Underestimated Damage Caused by the European Hazelnut Weevil, Curculio nucum (Curculionidae)

Abstract

Hazelnut is an important food resource for the larvae and adults of the hazelnut weevil, Curculio nucum. While wormy nuts reflect the impact of such weevils at harvest time, little is known about the other types of damage they cause. To establish a comprehensive list of damages, and thereby identify the period of hazelnut vulnerability, male and female weevils were collected weekly and isolated on fruiting branches for 1 week. Based on nut development, higher rates of dropped nutlets, belted nuts, and blank nuts were observed at harvest. Marks specific to weevils, including wormy nuts, riddled shells, and larvae paths on the basal scar, were recorded during nut lignification. Belted nuts and blank nuts are empty nuts and constituted the main damage. The feeding activities of both the adults and larvae, but also the oviposition punctures, are likely to be the main causes of embryo abortions. The greatest damages occurred during kernel growth and when the shell had almost reached its final size. The larvae failed to penetrate fully lignified shells, with dead larvae mainly being found on the basal scar, the later softer part of the hazelnut. In Ségorbe cultivars, the dynamic of hazelnut development is the main factor involved in its susceptibility to C. nucum, with aborted nuts being the most underestimated damage.

1. Introduction

Many species of hazelnut are cultivated around the world. The most common is Corylus avellana L. (Fagales: Corylaceae) [1]. Corylus avellana, also known as the European hazelnut, is a widespread Euro-Siberian plant species. After the last ice age, the species spread to the rest of Europe from refugia located in the Balkans, southern Italy, and southwestern France [2,3,4]. This old species was one of the first food resources for the first Europeans [5,6,7] and is still a popular product to this day. Major growth in hazelnut production has taken place in recent years.

Currently, the hazelnut is one of the most significant nut crops, accounting for over 1,015,216 ha and producing roughly 1,072,320 t in 2020 [8]. Turkey is the largest producer of hazelnuts in the world, supplying more than 62% of the growing global demand, followed by Italy (13.1%) and the USA (6%), with France in ninth place at 0.9% [8].

Depending on the country, hazel orchards are distinguished by their multiplicity, from small and traditional organic orchards with natural brushes to extensive orchards with several inputs. Hazelnut crops are generally poorly treated against pest insects. Few species had been identified as major pests [9,10,11], but when orchards are not treated with regularly with pesticides, these species can cause significant yield losses. In France, the hazelnut weevil, Curculio nucum Linnaeus, 1758 (Coleoptera: Curculionidae: Curculionini), is the main pest, followed by generalist pests, such as true bugs [12].

Curculio nucum is native to and widespread throughout Europe, predating European hazelnuts [13]. It is a pre-dispersal seed predator. The insect has coevolved with its host, leading to a strong relationship between the phenological traits of the insect and the fruit [14]. Contrary to other hazelnut weevils, C. nucum seems to have developed only in association with C. avellana [13,15] and remains at its vicinity [15,16]. Curculio nucum is a univoltine small nut weevil, measuring 6 to 7 mm in length, with a long rostrum (from 4 to 6 mm in males and females). In France, from April to May, the imagos leave the soil and climb to the hazelnut trees, where they feed on the nutlets, leaves, and shoots. The male/female ratio is close to one. In May, the insects explore the surrounding hedges, feeding on various small fruits [17]. After 3 months of pre-oviposition time [18], the insect becomes sexually mature and, in June, gravid females lay their eggs on unmature hazelnuts [19,20]. Up to four adults per branch per week can be detected in unmanaged orchards (R.H., personal observation, 2016). Their long rostrums allow the females to reach the exocarp, excavating egg chambers under the involucre. An extendable ovipositor, which is as long as the rostrum, allows them to deposit a single egg in each fruit. The future larvae are thus protected, while being close to their food source. The larvae feed on the kernel, developing through four instars [17,21]. At the end of the summer, the fourth instar chews an exit hole in the shell and drops to the soil where it enters to overwinter. The seasonal dynamics of the populations and the oviposition time vary according to the climatic conditions [21,22,23] and nut development [20,24,25,26]. Nut phenology is one of the main biotic parameters leading to cultivar susceptibility [13,22,27].

