.

5 The persistence of high outbreak densities in Europe is explained by a combina-tion of at least three factors: (i) high fecundity; (ii) multivoltinism; (iii) the unu-sually low impact of traditional natural enemies of leaf miners and particularly parasitoids.

6 Yearly variations in population densities could be at least partly explained by dif-ferences in larval mortality due to leaf senescence and intraspecific competition in the last generation in autumn.

Keywords Cameraria ohridella , fecundity , invasive species , life tables , mortality factors , parasitoids , predators

Correspondence: Marc Kenis, CABI Switzerland Centre, 1, Rue des Grillons, 2800 Delémont, Switzerland. Tel.: +41 32 421 48 84; fax: +41 32 421 48 71; e-mail: m.kenis@cabi.org.

142 S. Girardoz, D. L. J. Quicke and M. Kenis

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several studies both in Central Europe ( Grabenweger & Lethmayer, 1999; Hellrigl, 2001; Grabenweger, 2003; Girardoz et al. , 2006; Volter & Kenis, 2006 ) and in the Balkans where the host tree originates and where the moth was first discovered ( Freise et al. , 2002; Grabenweger et al. , 2005a ). Approximately 30 native generalist parasitoid spe-cies have been recorded as attacking this alien species. However, parasitism rates are low and, although reliable data on population dynamics are lacking, there is common agreement that the role of parasitoids in the natural regula-tion of C. ohridella populations is negligible.

Mortality factors other than parasitism have been poorly studied. Predation was investigated only recently in a single study ( Grabenweger et al. , 2005b ) and there are hardly any reliable and quantifiable data on other mortality factors and population traits such as winter, egg and adult mortality, fe-cundity, host resistance, intraspecific competition and insect-host plant synchronization.

In the present study, we present quantitative data on mor-tality factors and other traits affecting the population dynam-ics of C. ohridella in Switzerland, and integrate them into life tables ( Bellows et al. , 1992; Van Driesche & Bellows, 1996 ). The main aim was to understand the roles of these factors in the natural control and population dynamics of the moth, and to identify the causes of permanent outbreaks. Ideally, parallel studies should be carried out in the region of origin of the moth, or in regions where it occurs at low den-sity, to allow comparison between outbreaking and non-out-breaking populations with the aim of identifying differences leading to outbreaks. Such a comparative study would also allow us to spot ‘gaps’ among the mortality factors in the in-vaded region that could be targeted by new control methods, such as the importation of a key natural enemy from the re-gion of origin. However, the origin of C. ohridella is not yet known, and nor is there any region where the moth is known to occur at low density ( Kenis et al. , 2005 ). Consequently, such comparisons are not currently possible. In the mean-time, data on population traits of other leaf mining moths producing no, or temporary, outbreaks ( Kirizoglu, 1976; Faeth & Simberloff, 1981; Van Driesche & Taub, 1983; Hespenheide, 1991; Connor & Beck, 1993 ) can be used to assess the specificity of the permanent outbreak behaviour of C. ohridella .

Materials and methods

Field sites

The study was carried out at a site in north-eastern Switzerland, in Delémont (47°21 ¢ 59 ¢ ¢ N, 7°19 ¢ 59 ¢ ¢ E), in the Canton Jura. It consisted of an alley of 54 horse-chestnut trees situated along a road leading to a forest where the first mines of C. ohridella were observed in 2000.

Population size

Population size was measured at the end of each generation, when the majority of mines contained pupae. Two genera-

tions per year were observed in Delémont in 2001, 2002, 2004 and 2005, and three in 2003. Fifteen horse-chestnut leaves were chosen on 15 trees, at random, and the mine den-sities were estimated using the damage key of Gilbert & Grégoire (2003) , based on a visual assessment of the relative mined area per leaf. Each leaf was assigned to one of the eight scores defined by the authors: 0% damage, 2, 5, 10, 25, 50, 75 and 100% damage. The median value was taken as an indicator of the population size of one generation. Gilbert & Grégoire (2003) showed that their damage scoring system provides a good tool to estimate and compare population densities and it is now increasingly used in population stud-ies on C. ohridella ( Gilbert et al. , 2005; Grabenweger et al. , 2005b; Kehrli et al. , 2005 ). The sample size of 15 leaves was chosen after an analysis showing that the median value did not change with larger sample sizes (S. Girardoz and M. Kenis, unpublished data).

Fecundity

Potential fecundity was studied in 2001 (first generation, i.e. females emerging in early summer from the first generation of mines), 2003 (first and second generations) and 2004 (first generation). Pupae were separated by sex according to Freise & Heitland (1999) and stored in glass vials. Females were frozen within the day of emergence and kept until they were dissected under saline water (0.9%), and the number of oocytes in the ovaries was counted. Between 37 and 125 females were dissected per generation.

Realized fecundity was studied in 2001 (first and second generations), 2002 and 2003 (overwintering generation, i.e. females emerging from overwintering pupae from the second generation of the preceeding year, and first and second gen-erations). Freshly emerged (less than 8 h old) females and males were first maintained for a few hours in laboratory conditions in a cylinder (1.3 L) for mating (maximum 30 in-dividuals per cylinder). Females were then transferred indi-vidually to muslin cages (20 × 20 × 30 cm) with one male and one horse-chestnut leaf with its petiole immersed in wa-ter to increase the chances of the female being mated. These cages were placed outdoors in a shaded tunnel, and females were provided daily with water. Food was not provided be-cause it had been shown previously that females fed with honey neither lived longer nor laid more eggs than unfed ones ( Girardoz, 2001 ). The eggs laid on the leaves were counted after the female’s death and kept until hatching to assess viability. Only fertile eggs were included in the calcu-lation of fecundity, and females that had laid only sterile eggs were suspected to have been unmated and were discarded. Between seven and 28 fertile females per generation were in-cluded in the analyses. It cannot be excluded that some de-gree of unfertility also occurs under natural conditions. However, the proportion of sterile females occurring in na-ture is not known and is undoubtedly much lower than that observed in our laboratory experiments, where mating was not easily obtained and up to half of the females were found to be sterile. Therefore, it was decided to discard them from the analyses.

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Egg mortality

In 2002, 2003 and 2004, horse-chestnut seedlings (70 – 100 cm high) or cut branches placed in water were exposed to C. ohridella females in cages in the laboratory. The females were left on the leaves for three days to allow them to lay eggs, which were then counted and their spatial distribution noted. Tree seedlings or cut branches in water were then ex-posed in the canopies of mature trees in the last phase of the oviposition periods, to minimize additional natural oviposi-tion on the exposed leaves. After the majority of the eggs had hatched, the branches or seedlings were taken back to the laboratory and the eggs were scored as flat/empty, disap-peared, opened or hatched. The number of eggs exposed per generation was very variable (20 – 1173), but only generations for which at least 80 eggs could be exposed were included in the analyses.

To determine whether egg mortality was due to predators and, if so, which kind of predators, an experiment was car-ried out in 2004. Five seedlings per generation were exposed to C. ohridella females as described above. For each seed-ling, the leaves were separated into three batches with a simi-lar number of eggs on them. One batch was enclosed in a gauze bag, to exclude flying and crawling predators. The sec-ond batch of leaves had their petioles smeared with Tangle-coating (The Tanglefoot Company, Grand Rapids, Michigan) to exclude crawling predators only. A third batch was left as a control. The seedlings were then placed amongst the foli-age of mature trees, in an attempt to place their stems/trunk in contact with branches but keeping their leaves away from any contact. The seedlings were brought back to the labora-tory after the majority of the eggs had hatched. The eggs and first-instar larvae were counted and classified as in previous years.

Larval and pupal mortality during the summer and autumn

Summer larval and pupal mortality were studied in Delémont from 2002 to 2004, which corresponds to seven generations of the moth (two in 2002 and 2004, three in 2003). For each generation, 400 first instar larvae were chosen at random on the lower branches (max 2 m above ground level) of a mini-mum of 30 different trees. Leaves with selected mines were tagged, the position of the mines on the leaf was noted and the cohort of mines was checked every week to monitor larva and parasitoid development and fate. When mines with feed-ing stages of the larvae stopped growing, they were brought to the laboratory and examined. The developmental stage was noted and the mortality factor of dead or dying larvae classi-fied into the categories: (1) Parasitism (an egg or larva of a parasitoid was found in the mine); (2) Host feeding by para-sitoids (the integument of the host larva was stuck to the up-per inner surface of the mine as defined in Askew & Shaw, 1979 ); (3) Predation by birds (i.e. the upper surface of the mine was ripped open); (4) Predation by arthropods; (5) Plant defence reaction (i.e. necrosis around a young mine); (6) Competition with the leaf fungus Guignardia aesculi (Peck) Stewart (Ascomycetes); (7) Intra-specific competition at high

densities; (8) Senescence of the host leaf; (9) Unknown cause (i.e. no obvious sign of any mortality factor mentioned above). Categories 6, 7 and 9 were combined as ‘other’ for the analysis because the difference between these three fac-tors was not always obvious, and the numbers dying from each of these factors were low.