In C. avellana, pollination occurs in winter and fertilization occurs in spring. In southern France, where most hazelnut orchards are planted, ovule development begins in March and fertilization occurs between the end of May and the third week of June, based on the variety. In August, kernel maturation ends and the nuts are harvested [28]. Various non-exclusive problems may be associated with hazelnut weevil (adults and/or larvae) attacks that depend on the timing of the attack and, thus, on the stage of nut development (or cultivar), including nutlet drop (i.e., clusters of one to five small (<5 mm) nuts), blank nuts (i.e., having no kernel or kernel abortion), belted nuts (blank nuts where the shell is deformed at the lignification line), and shrivelled kernels, along with exclusive attacks, such as wormy nuts. Blank nuts and belted nuts are shells that contain no kernels or where the kernels only occupy up to a quarter of the shell’s capacity. While pollination encourages the development of the shell, it is unclear why the kernel fails to proceed normally. Either the embryos are aborted [29,30,31] or they begin to grow but stop or the kernel shrivels before filling the ovary cavity. Abortion may be trigged by climatic and/or physiological disturbances [29,32,33,34]. The primary symptom of abortion is “browning”, where the endocarp (i.e., parenchyma) has decayed [31].

Curculio nucum is the main threat for hazelnut crops. In France, without management, yields can be reduced by up to 80% [11]. According to our knowledge, no biological control solution exists against the pest. Pyrethroids are commonly used to control the pest in orchards. Contrary to previously used systemic products, such as neonicotinoids, pyrethroids have a short persistence and, therefore, the protection they afford is reduced. This implies an extended period of vulnerability to hazelnut weevils. The seasonality of the pest in hazelnut orchards is known [19,20], but their damage in relation to nut development has been poorly studied [20,26]. The well-known empty nut with the larval exit hole has been a focus of attention, whereas non-exclusive damages have not been systematically assessed. Only a few studies have been conducted on the various kinds of damage inflicted by C. nucum on hazelnuts [17,22], with none of these involving French orchards. The purpose of this study was, therefore, to assess all the internal and external defects caused by hazelnut weevils during nut development. For this purpose, weevils were isolated in net sleeves and the defects in Ségorbe hazelnuts were assessed. The results are discussed in light of the phenology of the nuts and the dynamics of the hazelnut weevil populations in the field.

2. Materials and Methods

2.1. Insects

From 7 April to 27 July 2020, adults of C. nucum were collected weekly from an untreated hazelnut orchard where the insect was abundant. The orchard was planted with Fertile and Ségorbe cultivars and located close to the city of Castelmoron-d’Albret, France (44°41′29.6″ N, 0°01′06.2″ W, 93 m a.s.l.). The insects were collected weekly because the hazelnut weevil’s physiology evolves through time, from immature insects in spring to gravid females in summer. The weevils were kept in cages (BugDorm-1, MegaView Science, Taipei, Taiwan) and supplied with water (in a glass tube plugged with cotton) and food (apples and hazelnuts). The cages were maintained under laboratory conditions at 21 ± 1 °C and 40 ± 5% relative humidity, with a natural light rhythm provided by windows (from 14 h of daylight at the beginning of May to 13 h of daylight at the end of August). The insects were kept in the cages for 24 h, at most, before being introduced into the net sleeves. One week of net sleeve isolation was made for successive weeks separately during the period of 15–31 weeks of the year. After 1 week of net sleeve isolation, the weevils were removed and counted. The mortality rate was estimated and compared between the sexes.

2.2. Field Study

An untreated orchard planted with the Ségorbe cultivar was used for the trials. In France, Ségorbe is one of the main commercial hazelnut cultivars and also a cultivar susceptible to weevil damage. The orchard was located in the city of Cancon, France (44°32′31.7″ N, 0°36′04.4″ E, 113 m a.s.l.), and the experiment was conducted from 8 April to 28 July 2020. Eighty-five trees of the same rank were selected. On 1 April, net sleeves were installed on 255 boughs bearing at least two nutlet clusters, with three sleeves per tree. At that time, the exact number of future fruits was impossible to determine. According to the literature, clusters in Ségorbe cultivars bear 3–4 nuts per nutlet [11]. Three net sleeves per tree and one sleeve net per bough were used. Three males were inserted into one of the net sleeves, three females in another, and the last was kept free of insects to use as the control. The weevils were kept in the net sleeves for 1 week to allow them to be in contact with the nuts. Five replicates were settled per week. The net sleeves were then opened to remove the weevils and treated to avoid missing any, as described by Hamidi and coll. [12]. The experiment ended on 2 August. Two weeks later, when the orchard hazelnuts were harvested, the boughs inside the net sleeves were cut and the net sleeves were taken to the laboratory where they were kept in a ventilated room until examined.