For all generations but the last one of the season, pupae were left on the trees until the adults emerged. If no adult had emerged one month after pupation, two thirds of the mines were brought back to the laboratory and examined. The remaining third was left on the trees to assess mortality affecting summer diapausing pupae.

The proportions of larvae and pupae killed by the different mortality factors were assessed for each stage and each gen-eration investigated.

Overwintering mortality

To assess winter mortality of C. ohridella pupae in the leaf litter, leaves were collected at leaf fall in Delémont on 30 October 2002 and 27 October 2003. For each leaf, the number of pupae was noted on a small plastic tag attached to the main vein of the leaf. One thousand pupae were selected per year, and separated in ten groups of 100 mines. Five groups were placed in an envelope of chicken wire, five groups were placed between a plastic mesh on the bottom and the chicken wire on top. The chicken wire was used to prevent the loss of leaves. Earthworms, and possibly other leaf decomposers, were partly (2002 – 03) or entirely (2003 – 04) excluded by separating the leaves from the ground by means of plastic mesh, 3 mm in diameter in the first year, 0.2 mm in the sec-ond. The batches of leaves were placed amongst the leaf lit-ter underneath mature horse-chestnuts at the study site. The leaves were removed in the spring, as soon as the first adult C. ohridella was caught in a pheromone trap at the site ( Kalinova et al. , 2003 ) (i.e. on 17 April 2003 and 18 April 2004). The remaining pupae were counted and the mortality was assessed. In winter 2003 – 04, one control grid and one with mesh were checked monthly from November to April to assess when pupae disappear. Only two grids were inspected monthly, to minimize disturbance.

Construction of life tables

The columns of the life tables were defined in accordance with the structure of Van Driesche & Bellows (1996) as fol-lows: (i) l x , the number of individuals entering stage x ; (ii) d x , the number of individuals dying in stage x ; (iii) factor d x , the number of individuals dying from a given factor; (iv) marginal attack rates ( m x ); (v) apparent mortality; (vi) real mortality; and (viii) k -values . Further details can be found in Southwood (1978) and Bellows et al. (1992) . Marginal at-tack rates were calculated after Elkinton et al. (1992) . In the case of two contemporaneous mortality factors, of which one is always decided to be the ‘winner’ in case of competition, we used Eq. (6) from Elkinton et al. (1992) . In the case of more than two contemporaneously acting mortality factors, we used Eq. (9).

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The number of eggs entering the next generation ( F 1 prog-eny) was estimated as the number of adults × sex ratio × fe-male realized fecundity. The sex ratio used in the life tables was of 0.54, as calculated by Freise (2001) . The net repro-ductive rate ( R 0 ), was taken as the ratio of the F 1 progeny to the initial number of individuals entering the life table.

It was not possible to assess the fecundity of C. ohridella females and the mortality affecting certain stages in all years and all generations. Potential fecundity could not be obtained in 2002 and in the second generation of 2004. For the miss-ing data, we used those of the corresponding generation in 2003. Data on the realized fecundity of females could not be obtained in 2004, and thus the corresponding data of 2003 were used. In 2003, egg mortality could not be assessed for the first generation, so we used the mean of the first genera-tions of the years 2002 and 2004. Winter mortality was not assessed for the winter 2004 – 05. Instead, we used the aver-age of the two previous years.

For certain mortality factors, some assumptions had to be made. For mortality through leaf senescence, we assumed that larvae that were still in the feeding stages and spinning stages in the last sample when leaves were senescing would die, whereas pupae were assumed to survive (S. Girardoz and M. Kenis, unpublished data). The few pupae of the first gen-erations that were entering into an early diapause were con-sidered as dead because we observed that, in general, these could not survive until leaf senescence (S. Girardoz and M. Kenis, unpublished data). By contrast, we considered that diapausing pupae of the second generation were able to survive until the winter, even when a third generation was observed.

Results

Population size

Population densities in Delémont increased over the years 2001 – 03 ( Table 1) but the 2004 populations were lower in comparison with the previous year, with an estimated dam-age of 5% and 25% for the first and second generations, re-spectively. The population increased again in 2005, with a total defoliation observed in the second generation.

Fecundity

Freshly emerged C. ohridella females contained a mean of 106.63, mostly immature, eggs (SE = 0.99, n = 314). A maxi-mum of 180 eggs per female was found. Females of the first

generation of 2001 were found to have 124.59 eggs on aver-age (SE = 2.25, n = 37). In 2003, females had 102.74 eggs on average (SE = 1.58, n = 105) in the first generation and 100.25 (SE = 1.07, n = 125) in the second generation. In 2004, females of the first generation had 118.17 eggs on av-erage (SE = 3.08, n = 47). The difference between the years was highly significant [one-way analysis of variance (anova): F = 10.01, d.f = 2, P < 0.001] with fecundity in 2003 being significantly lower than in the two other years (Scheffe test, P < 0.001).

The realized fecundity for all generations is shown in Table 2. The mean number of eggs laid per female varied be-tween 34 and 82 eggs, with a maximum of 184 eggs. The number of eggs strongly decreased with years and the differ-ence was significant (two-way anova, F = 4.93, d.f. = 2, P = 0.009; fecundity lower in 2001 than in 2002 and 2003, Scheffe test, P < 0.01). There was no significant difference between generations ( F = 0.49, d.f. = 2; P = 0.611).

Egg mortality

Results for egg mortality are given in Table 3. Survival rates were found to vary little between the first and second genera-tion with 61% to 82% of the eggs hatching. The one third generation observed showed a much lower survival rate, per-haps because the eggs were laid on severely attacked leaves, including on mines, in which case hatching larvae were una-ble to survive. The majority of the eggs that did not hatch were simply not recovered. However, in some generations, a sizeable number of eggs were found to be unhatched, flat and dry ( Table 3 ). Very few eggs were found destroyed with any obvious signs of predation.

Results obtained in the experiment set up in 2004 to assess the role of predators are shown in Fig. 1. There were no sig-nificant differences in mortality between the different treat-ments neither in the first generation (Friedman: n = 15, c 2 = 3.00, d.f. = 1, P = 0.083) nor in the second ( n = 15, c 2 = 3.00, d.f. = 1, P = 0.093) and approximately 70% of eggs hatched in both generations.

Winter mortality

The pupal mortality observed in the winters 2002 – 03 and 2003 – 04 is shown in Fig. 2. In both years, less than 15% of the pupae survived, as shown in the control samples. Most pupae had disappeared, eaten by predators or saprophages. Leaf veins were often found half buried in the soil, suggesting that they had been moved there by earthworms. In 2002 – 03, the number of pupae that disappeared was not significantly greater in the

Table 1 Estimated damage from Cameraria ohridella at the end of each generation in Delémont over the years 2001 – 05

2001 2002 2003 2004 2005

First generation 2% 10% 25% 5% 50% Second generation 25% 50% 50% 25% 100% Third generation – – 75% – –

Percentages indicate the leaf surface damaged by the mines.

Life tables of C. ohridella 145

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control than in the earthworm- excluded batches (Mann – Whitney U -test: Z = – 1.984, P = 0.056).

By contrast, in 2003 – 04, the number of pupae disappeared was significantly greater in the control than in the earth-worm-excluded batches, in which more than 50% of the pu-pae were still alive in spring ( Z = – 2.611, P = 0.008). These results suggest that earthworms play an important role in the overwintering mortality of C. ohridella and that the mesh used in 2002 – 03 may have not been fine enough to exclude earthworms effectively. The monthly monitoring of two grids suggested that earthworms are active mainly in early spring ( Fig. 3) as numbers started to differ in March

Larval and pupal mortality and construction of life tables

Life tables are presented in Tables 4 – 10. All generations ex-cept for the last ones of the season had a very high net repro-ductive rate: they increased from 4.1-fold to 11.4-fold. Only the last, overwintering generations had a net increase rate be-low 1, due to high mortality rates on overwintering pupae ( Fig. 4).

Total mortality ranged from 55.3% of the total population to 77.6% in the first and intermediate generations and from 96.0% to 99.6% for the last generation of the season ( Fig. 4 ). Egg mortality generally accounted for the death of 18 – 36% of the population of one generation, the only third generation examined had the highest egg mortality rate observed, reach-ing 75% of the total population. Real mortality rates in the first- and second-instar larvae were usually below 10%. First- (L1) and second- (L2) instar larvae were subject to only a few mortality factors, mostly plant defence reaction and un-

known mortality, whereas parasitism and predation were rare. Third-instar larvae (L3) were subject to more mortality fac-tors than the younger larvae, but a maximum of 5% of the population died in this stage in the first and second genera-tions. Fourth-instar larvae (L4) suffered the highest mortality amongst feeding stages: 2 – 11% of the total population died at this stage. In spring and summer, the major mortality fac-tor affecting L4 was predation either by birds or by arthro-pods (with marginal attack rates of 1 – 19%). Birds feeding on C. ohridella were mostly great tits Parus major L. and blue tits Parus caeruleus L. whereas other predators were not clearly identified, although a bush-cricket, Meconema merid-ionale (Orthoptera, Tettigoniidae) was often seen on leaves and has been described by Grabenweger et al. (2005b) as a predator of C. ohridella. In the last generations, leaf senes-cence was a major cause of mortality in 2002 and 2003 (e.g. with marginal attack rates of 10% and 20%). Parasitism re-mained low, with marginal attack rates of less than 1% in most cases. The main parasitoids attacking C. ohridella were Minotetrastichus frontalis (Nees) and Pnigalio agraules (Walker) (Hymenoptera: Eulophidae). Patterns for spinning stages were similar to those observed for L4. Indeed, for non-overwintering generations, the major mortality was often bird predation, with marginal attack rates of 1 – 11%, but real mortality remaining under 7%. For overwintering genera-tions, the major mortality factor was leaf senescence, with marginal attack rates of 5 – 44%. Pupae of all generations were attacked less than L4 and spinning stages, with only 0 – 9% of the population dying in that stage. Only one genera-tion, the intermediate generation in 2003, had higher values, with 26% of the total population dying in the pupal stage, which was mostly due to a higher impact of birds.

Table 2 Realized fecundity of Cameraria ohridella females in Delémont, Switzerland in 2001, 2002 and 2003

2001 2002 2003

Overwintering generation a – 41.62 ± 6.60 (16, 85) 38.35 ± 4.68 (17, 81) 1st generation 81.69 ± 13.74 (13, 184) 58.76 ± 11.31 (17, 141) 40.26 ± 4.56 (27, 95) 2nd generation b 82.41 ± 7.88 (28, 161) 58.57 ± 5.40 (7, 87) 34.00 ± 5.50 (5, 52) Mean 82.08 ± 6.83 (41, 184) 51.87 ± 5.62 (40, 141) 39.96 ± 3.01 (49, 95)

a Overwintering generation, females emerging from overwintering pupae (i.e. from the second generation of the preceeding year). b 2nd generation, females emerged before winter, even when, as in 2001 and 2002, the majority of the pupae of the second generation went into diapause. Numbers indicate the mean ± SE number of eggs per female (no. of females, maximum number of eggs).

Table 3 Mortality of Cameraria ohridella eggs over the years 2002 – 04 in Delémont

2002 2003 2004

First generation

Second generation

Second generation

Third generation

First generation

Second generation

Total 1173 88 112 246 292 331 Eggs dry 4 4 89 76 2 Eggs disappeared 372 32 15 94 28 97 Eggs opened 1 1 1 Eggs hatched 801 56 92 62 187 232 Survival rate 0.68 0.64 0.82 0.25 0.64 0.70

Numbers are given only for generations for which a minimum of 80 eggs could be exposed.

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‘Other mortality’ was observed in all stages, but remained low. Marginal attack rates were, in most cases, below 10%.

Discussion

Subsequent to the first discovery of C. ohridella in Macedonia in 1984 and its subsequent spread to most of Europe, out-breaks have continued unabated. Despite yearly fluctuations in population levels, no outbreak has ever collapsed. Our life tables confirm these observations. For all non-overwintering generations, high net rates of increase were found, which were consistent with the increases in populations observed at the study sites. A combination of at least three factors can explain the permanence of outbreak densities in central Europe: (i) high fecundity; (ii) multivoltinism; and (ii) an unusually low impact of the traditional natural enemies of leaf miners, in particular parasitoids.

The fecundity of C. ohridella was previously thought to be rather low. Skuhravy (1998) had suggested a fecundity of 20 – 30 eggs whereas Freise (2001) had measured an average realized fecundity of 23 and a potential fecundity of 42, with a maximum of 80 eggs per female. We found fecundities that were substantially higher. Both dissections of ovarioles

(potential fecundity) and oviposition tests in cages (realized fecundity) showed that a female can lay up to 180 eggs. On average, potential fecundity was much higher than realized fecundity, probably because conditions in cages were not op-timal for oviposition tests, and many tested females laid few eggs. Because realized fecundity was used in the calculation of the life tables, it is likely that we underestimated the real

Figure 1 Percentage of eggs hatched (white bars), unhatched (striped bars) and disappeared (grey bars) after the three treatments (exclusion of all predators, exclusion of crawling predators and control), in the first (A) and second (B) generation of Cameraria ohridella in 2004 in Delémont, Switzerland.

Figure 2 Mortality of pupae of Cameraria ohridella during the winter 2002 – 03 (A) and the winter 2003 – 04 (B) in Delémont, Switzerland.

Figure 3 Numbers of pupae of Cameraria ohridella present in two grids during the winter 2003 – 04 in Delémont, Switzerland. The grids were not examined in February because they were covered by snow.

Life tables of C. ohridella 147

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Tab

le 4

Life

tab

le f

or t

he f

irst

gen

erat

ion

of C

amer

aria

ohr

idel

la in

Del

émon

t, S

witz

erla

nd,

2002

Ap

par

ent

mor

talit

y

Rea

l mor

talit

y

Sta

ge

Fa

ctor

M

arg

inal

atta

ck

rate

Sta

ge

Fact

or

Sta

ge

Fact

or

k -va

lue

Sta

ge

Fact

or

l x d

x d

x q

x q

x d

x / l 0

d x /

l 0 Fa

ctor

Eg

g

10

00

319.

46

0.

3195

0.31

95

Eg

gs

dis

app

ear

off l

eaf

31

6.05

78

0.31

61

0.

3161

0.31

61

0.16

50

E

gg

s fl a

t and

em

pty

3.39

85

0.00

50

0.

0034

0.00

34

0.00

22

L1

68

0.54

6.

81

0.

0100

0.00

68

Leaf

sen

esce

nce

6.

8054

0.

0100

0.01

00

0.

0068

0.

0044

L2

673.

74

69.7

6

0.10

35

0.

0698

P

lant

def

ense

rea

ctio

n

34.0

272

0.05

19

0.

0505

0.03

40

0.02

32

O

ther

15.3

122

0.02

37

0.

0227

0.01

53

0.01

04

P

aras

itism

8.50

68

0.01

32

0.

0126

0.00

85

0.00

58

H

ost f

eed

ing

6.80

54

0.01

06

0.

0101

0.00

68

0.00

46

Le

af s

enes

cenc

e

3.40

27

0.00

51

0.

0051

0.00

34

0.00

22

P

red

atio

n (a

rthr

opod

s)

1.

7014

0.

0027

0.00

25

0.

0017

0.

0012

L3

603.

98

32.3

3

0.05

35

0.

0323

O

ther

13.6

109

0.02

29

0.

0225

0.01

36

0.01

01

Le

af s

enes

cenc

e

8.50

68

0.01

41

0.

0141

0.00

85

0.00

62

P

aras

itism

6.80

54

0.01

15

0.

0113

0.00

68

0.00

50

P

red

atio

n (b

irds)

1.70

14

0.00

29

0.

0028

0.00

17

0.00

13

P

red

atio

n (a

rthr

opod

s)

1.

7014

0.

0029

0.00

28

0.

0017

0.

0013

L4

571.

66

74.8

6

0.13

10

0.