2.3. Hazelnut Damage

From October to December, the net sleeves were open. First, the number of dropped nutlets was counted. Then, the external and internal defects of the hazelnuts were assessed. For the external defects, this involved the rate of belted nuts (deformation of the shell caused by premature ending of the lignification process), frequency of riddled shells (hazelnuts with small perforations, Ø < 1 mm), and nuts with dark larvae paths on them. The larvae paths were carefully observed, and indications of the presence of larvae were noted (i.e., dried larvae, cephalic capsules, and excrement). The internal defects were expressed as the percentage of blank nuts (i.e., no kernel or kernel abortion), shrivelled kernels, and the presence of larvae or their exit holes (Ø > 2 mm). Depending on the indications, the damages were grouped into two categories: exclusive (wormy nuts, drilled shells, and the presence of larvae paths) and non-exclusive (dropped nutlets, blank nuts, belted nuts, and shrivelled kernels). Supplementary Material available in Figures S1 and S2 show images from freshly attacked hazelnuts regularly field collected and damages observed in net sleeves at harvest, respectively.

Finally, to study their relationship to the hazelnut phenology, nut development was monitored using the hazelnuts collected weekly. Ten hazelnuts were collected randomly from each of the trees bearing net sleeves. The nuts were shelled, and the kernels were cut laterally into two parts with a knife. The nuts and kernels were measured using a caliper. Using the BBCH scale (Biologische Bundesanstalt, Bundessortenamt and Chemical Industry), the hazelnut phenology was divided into four main stages of development: pre-expansion (Stages 691 to 695 on the BBCH scale), shell expansion (Stages 710 to 750), kernel expansion (Stages 751 to 799), and kernel maturation (Stages 81 to 89) [28]. In the pre-expansion stage, neither the nut nor the kernel was well developed. In the shell-expansion stage, the nut was growing, the shell was hardening, and fertilization had occurred. In the kernel-expansion stage, the kernel was growing but the nut and the shell had stopped growing and had hardened. Finally, in the maturation stage, the kernel had finished growing and filled the shell. Finally, to estimate the total damages, the main external and internal defects were pooled (belted nuts, blank nuts, and wormy nuts). The total damage was corrected for control using Abbott’s formula [35], and the main period of total damages was estimated in relationship to the phenological development of the hazelnuts.

2.4. Statistical Analysis

Statistical analyses were conducted using XLSTAT v.2017.1.1 software (Addinsoft, Paris, France). After testing the homogeneity of variance and normality at the same phenological stage of hazelnut development, the rate of damage (e.g., blank nuts, belted nuts, shrivelled or wormy nuts) was compared against the controls and between the sexes. These comparisons were performed using either a one- or two-way non-parametric Mann–Whitney U test, respectively. The data are expressed as the mean associated with the standard deviation (mean ± SD).

3. Results

3.1. Damage

3.1.1. Dropped Nutlets

During this study, the nutlets mainly dropped between weeks 15 and 22 (Figure 1(a1)), corresponding to the period of pre-expansion of the shell (BBCH Stages 691 to 695). In the net sleeves, 1.55 ± 1.89 nutlets dropped in a control net sleeve, increasing to 2.77 ± 2.61 when in the presence of female weevils. More nutlets dropped (p < 0.05) in these than in the controls. The number of nutlets dropped consequently increased by a factor of 1.78. Observations of the nutlets indicated that the involucre was abnormally large compared to the expected nut size, especially in the latest weeks of the pre-expansion period. The nuts died while the involucre continued to grow, which was particularly notable at week 24 (see images in Figure 1(a1)). As expected, during shell expansion and maturation, the number of dropped nutlets did not differ from the control (p > 0.05).

3.1.2. Belted Nuts

The nuts became differentiated from week 23 and grew until week 26. A total of 472 hazelnuts were collected. Belted nuts were mainly observed during shell expansion (Figure 1(b1)). When females or males were present in the net sleeves, higher rates (p < 0.0001) of belted nuts were observed (Figure 1(b2)). A total of 28.84 ± 37.68 and 18.69 ± 30.09 belted nuts were observed in females and males, respectively. No sex-ratio bias was observed (p > 0.05) (Figure 2(b2)). There were no kernels present in the shelled belted nuts, and the remaining cupule was still adhered to the basal scar (i.e., hilum). Only a few belted nuts were observed in the controls.