0749

P

red

atio

n (b

irds)

20.4

163

0.03

76

0.

0357

0.02

04

0.01

66

P

red

atio

n (a

rthr

opod

s)

17

.013

6 0.

0314

0.02

98

0.

0170

0.

0139

Par

asiti

sm

13

.610

9 0.

0252

0.02

38

0.

0136

0.

0111

Oth

er

10

.208

2 0.

0190

0.01

79

0.

0102

0.

0083

Leaf

sen

esce

nce

8.

5068

0.

0149

0.01

49

0.

0085

0.

0065

Hos

t fee

din

g

5.

1041

0.

0095

0.00

89

0.

0051

0.

0042

S

pin

496.

80

28.9

2

0.05

82

0.

0289

P

aras

itism

15.3

122

0.03

13

0.

0308

0.01

53

0.01

38

P

red

atio

n (b

irds)

8.50

68

0.01

71

0.

0171

0.00

85

0.00

75

O

ther

3.40

27

0.00

70

0.

0068

0.00

34

0.00

31

H

ost f

eed

ing

1.70

14

0.00

35

0.

0034

0.00

17

0.00

15

Pup

ae

46

7.87

80

.26

0.

171

5

0.08

03

Pre

dat

ion

(bird

s)

35

.858

9 0.

0766

0.07

66

0.

0359

0.

0346

Par

asiti

sm

23

.906

0 0.

0545

0.05

11

0.

0239

0.

0243

Oth

er

15

.368

1 0.

0354

0.03

28

0.

0154

0.

0156

Pre

dat

ion

(art

hrop

ods)

1.70

76

0.00

40

0.

0036

0.00

17

0.00

17

H

ost f

eed

ing

1.70

76

0.00

40

0.

0036

0.00

17

0.00

17

P

upae

in d

iap

ause

1.70

76

0.00

40

0.

0036

0.00

17

0.00

17

Ad

ults

387.

62

S

ex r

atio

0.5

P

oten

tial

fe

cund

ity

10

2.74

Con

tinue

d

148 S. Girardoz, D. L. J. Quicke and M. Kenis

© 2007 The Authors

Journal compilation © 2007 The Royal Entomological Society, Agricultural and Forest Entomology, 9, 141–158

fecundity of females in the field in the calculations. However, adults are the only developmental stage for which mortality could not be estimated in the field and we must admit that we still know very little about the number of eggs laid per female under field conditions. The estimation of adult mor-tality and real fecundity in the field is a recurrent problem in life tables and population dynamics studies and fecundity may depend strongly of environmental factors, such as weather and host plant quality ( Courtney & Duggan, 1983; Preszler & Price, 1988; Awmack & Leather, 2002 ). To our knowledge, there are no good data on adult mortality in leaf miners and only a few studies have measured the fecundity of gracillariid leaf miners, exclusively in laboratory or under semifield conditions. In most cases, realized fecundity ap-peared lower than with C. ohridella . For example, laboratory experiments gave a mean fecundity of 18.3 eggs per female in Phyllonorycter elmaella ( Barrett & Brunner, 1988 ), 48.5 eggs in Marmara sp. ( Guillén et al. , 2001 ) and 20 – 29 eggs in Phyllonorycter blancardella ( Pottinger & Leroux, 1971 ). However, Pfeiffer et al. (1995) mentioned that P. blancar-della females could lay up to 152 eggs, a number that is close to the one obtained for C. ohridella , suggesting that differ-ences between potential fecundity and the realized fecundity in captivity can be substantial.

It is interesting to note that, from 2001 to 2003, the real-ized fecundity in cages dropped significantly, from an aver-age of 82 – 40 eggs per female whereas, at the same time, the potential fecundity decreased from 125 to 103. Because, at the same time, population densities strongly increased, it is possible that the decrease in fecundity may be due to a lower fitness resulting from higher population densities, as has of-ten been observed in insects ( McClure, 1991; Klemola et al. , 2004; Sato et al. , 2004 )

Multivoltinism is another factor that favours high popula-tion densities. In temperate regions, most leaf miners have either one or two generations per year ( Hering, 1951 ). In Europe, C. ohridella has mainly three full generations per year (e.g. Pschorn-Walcher, 1994; Hellrigl & Ambrosi, 2000; Freise & Heitland, 2001 ). Only in cooler areas, such as the Swiss Jura in cool summers, may the whole population enter into dia-pause after two generations. In southern Europe, four com-plete generations are commonly observed ( Del Bene et al. , 2001; Hellrigl, 2001 ). Non-overwintering generations have

Figure 4 Net reproductive rate ( R 0 ) and total mortality affecting first, intermediate and last generations of Cameraria ohridella in Delémont, Switzerland, over the years 2002 – 04.

Ap

par

ent

mor

talit

y

Rea

l mor

talit

y

Sta

ge

Fa

ctor

M

arg

inal

atta

ck

rate

Sta

ge

Fact

or

Sta

ge

Fact

or

k -va

lue

Sta

ge

Fact

or

l x d

x d

x q

x q

x d

x / l 0

d x /

l 0 Fa

ctor

Pot

entia

l F 1

p

rog

eny

19

911.

94

8523

.72

0.

4281

0.42

81

Rea

lized

fecu

ndity

58.7

6

8523

.72

0.42

81

0.

4281

0.42

81

0.24

27

Rea

lized

F 1

p

rog

eny

11

388.

22

R 0

( F 1 /

l 0 )

11

.388

2

Tab

le 4

Co

nti

nu

ed

Life tables of C. ohridella 149

© 2007 The Authors

Journal compilation © 2007 The Royal Entomological Society, Agricultural and Forest Entomology, 9, 141–158

Tab

le 5

Life

tab

le f

or t

he s

econ

d,

over

win

terin

g g

ener

atio

n of

Cam

erar

ia o

hrid

ella

in D

elém

ont,

Sw

itzer

land

, 20

02

Ap

par

ent

mor

talit

y

Rea

l mor

talit

y

Sta

ge

Fa

ctor

M

arg

inal

atta

ck

rate

Sta

ge

Fact

or

Sta

ge

Fact

or

k -va

lue

Sta

ge

Fact

or

l x d

x d

x q

x q

x d

x / l 0

d x /

l 0 Fa

ctor

Eg

g

10

00.0

0 36

3.64

0.36

36

0.

3636

E

gg

s d

isap

pea

r of

f lea

f

363.

6364

0.

3636

0.36

36

0.

3636

0.

1963

L1

636.

36

7.95

0.01

25

0.

0080

Le

af s

enes

cenc

e

7.95

45

0.01

25

0.

0125

0.00

80

0.00

55

L2

62

8.41

60

.45

0.

0962

0.06

05

Pla

nt d

efen

se r

eact

ion

25

.454

5 0.

0417

0.04

05

0.

0255

0.

0185

Leaf

sen

esce

nce

15

.909

1 0.

0253

0.02

53

0.

0159

0.

0111

Oth

er

15

.909

1 0.

0263

0.02

53

0.

0159

0.

0116

Hos

t fee

din

g

1.

5909

0.

0027

0.00

25

0.

0016

0.

0012

Pre

dat

ion

(art

hrop

ods)

1.59

09

0.00

27

0.

0025

0.00

16

0.00

12

L3

56

7.95

39

.77

0.

0700

0.03

98

Oth

er

28

.636

4 0.

0509

0.05

04

0.

0286

0.

0227

Leaf

sen

esce

nce

9.

5455

0.

0168

0.01

68

0.

0095

0.

0074

Pre

dat

ion

(art

hrop

ods)

1.59

09

0.00

29

0.

0028

0.00

16

0.00

13

L4-5

528.

18

105.

00

0.

1988

0.10

50

Leaf

sen

esce

nce

52

.500

0 0.

0994

0.09

94

0.

0525

0.

0455

Oth

er

42

.954

5 0.

0867

0.08

13

0.

0430

0.

0394

Pre

dat

ion

(bird

s)

4.

7727

0.

0100

0.00

90

0.

0048

0.

0044

Pre

dat

ion

(art

hrop

ods)

3.18

18

0.00

67

0.

0060

0.00

32

0.00

29

H

ost f

eed

ing

1.59

09

0.00

34

0.

0030

0.00

16

0.00

15

Sp

in

42

3.18

22

0.85

0.52

19

0.

2208

Le

af s

enes

cenc

e

187.

4367

0.

4429

0.44

29

0.

1874

0.

2541

Pre

dat

ion

(bird

s)

17

.500

0 0.

0568

0.04

14

0.

0175

0.

0254

Oth

er

9.

5455

0.

0314

0.02

26

0.

0095

0.

0139

Par

asiti

sm

4.

7727

0.

0158

0.01

13

0.

0048

0.

0069

Pre

dat

ion

(art

hrop

ods)

1.59

09

0.00

53

0.

0038

0.00

16

0.00

23

Pup

ae

20

2.34

11

.09

0.

0548

0.01

11

Pre

dat

ion

(bird

s)

5.

5435

0.

0274

0.02

74

0.

0055

0.

0121

Oth

er

4.

6195

0.

0232

0.02

28

0.

0046

0.

0102

Hos

t fee

din

g

0.

9239

0.

0047

0.00

46

0.

0009

0.

0020

P

upae

in d

iap

ause

19

1.25

18

2.17

0.95

25

0.

1822

E

arth

wor

ms

17

0.82

83

0.94

26

0.

8932

0.17

08

1.24

10

O

ther

9.42

50

0.14

59

0.

0493

0.00

94

0.06

85

P

aras

itism

1.91

25

0.03

15

0.

0100

0.00

19

0.01

39

Ad

ults

9.08

Sex

rat

io

0.

5

Pot

entia

l fec

und

ity

10

2.74

Pot

entia

l F 1

pro

gen

y

466.

61

292.

43

0.

6267

0.62

67

R

ealiz

ed fe

cund

ity

38

.35

29

2.43

0.

6267

0.62

67

0.

6267

0.

4279

R

ealiz

ed F

1 p

rog

eny

17

4.19

R 0

( F 1 /

l 0 )

0.

1742

150 S. Girardoz, D. L. J. Quicke and M. Kenis

© 2007 The Authors

Journal compilation © 2007 The Royal Entomological Society, Agricultural and Forest Entomology, 9, 141–158

Tab

le 6

Life

tab

le f

or t

he f

irst

gen

erat

ion

of C

amer

aria

ohr

idel

la in

Del

émon

t, S

witz

erla

nd,

2003

Ap

par

ent

mor

talit

y

Rea

l mor

talit

y

Sta

ge

Fa

ctor

Mar

gin

al a

ttack

ra

te

Sta

ge

Fact

or

Sta

ge

Fact

or

k -va

lue

Sta

ge

Fact

or

l x d

x d

x q

x q

x d

x / l 0

d x /

l 0 Fa

ctor

Eg

g

10

00

178.

57

0.

178

6

0.17

86

Eg

gs

dis

app

ear

off l

eaf

13

3.92

86

0.13

39

0.

1339

0.13

39

0.06

24

E

gg

s fl a

t and

em

pty

35.7

143

0.03

86

0.

0357

0.03

57

0.01

71

E

gg

s op

ened

8.92

86

0.00

98

0.

0089

0.00

89

0.00

43

L1

82

1.43

12

.32

0.

0150

0.01

23

Pla

nt d

efen

se r

eact

ion

10

.267

9 0.

0125

0.01

25

0.

0103

0.

0055

Oth

er

2.

0536

0.

0025

0.00

25

0.

0021

0.

0011

L2

809.

11

197.

14

0.

2437

0.19

71

Pla

nt d

efen

se r

eact

ion

10

6.78

57

0.14

04

0.

1320

0.10

68

0.06

57

P

aras

itism

39.0

179

0.05

38

0.

0482

0.03

90

0.02

40

O

ther

24.6

429

0.03

43

0.

0305

0.02

46

0.01

52

H

ost f

eed

ing

14.3

750

0.02

02

0.

0178

0.01

44

0.00

88

Le

af s

enes

cenc

e

8.21

43

0.01

02

0.

0102

0.00

82

0.00

44

P

red

atio

n (a

rthr

opod

s)

4.

1071

0.

0058

0.00

51

0.

0041

0.

0025

L3

611.

96

49.2

9

0.08

05

0.

0493

Le

af s

enes

cenc

e

16.4

286

0.02

68

0.

0268

0.01

64

0.01

18

O

ther

10.2

679

0.01

73

0.

0168

0.01

03

0.00

76

P

aras

itism

10.2

679

0.01

73

0.

0168

0.01

03

0.00

76

P

red

atio

n (a

rthr

opod

s)

6.

1607

0.

0104

0.01

01

0.

0062

0.

0046

Hos

t fee

din

g

4.

1071

0.

0070

0.00

67

0.

0041

0.

0030

Pre

dat

ion

(bird

s)

2.

0536

0.

0035

0.00

34

0.

0021

0.

0015

L4

562.

68

20.5

4

0.03

65

0.

0205

P

red

atio

n (a

rthr

opod

s)

12

.321

4 0.

0221

0.02

19

0.

0123

0.

0097

Pre

dat

ion

(bird

s)

6.

1607

0.

0109

0.01

09

0.

0062

0.

0048

Par

asiti

sm

2.

0536

0.

0037

0.00

36

0.

0021

0.

0016

S

pin

542.

14

26.1

0

0.04

81

0.

0261

P

red

atio

n (b

irds)

10.0

397

0.01

85

0.

0185

0.01

00

0.00

81

P

aras

itism

10.0

397

0.01

88

0.

0185

0.01

00

0.00

82

P

red

atio

n (a

rthr

opod

s)

4.

0159

0.

0076

0.00

74

0.

0040

0.

0033

Oth

er

2.

0079

0.

0038

0.00

37

0.

0020

0.

0016

P

upae

516.

04

68.3

9

0.13

25

0.

0684

P

upae

in d

iap

ause

26.9

418

0.05

45

0.

0522

0.02

69

0.02

43

P

red

atio

n (b

irds)

16.5

796

0.03

21

0.

0321

0.01

66

0.01

42

P

red

atio

n (a

rthr

opod

s)

14

.507

1 0.

0297

0.02

81

0.

0145

0.

0131

Par

asiti

sm

10

.362

2 0.

0213

0.02

01

0.

0104

0.

0094

A

dul

ts

44

7.65

Sex

rat

io

0.

54

P

oten

tial f

ecun

dity

102.

74

P

oten

tial F

1 p

rog

eny

24

881.

31

1513

1.70

0.60

82

0.

6082

Rea

lized

fecu

ndity

40.2

593

15

131.

70

0.60

82

0.

6082

0.60

82

0.40

69

Rea

lized

F 1

pro

gen

y

9749

.61

R

0 ( F

1 / l 0 )

9.74

96

Life tables of C. ohridella 151

© 2007 The Authors

Journal compilation © 2007 The Royal Entomological Society, Agricultural and Forest Entomology, 9, 141–158

Tab

le 7

Life

tab

le f

or t

he s

econ

d g

ener

atio

n of

Cam

erar

ia o

hrid

ella

in D

elém

ont,

Sw

itzer

land

, 20

03

Ap

par

ent

mor

talit

y R

eal m

orta

lity

Sta

ge

Fa

ctor

M

arg

inal

atta

ck

rate

Sta

ge

Fact

or

Sta

ge

Fact

or

k -va

lue

Sta

ge

Fact

or

l x d

x d

x q

x q

x d

x / l 0

d x /

l 0 Fa

ctor

Eg

g

10

00

178.

57

0.

1786

0.17

86

Eg

gs

dis

app

ear

off l

eaf

13

3.92

86

0.13

39

0.

1339

0.13

39

0.06

24

E

gg

s fl a

t and

em

pty

35.7

143

0.03

86

0.

0357

0.03

57

0.01

71

E

gg

s op

ened

8.92

86

0.00

98

0.

0089

0.00

89

0.00

43

L1

82

1.43

41

.07

0.

0500

0.04

11

Pla

nt d

efen

se r

eact

ion

28

.750

0 0.

0353

0.03

50

0.

0288

0.

0156

Oth

er

10

.267

9 0.

0127

0.01

25

0.

0103

0.

0056

Leaf

sen

esce

nce

2.

0536

0.

0025

0.00

25

0.

0021

0.

0011

L2

780.

36

84.2

0

0.10

79

0.

0842

P

lant

def

ense

rea

ctio

n

47.2

321

0.06

20

0.

0605

0.04

72

0.02

78

O

ther

32.8

571

0.04

36

0.

0421

0.03

29

0.01

93

P

red

atio

n (b

irds)

2.05

36

0.00

28

0.