3.1.3. Blank Nuts

Prior to week 27, the kernels were small (<5 mm). Hazelnut death first led to belted nuts and then to blank nuts (fully lignified empty shells) (Figure 1(c1)). In both cases, either no kernel or only a very small, dried kernel (apple seed-like) was observed. A higher proportion of blank nuts was found in the net sleeves between weeks 25 and 26, when the nuts had reached 85% of their final size and the kernels had begun to grow. During shell expansion and maturation, where 800 hazelnuts were observed (weeks 23 to 29), blank nuts were observed in the control (6.56 ± 12.40%). However, in the same period, blank nuts were five times more important in the net sleeves containing weevils, regardless of sex, being present as 34.8 ± 34.48% for females and 25.79 ± 25.63% for males (p < 0.05, respectively) (Figure 1(c2)).

3.1.4. Shrivelled Kernels

Shrivelled kernels were mainly observed during the period of kernel expansion (Figure 1(d1)). Kernel expansion occurred from weeks 26 to 29 (Figure 1(d1)). Over the period, 460 hazelnuts were observed. No differences were observed between the controls (2.34 ± 4.18%) and the net sleeves containing males (3.85 ± 8.62%) or females (8.22 ± 13.10%), with p = 0.066 (Figure 1(d2)).

3.1.5. Riddled Hazelnuts

Riddled hazelnuts were observed between weeks 22 and 31 (Figure 2(a1)). Half of the belted nuts collected from net sleeves had drilled holes. Multiple drilled holes were present in the shells. The drilled hole diameters corresponded to the rostrum diameters of both the males and females (R.H., personal observation, 2022). In the belted nuts, punctures were frequently observed in the lower third of the hazelnuts. The rate of riddled hazelnuts was higher in the net sleeves containing females (p = 0.017) (Figure 2(a2)). Females seemed to drill the shells later than males, especially from week 28.

3.1.6. Wormy Hazelnuts

Wormy nuts were observed between weeks 25 and 29, when the kernel was going through expansion and the shell had stopped growing (Figure 2(b1)). Among the 246 hazelnuts collected during this period in net sleeves with females, only 13 wormy ones were found. Three mature larvae were collected from among these and 10 had specific exit holes, with only one hole per hazelnut (Figure 2(b2)). As expected, holes (>2 mm) were found only on net sleeves containing females. No larvae were founded in the net sleeves, which suggests that they escaped by piercing the net or they had died and decomposed.

3.1.7. Hazelnuts with Larvae Paths

Larvae paths were observed on the shells collected from weeks 25 to 31 (Figure 2(c1)). The paths occurred as erratic dark-colored tracks on the basal scars of the shells. No paths were observed in the controls and net sleeves containing male weevils (Figure 2(c2)). Careful binocular observations showed the presence of small, dried larvae or at least their cephalic capsules (see images in Figure S2). The rate of nuts with paths increased over time (linear regression: n = 7, r = 0.87, p < 0.01).

Some of the larvae had managed to penetrate the shells, as indicated by paths oriented with the funicle canal positioned in the middle of the basal scar (i.e., the micropyle). Some instar larvae used the same hole used as an entrance to exit from, as suggested by the presence of a larger hole at the micropyle (illustrated in Figure 2(b1)). In the field, the same symptoms were observed on fresh nuts. These paths can also be observed on the cupule side, fixed to the basal scar (images are available in Figure S1).

3.1.8. Weevil Mortality and Total Damage

Between week 15 and 31, after 1 week of isolation, a mean of 2.80 ± 0.59 females and 2.53 ± 0.86 males were still living in the net sleeves per week. In the control sleeves, healthy hazelnuts accounted for 76.31 ± 21.79%, whereas in the net sleeves with weevils, there was 37.01 ± 29.74% (p < 0.0001). The healthy nuts had fully developed kernels. In terms of the total amount of primary damage (belted nuts, blank nuts, and wormy nuts), similar proportions of healthy nuts were recorded in the net sleeves with males as for females, at 35.88 ± 41.58% and 36.23 ± 42.85%, respectively (p > 0.05). The cumulative corrected damage showed that 78% of the total damage occurred between weeks 23 and 26, peaking at week 25, during which the rate more than doubled (Figure 3). The shell sizes varied from 12.06 ± 2.75 to 19.01 ± 2.97 mm and the kernels from 0.74 ± 0.49 to 4.75 ± 2.05 mm. At the peak, the shell and kernel sizes were 17.22 ± 2.03 and 2.21 ± 0.56 mm, respectively, with the nuts reaching 83.55% of their final size.