0026

0.00

21

0.00

12

Le

af s

enes

cenc

e

2.05

36

0.00

26

0.

0026

0.00

21

0.00

11

L3

69

6.16

51

.34

0.

0737

0.05

13

Pre

dat

ion

(art

hrop

ods)

14.3

750

0.02

12

0.

0206

0.01

44

0.00

93

P

red

atio

n (b

irds)

12.3

214

0.01

82

0.

0177

0.01

23

0.00

80

O

ther

12.3

214

0.01

82

0.

0177

0.01

23

0.00

80

Le

af s

enes

cenc

e

4.10

71

0.00

59

0.

0059

0.00

41

0.00

26

P

lant

def

ense

rea

ctio

n

4.10

71

0.00

61

0.

0059

0.00

41

0.00

27

P

aras

itism

4.10

71

0.00

61

0.

0059

0.00

41

0.00

27

L4

64

4.82

80

.09

0.

1242

0.08

01

Pre

dat

ion

(bird

s)

45

.178

6 0.

0721

0.07

01

0.

0452

0.

0325

Pre

dat

ion

(art

hrop

ods)

12.3

214

0.02

02

0.

0191

0.01

23

0.00

89

O

ther

12.3

214

0.02

02

0.

0191

0.01

23

0.00

89

Le

af s

enes

cenc

e

6.16

07

0.00

96

0.

0096

0.00

62

0.00

42

P

aras

itism

4.10

71

0.00

68

0.

0064

0.00

41

0.00

30

Sp

in

56

4.73

76

.75

0.

1359

0.07

68

Pre

dat

ion

(bird

s)

61

.607

1 0.

1106

0.10

91

0.

0616

0.

0509

Pre

dat

ion

(art

hrop

ods)

8.21

43

0.01

55

0.

0145

0.00

82

0.00

68

P

aras

itism

4.10

71

0.00

78

0.

0073

0.00

41

0.00

34

Le

af s

enes

cenc

e

2.82

37

0.00

50

0.

0050

0.00

28

0.00

22

Pup

ae

48

7.98

26

3.55

0.54

01

0.

2636

P

red

atio

n (b

irds)

181.

1909

0.

4137

0.37

13

0.

1812

0.

2319

Leaf

sen

esce

nce

70

.005

6 0.

1435

0.14

35

0.

0700

0.

0673

Oth

er

10

.294

9 0.

0299

0.02

11

0.

0103

0.

0132

Par

asiti

sm

2.

0590

0.

0060

0.00

42

0.

0021

0.

0026

A

dul

ts

22

4.43

Sex

rat

io

0.

54

P

oten

tial f

ecun

dity

100.

248

P

oten

tial F

1 p

rog

eny

12

171.

38

8043

.35

0.

6608

0.66

08

R

ealiz

ed fe

cund

ity

34

8043

.35

0.66

08

0.

6608

0.66

08

0.46

96

Rea

lized

F 1

pro

gen

y

4128

.03

R

0 ( F

1 / l 0 )

4.12

80

152 S. Girardoz, D. L. J. Quicke and M. Kenis

© 2007 The Authors

Journal compilation © 2007 The Royal Entomological Society, Agricultural and Forest Entomology, 9, 141–158

Tab

le 8

Life

tab

le f

or t

he t

hird

, ov

ewin

terin

g g

ener

atio

n of

Cam

erar

ia o

hrid

ella

in D

elém

ont,

Sw

itzer

land

, 20

03

Ap

par

ent

mor

talit

y R

eal m

orta

lity

Sta

ge

Fa

ctor

M

arg

inal

atta

ck

rate

Sta

ge

Fact

or

Sta

ge

Fact

or

k -va

lue

Sta

ge

Fact

or

l x d

x d

x q

x q

x d

x / l 0

d x /

l 0 Fa

ctor

Eg

g

10

00

756.

10

0.

7561

0.75

61

Eg

gs

dis

app

ear

off l

eaf

38

2.11

38

0.38

21

0.

3821

0.38

21

0.20

91

E

gg

s fl a

t and

em

pty

361.

7886

0.

4909

0.36

18

0.

3618

0.

2932

Eg

gs

open

ed

12

. 195

1 0.

0225

0.01

22

0.

0122

0.

0099

L1

243.

90

17.6

8

0.07

25

0.

0177

O

ther

9.14

63

0.03

82

0.

0375

0.00

91

0.01

69

P

lant

def

ense

rea

ctio

n

8.53

66

0.03

57

0.

0350

0.00

85

0.01

58

L2

22

6.22

25

.61

0.

1132

0.02

56

Leaf

sen

esce

nce

10

.365

9 0.

0458

0.04

58

0.

0104

0.

0204

Oth

er

7.

9268

0.

0365

0.03

50

0.

0079

0.

0162

Pla

nt d

efen

se r

eact

ion

7.

3171

0.

0337

0.03

23

0.

0073

0.

0149

L3

200.

61

27.4

4

0.13

68

0.

0274

Le

af s

enes

cenc

e

10.9

756

0.05

47

0.

0547

0.01

10

0.02

44

O

ther

8.53

66

0.04

47

0.

0426

0.00

85

0.01

99

P

aras

itism

3.65

85

0.01

94

0.

0182

0.00

37

0.00

85

H

ost f

eed

ing

2.43

90

0.01

30

0.

0122

0.00

24

0.00

57

P

red

atio

n (a

rthr

opod

s)

1.

2195

0.

0065

0.00

61

0.

0012

0.

0028

Pre

dat

ion

(bird

s)

0.

6098

0.

0033

0.00

30

0.

0006

0.

0014

L4

173.

17

68.9

0

0.39

79

0.

0689

Le

af s

enes

cenc

e

34.7

561

0. 2

007

0.

200

7

0.03

48

0.09

73

O

ther

14.6

341

0.10

21

0.

0845

0.01

46

0.04

68

P

red

atio

n (b

irds)

8.53

66

0.06

09

0.

0493

0.00

85

0.02

73

P

aras

itism

7.92

68

0.05

67

0.

0458

0.00

79

0.02

53

P

red

atio

n (a

rthr

opod

s)

2.

4390

0.

0178

0.01

41

0.

0024

0.

0078

Hos

t fee

din

g

0.

6098

0.

0045

0.00

35

0.

0006

0.

0019

S

pin

104.

27

73.7

8

0.70

76

0.

0738

Le

af s

enes

cenc

e

39.0

244

0.37

43

0.

3743

0.03

90

0.20

36

P

red

atio

n (b

irds)

32.3

171

0.41

64

0.

3099

0.03

23

0.23

39

P

aras

itism

2.43

90

0.03

98

0.

0234

0.00

24

0.01

77

Pup

ae

30

.49

4.27

0.14

00

0.

0043

P

red

atio

n (b

irds)

4.26

83

0.14

00

0.

1400

0.00

43

0.06

55

Pup

ae in

dia

pau

se

26.2

2 22

.64

0.

8636

0.02

26

Ear

thw

orm

s

22.3

0 0.

8595

0.85

06

0.

0223

0.

8523

Par

asiti

sm

0.

17

0.01

49

0.

0065

0.00

02

0.00

65

O

ther

0.17

0.

0149

0.00

65

0.

0002

0.

0065

A

dul

ts

3.

58

S

ex r

atio

0.54

Pot

entia

l fec

und

ity

10

0.24

8

Pot

entia

l F 1

pro

gen

y

193.

90

128.

14

0.

6608

0.66

08

R

ealiz

ed fe

cund

ity

34

128.

14

0.66

08

0.

6608

0.66

08

0.46

96

Rea

lized

F 1

pro

gen

y

65.7

6

R 0

( F 1 /

l 0 )

0.

0658

Life tables of C. ohridella 153

© 2007 The Authors

Journal compilation © 2007 The Royal Entomological Society, Agricultural and Forest Entomology, 9, 141–158

Tab

le 9

Life

tab

le f

or t

he f

irst

gen

erat

ion

of C

amer

aria

ohr

idel

la in

Del

émon

t, S

witz

erla

nd,

2004

Ap

par

ent

mor

talit

y R

eal m

orta

lity

Sta

ge

Fa

ctor

M

arg

inal

atta

ck

rate

Sta

ge

Fact

or

Sta

ge

Fact

or

k -va

lue

Sta

ge

Fact

or

l x d

x d

x q

x q

x d

x / l 0

d x /

l 0 Fa

ctor

Eg

g

10

00

316.