4. Discussion

If the hazelnut weevil damage has been long established [17], only the well-known hole in the shell and the consumed kernel caused by the last instar will draw attention. The non-exclusive symptoms are difficult to determine; therefore, so few studies have assessed their impact on the yield. Here, using net sleeves to isolate weevils on fruiting branches, a non-exclusive list of symptoms was determined, linked to the growth stages of the hazelnuts and, therefore, to weevils’ attacks. In order of importance, these were dropped nutlets, belted nuts, blank nuts, and wormy nuts. In terms of external damage, dark larvae paths and riddled nuts caused by the larvae and adults, respectively, were found. The main (and worst) symptoms observed from the net sleeves were empty nuts (i.e., belted nuts and blank nuts). Unlike the aesthetic defects, such as kernel deformation, the empty nuts represented a net loss for the growers.

In orchards, from April to May (weeks 15 to 22), sexually immature weevils emerge from the soil and climb into the trees [19]. At this time, the trees bear nutlets and the weevils can feed on them. The results showed that the nutlets dropped 1.8 times more frequently when the weevils were isolated with the nutlets. By comparison, in Turkey, Akça and Tuncer [22] showed that the rate of dropped nuts was 3.91 times higher in the presence of weevils. In the Ségorbe cultivar, based on the average of 3–4 hazelnuts per nutlet that would have been produced, these types of damages are potentially more severe than the other types of damages from later stages of nut growth.

In hazelnuts, shell lignification begins at the tip and proceeds towards the basal scar. The hardening stage is a race between seed survival and environmental stress. In the net sleeves, hardening proceeded from weeks 23 to 26 and, during that time, the main symptoms of damage observed were belted hazelnuts. When a hazelnut stops growing before becoming fully lignified (i.e., sclerotization), the unlignified part shrivels, leading to deformed shells (i.e., belted nuts). Almost all belted nuts were observed in the net sleeves containing weevils (93%). Both males and females feed on the shell, as indicated by the numerous riddled hazelnuts. Weevils can thus kill the nuts at different stages of the lignification progress, leading to various degrees of belted nuts. Observations showed that the weevils preferentially fed on the lower third of the shell (i.e., on the softer and unlignified part). Under both field and laboratory conditions, belted nuts were observed after the weevils had fed on green hazelnuts. Parenchyma oxidation (or decay) was initiated after the feeding punctures created brown and watery areas, leading to bicolored hazelnuts: brown on the unlignified part and green on the lignified tip of the shell (see images in Figure S1).

The relationship between belted nuts, blank nuts, and shrivelled kernels and kernel development stage was the same observed with true bugs [12,36,37]; that is, when the kernels were less than ~5 mm in diameter, the seeds died, leading from belted to blank nuts. When the shells stopped growing, blank nut symptoms were prevalent. According to Miller [31], when the whole internal structure turns a watery brown, the development of the kernel has stopped, leading to blank nuts. It is well known that a number of stressors are connected to the occurrence of blank nuts. This explains why they were present in insect-free net sleeves [29,32,33,34]. Blank nuts were numerous in the net sleeves containing weevils. Six times more blank nuts were observed with weevils than without. In the Turkish study, 12.6 times more blank nuts were caused by the presence of weevils [22]. Parenchyma oxidation occurs when it comes into contact with the exterior. Indeed, the observation of this on freshly attacked nuts indicates that rostrum penetration has led to parenchyma oxidation and, therefore, to seed death (Figure S1). Different damage behavior may lead to parenchyma oxidation, where adults puncture through to the epicarp (to feed, or to lay eggs in the case of females) and also where larvae have dug through the parenchyma to reach the kernel.

In terms of the adult weevils, the rate of blank nuts was not dependent on sex. The males exhibit more active feeding behavior than the females, but the females drill to deposit eggs [17]. Both these behaviors may explain why there were no differences in the blank-nut rate between sexes in the net sleeves. Observations of the fresh hazelnuts confirmed that parenchyma oxidation was initiated from the oviposition and that feeding punctures or larvae creating an area of decay around them led to the death of both the larvae and the seeds (see images in Figure S1). The decay caused by punctures or larvae was previously mentioned by Martin in 1949 [17] and also was observed in the North American hazelnut weevil, Curculio obtusus (Blanchard) [38].