42

0.

3164

0.31

64

Eg

gs

dis

app

ear

off l

eaf

23

9.72

38

0.23

97

0.

2397

0.23

97

0.11

90

E

gg

s fl a

t and

em

pty

70.6

389

0.08

14

0.

0706

0.07

06

0.03

69

E

gg

s op

ened

6.06

06

0.00

73

0.

0061

0.00

61

0.00

32

L1

68

3.58

51

.27

0.

0750

0.05

13

Pla

nt d

efen

se r

eact

ion

41

.014

6 0.

0605

0.06

00

0.

0410

0.

0271

Leaf

sen

esce

nce

6.

8358

0.

0100

0.01

00

0.

0068

0.

0044

Oth

er

3.

4179

0.

0052

0.00

50

0.

0034

0.

0023

L2

632.

31

93.9

9

0.14

86

0.

0940

P

lant

def

ense

rea

ctio

n

49.5

593

0.08

14

0.

0784

0.04

96

0.03

69

O

ther

18.7

984

0.03

17

0.

0297

0.01

88

0.01

40

P

red

atio

n (a

rthr

opod

s)

10

.253

7 0.

0174

0.01

62

0.

0103

0.

0076

Leaf

sen

esce

nce

8.

5447

0.

0135

0.01

35

0.

0085

0.

0059

Hos

t fee

din

g

5.

1268

0.

0087

0.00

81

0.

0051

0.

0038

Par

asiti

sm

1.

7089

0.

0029

0.00

27

0.

0017

0.

0013

L3

538.

32

30.7

6

0.05

71

0.

0308

P

red

atio

n (a

rthr

opod

s)

18

.798

4 0.

0349

0.03

49

0.

0188

0.

0154

Par

asiti

sm

5.

1268

0.

0098

0.00

95

0.

0051

0.

0043

Oth

er

3.

4179

0.

0065

0.00

63

0.

0034

0.

0028

Pla

nt d

efen

se r

eact

ion

3.

4179

0.

0065

0.00

63

0.

0034

0.

0028

L4

507.

56

109.

37

0.

2155

0.10

94

Pre

dat

ion

(art

hrop

ods)

97.4

097

0.19

44

0.

1919

0.09

74

0.09

39

P

red

atio

n (b

irds)

3.41

79

0.00

76

0.

0067

0.00

34

0.00

33

Le

af s

enes

cenc

e

3.41

79

0.00

67

0.

0067

0.00

34

0.00

29

P

aras

itism

3.41

79

0.00

76

0.

0067

0.00

34

0.00

33

O

ther

1.70

89

0.00

38

0.

0034

0.00

17

0.00

16

Sp

in

39

8.18

44

.43

0.

1116

0.04

44

Pre

dat

ion

(art

hrop

ods)

27.3

431

0.07

02

0.

0687

0.02

73

0.03

16

P

red

atio

n (b

irds)

6.83

58

0.01

80

0.

0172

0.00

68

0.00

79

Le

af s

enes

cenc

e

5.12

68

0.01

29

0.

0129

0.00

51

0.00

56

P

aras

itism

3.41

79

0.00

91

0.

0086

0.00

34

0.00

40

O

ther

1.70

89

0.00

45

0.

0043

0.00

17

0.00

20

Pup

ae

35

3.75

90

.57

0.

2560

0.09

06

Pre

dat

ion

(art

hrop

ods)

35.8

878

0.11

06

0.

1014

0.03

59

0.05

09

Le

af s

enes

cenc

e

23.9

252

0.06

76

0.

0676

0.02

39

0.03

04

P

red

atio

n (b

irds)

11.9

626

0.03

83

0.

0338

0.01

20

0.01

70

O

ther

8.54

47

0.02

75

0.

0242

0.00

85

0.01

21

P

aras

itism

6.83

58

0.02

21

0.

0193

0.00

68

0.00

97

Con

tinue

d

154 S. Girardoz, D. L. J. Quicke and M. Kenis

© 2007 The Authors

Journal compilation © 2007 The Royal Entomological Society, Agricultural and Forest Entomology, 9, 141–158

high net rates of increase, as shown in this study, which allows C. ohridella to build outbreak populations year after year.

Parasitoids are known as the most important natural ene-mies of leaf miners ( Askew & Shaw, 1979; Faeth & Simberloff, 1981; Van Driesche & Taub, 1983; Hespenheide, 1991; Hawkins et al. , 1997 ) and parasitism rates of 40% and higher are commonly cited. Faeth & Simberloff (1981) men-tioned parasitism rates of 40 – 50% on a Cameraria sp. and noted that exclusion of parasitoids considerably reduced the mortality of larvae. Askew & Shaw (1979) studied Phyllonorycter spp. on oak and birch and found out that pop-ulations were regulated and kept at low levels almost entirely by the action of parasitoids. With C. ohridella being an ex-otic insect in central Europe, it is expected to be less heavily parasitized than native leaf miners. However, leaf miners are notorious among insects for being parasitized, mainly by polyphagous parasitoids attacking various groups of leaf miners on different host plants. Consequently, it is common for exotic leaf miners to become heavily parasitized by na-tive parasitoids. Examples include Phyllonorycter robiniella introduced in Europe in the 1980s, which exhibits parasitism rates of 30 – 70% ( Stojanovic & Markovic, 2005 ), Phyllocnistis citrella , introduced to Spain in 1993 and parasitized up to 70% by native parasitoids 4 years later ( Urbaneja et al. , 2000 ), and Phyllonorycter leucographella , which was al-ready parasitized at 56% 16 years after its introduction to England ( Godfray et al. , 1995 ). In Europe, C. ohridella has indeed been adopted by over 30 native, polyphagous parasi-toids. However, parasitism rates remain low (Grabenweger et al. , 2005a; Girardoz et al. , 2006; Volter & Kenis, 2006) . Several reasons have been proposed to explain the low para-sitism rates observed in C. ohridella . One of them is a lack of synchronization between parasitoid emergence and the first generation of C. ohridella in spring ( Grabenweger, 2004; Girardoz et al. , 2006 ). Indeed, the bulk of the parasitoids emerge at least 6 weeks before the first suitable C. ohridella larvae are available, suggesting that alternate hosts are needed. However, Girardoz et al. (2006) showed that parasit-ism is not greater in forests, where alternate hosts are sup-posed to be more available, than in cities. Furthermore, parasitism rates do not increase in the subsequent generations in summer and autumn, when generations overlap and syn-chronization is not problematical. Other possible reasons for low observed parasitism rates could be that parasitoids are poorly attracted or even repelled by A. hippocastanum , which does not host any other leaf miner, or the low physiological suitability of larvae and pupae of the non-European genus Cameraria for European parasitoids. Laboratory rearing tests and olfactometry observations are needed to test these hypotheses.

Predation rates were very variable but were often greater than parasitism rates. Predation by birds was often the main mortality factor on mature larvae of non-overwintering gen-erations. Predation has been poorly studied in C. ohridella . Zegula et al. (2002) and Radeghieri (2004) made observa-tions on bird and ant predation, respectively, but it is the re-cent study by Grabenweger et al. (2005b) that provides the most complete information on predation on C. ohridella . They determined and quantified invertebrate and bird

A

pp

aren

t m

orta

lity

Rea

l mor

talit

y

Sta

ge

Fa

ctor

M

arg

inal

atta

ck

rate

Sta

ge

Fact

or

Sta

ge

Fact

or

k -va

lue

Sta

ge

Fact

or

l x d

x d

x q

x q

x d

x / l 0

d x /

l 0 Fa

ctor

P

upae

in d

iap

ause

3.41

79

0.01

11

0.

0097

0.00

34

0.00

48

Ad

ults

263.

18

S

ex r

atio

0.54

Pot

entia

l fec

und

ity

10

2.74

Pot

entia

l F 1

pro

gen

y

1462

7.96

88

96.0

7

0.60

82

0.

6082

Rea

lized

fecu

ndity

40.2

593

88

96.0

7 0.

6082

0.60

82

0.

6082

0.

4069

R

ealiz

ed F

1 p

rog

eny

57

31.8

9

R 0

( F 1 /

l 0 )

5.

7319

Tab

le 9

Co

nti

nu

ed

Life tables of C. ohridella 155

© 2007 The Authors

Journal compilation © 2007 The Royal Entomological Society, Agricultural and Forest Entomology, 9, 141–158

Tab

le 1

0 Li

fe t

able

for

the

sec

ond

, ov

erw

inte

ring

gen

erat

ion

of C

amer

aria

ohr

idel

la in

Del

émon

t, S

witz

erla

nd,

2004

Ap

par

ent

mor

talit

y

Rea

l mor

talit

y

Sta

ge

Fa

ctor

M

arg

inal

atta

ck

rate

Sta

ge

Fact

or

Sta

ge

Fact

or

k -va

lue

Sta

ge

Fact

or

l x d

x d

x q

x q

x d

x / l 0

d x /

l 0 Fa

ctor

Eg

g

10

00

311.

02

0.

3110

0.31

10

Eg

gs

dis

app

ear

off l

eaf

30

6.47

81

0.30

65

0.

3065

0.30

65

0.15

89

E

gg

s fl a

t and

em

pty

4.54

55

0.00

66

0.

0045

0.00

45

0.00

29

L1

68

8.98

29

.28

0.

0425

0.02

93

Pla

nt d

efen

se r

eact

ion

17

.224

4 0.

0252

0.02

50

0.

0172

0.

0111

Oth

er

8.

6122

0.

0127

0.01

25

0.

0086

0.

0055

Leaf

sen

esce

nce

3.

4449

0.

0050

0.00

50

0.

0034

0.

0022

L2

659.

69

60.2

9

0.09

14

0.

0603

P

lant

def

ense

rea

ctio

n

34.4

488

0.05

33

0.

0522

0.03

44

0.02

38

O

ther

17.2

244

0.02

70

0.

0261

0.01

72

0.01

19

Le

af s

enes

cenc

e

5.16

73

0.00

78

0.

0078

0.00

52

0.00

34

P

red

atio

n (a

rthr

opod

s)

3.

4449

0.

0055

0.00

52

0.

0034

0.

0024

L3

599.

41

29.2

8

0.04

89

0.

0293

P

red

atio

n (a

rthr

opod

s)

17

.224

4 0.

0290

0.02

87

0.

0172

0.

0128

Leaf

sen

esce

nce

8.

6122

0.

0144

0.01

44

0.

0086

0.

0063

Oth

er

3.

4449

0.

0059

0.00

57

0.

0034

0.

0026

L4

570.

13

55.1

2

0.09

67

0.

0551

P

red

atio

n (b

irds)

15.5

020

0.02

82

0.

0272

0.01

55

0.01

24

P

red

atio

n (a

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156 S. Girardoz, D. L. J. Quicke and M. Kenis

© 2007 The Authors

Journal compilation © 2007 The Royal Entomological Society, Agricultural and Forest Entomology, 9, 141–158

predation in Austria and Switzerland and identified tits and the bush-cricket Meconema meridionale as the main preda-tors, which confirms our observations in Switzerland. Both Grabenweger et al. (2005b) and our study found that bird predation was mainly on spinning larvae and pupae whereas invertebrate predation occurred nearly exclusively on the last feeding stages. Grabenweger et al. (2005b) found M. meridi-onale to have a measurable negative impact on C. ohridella populations. Bird predation was estimated at 2 – 4% (i.e. of similar magnitude as parasitism). Although the comparison of predation rates between the two studies is difficult because of the different methods of measurement used, it appears that predation by birds was sometimes much greater in our study. For example, in the second and third generations of 2003, birds ate 7 – 41% of each of the stages L4, spinning larvae and pupae. In the second moth generation, birds killed 29% of the total generation, as shown by the real mortality rates in Table 7 . The fact that predation by birds was much higher in 2003, when moth populations were highest, compared with the two other years, suggests that predation may be density dependent, although Grabenweger et al. (2005b) could not draw any clear conclusions regarding density-dependence. Avian predation on C. ohridella requires further research, particularly its density-dependence and its evolution over time. Considering the great learning capacity of tits, it cannot be ruled out that they will adapt their behaviour to this new prey at a faster rate than arthropod predators or parasitoids ( Grabenweger et al. , 2005b ).

Predation on leaf-mining Lepidoptera by birds and inverte-brates has often been documented, but few studies provide a precise account of mortality due to all predators. Kirizoglu (1976) measured predation rates on larvae of Caloptilia syring-ella due to invertebrates of 33 and 50% in a spring and autumn generation, respectively. Predators were also reported to kill 24.7% of the leaf-mining stages of Cameraria hamadryadella ( Connor & Beck, 1993 ), 10 – 30% of those of a Cameraria sp. ( Faeth & Simberloff, 1981 ) and up to 60% of those of the inva-sive Phyllocnistis citrella ( Urbaneja et al. , 2000 ).

The main mortality factors of C. ohridella occur on the last, overwintering generation, which is the only one having a net rate of increase usually lower than one. Indeed, it is well known that, in most cases, population densities in spring are lower than in the previous generation in autumn. Our ob-servations showed that nearly 90% of the pupae in dead leaves died during winter, a proportion that corresponds to what other authors have found on Phyllonorycter spp. Pottinger & Leroux (1971) found that 84% of populations of P. blancardella died during the winter and for Phyllonorycter spp. on oak, this percentage was of 50% ( Connor, 1984 ). Laing et al. (1986) determined that the majority of this mor-tality is due to earthworms, which bury and eat the leaves and therefore destroy the pupae or prevent the hatching adults from reaching the surface. Our study was made at one loca-tion only and it remains to be determined whether earth-worms and other leaf decomposers have a similar impact in other localities and on other soils. The observations were made in the countryside, at the edge of a meadow and a for-est. In urban areas, where most horse-chestnut trees are found in Central Europe, most dead leaves are removed or blown

away, which probably has a similar effect on moth popula-tions as leaf decomposers in rural areas. Leaf removal in au-tumn has an important impact on populations of C. ohridella in the next spring ( Gilbert et al. , 2003; Pavan et al. , 2003 ), suggesting again that winter mortality has a key role in the population dynamics of the moth.

Other major causes of mortality in the last generation are leaf senescence and intraspecific competition. Climatic con-ditions during the summer largely determine the synchroni-zation between the development of C. ohridella and leaf senescence in autumn. In Delémont, during the relatively cool summers in 2002 and 2004, the development of C. ohridella was rather slow and only two generations devel-oped. Nearly all pupae of the second generation entered into diapause and, consequently, populations in the next year in-creased compared with the previous year. By contrast, in 2003, the unusually warm summer induced a third genera-tion. Only a part of this third generation reached the pupal stage due to high larval mortality, which resulted in a low level of attack in spring 2004.

When horse-chestnuts are heavily attacked by C. ohridella , larvae may die from intraspecific competition, and leaf se-nescence occurs earlier than normal ( Pschorn-Walcher, 2001 ), a phenomenon that is often seen in leaf-miners when they occur at high densities ( Quiring & McNeil, 1984; Faeth, 1992; Connor & Beck, 1993 ). Connor & Beck (1993) even described epidemic years of Cameraria hamadryadella (Clemens) where 53% of the population died as a result of intraspecific competition and only 0.6% of the population survived. Intra-specific competition did not appear as an im-portant mortality factor in our life tables. In 2002 and 2004, populations were too low to suffer from competition. In 2003, mortality through intraspecific competition was re-corded, in the ‘other mortality’ category, but was probably largely underestimated, especially in the last generations. First, leaf samples were always taken from the trees, even late in the season when the heaviest attacked leaves (i.e. those in which intraspecific competition was most likely to occur) had already dropped. Second, leaf senescence and in-traspecific competition are clearly overlapping mortality fac-tors. High mine densities (i.e. intraspecific competition) cause early leaf senescence and, most probably, delays in lar-val development due to lower food quality. Thus, at least a part of the mortality attributed to leaf senescence could have been attributed to intraspecific competition.

Acknowledgements

We thank Giselher Grabenweger (BOKU, Vienna) and Hannes Bauer (Natural History Museum, Bern) for their help in the identification of parasitoids, Natalia Guazzone, Sébastien Marcombe, Ghislaine Cortat and Audrey Favereau for their help in field and laboratory work, Hefin Jones and Jon Knight for fruitful discussion and comments on the manuscript, and Werner Heitland for his support during the whole study. The project was funded by the Swiss Federal Office for Education and Science as part of the European Union FWP5 project CONTROCAM (QLK5-CT-2000-01684), and by the EU FWP6 project ALARM (GOCE-CT-2003-506675).

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Accepted 2 January 2007 First published online 2 March 2007