Around mid-June, in the field, the females had mated and laid their first eggs. The egg-laying period lasts about a month, depending on the phenological development of the nuts [17,20,25]. In the net sleeves, wormy nuts were observed between weeks 25 and 29 (i.e., 16 June to 15 July). The first larvae were found after the kernel had started to grow. As with other Curculio species, the egg laying occurred during kernel development, at a time when the endosperm is jelly-like [39,40,41]. The latest larvae were found when the shell was fully developed. Lignification is complete when the shell has finished developing [20,25,42]. Hardness is one of the factors related to the end of larvae penetration [20,24,25], but it is not the only one [16,26,43]. During hazelnut growth, lignification starts at the tip, where the young embryo is located, and proceeds to the basal scar. The basal scar is therefore the last zone to lignify. The results of the net-sleeve experiment confirmed the hardness hypothesis. Indeed, from weeks 25 to 31, the rate of shells showing penetration failure increased as lignification progressed. Numerous young larvae were found in dark paths on the basal scars. Because the basal scar is the last part to be lignified, this may explain the path concentrations. Behavioral convergence was observed with the filbertworm, Cydia latiferreana Walsingham (Lepidoptera). The latter can penetrate the nut using the micropyle located on the basal scar, the softer, and also thinner, part of the shell [44,45,46]. From an evolutionary point of view, it would be strategic for a female of C. nucum to position her eggs as far from the tip as possible so that the female and larvae are able to pierce the epicarp; thus, by the time the first instar reached the embryo, the latter would be of sufficient size to enable it to complete its development.

As expected, one exit hole was observed per nut. In several Curculio species, the number of larvae and their developmental size are related to the resources available [17,47,48]. The embryo is the main food source, whereas parenchymatous tissue is not nutritious. The first larval transformation (from L1 to L2) takes place only when L1 begins to feed on the embryo [17,38]. According to the study by Martin [17], 47% of the larvae died in aborted hazelnuts: 32% of starvation and 15% by ingesting the bacteria present. The presence of pathogens in parenchyma decay was also mentioned by Akça and Tuncer [22]. In addition, larvae can kill the embryo, leading to abortion and starvation (see Figure S1). The limited amount of resources provided by the size of the seed could set an upper limit to their success, as has been described for various Curculio species [14,47,48]. The time of attack is therefore a key element in the success of the species. However, many failures (i.e., weevil development) were observed, as discussed above. This high failure rate, as mentioned in other studies [17,22,38], might not be a coincidence. In Europe, no pre-dispersal seed predators occur on hazel trees except for C. nucum, which destroys up to 80% of the seeds. Curculio nucum has probably had a major influence on the evolution of the protective characteristics of C. avellana, it being their obligate host plant and with the weevils staying within a short range of their host [15]. Therefore, abortion can be viewed as a mechanism whereby plants end their investment that contains offspring that would be unlikely to contribute to future generations except for that of its parasite. Nuts may therefore act as a dead end for many weevils, contributing to a reduction in local pressures.

In this study, a list of potential damages was identified, and their occurrence should be taken with caution. Here, a fixed number of weevils were isolated in net sleeves and therefore forced to be in contact with hazelnuts; but their occurrence and abundance in the field greatly depend on the agro-ecological context and abiotic parameters. The presence of larvae paths until the last week of experimentation (week 31, i.e., 28 July) showed that females are, however, able to lay eggs late in the season, making late cultivars susceptible to the pest. To contextualize the conclusions and evaluate the risk assessment of cultivars, temporal pattern study weevil populations are currently in progress at French orchards.

5. Conclusions

To conclude, in the present study, specific and non-specific weevil damages were identified. In order of importance, these were aborted embryos (belted nuts and blank nuts) and wormy nuts. Feeding and oviposition punctures and larvae feeding are likely the main causes of embryo abortion. Damage can occur throughout nut development, peaking when the nuts reach 83% of their final size and the kernel starts to grow. Insects can lay eggs late in the season, on lignified shells, although the larvae fail to penetrate these. In Ségorbe cultivars, the dynamic of hazelnut development is the main factor involved in its susceptibility to C. nucum, and empty nuts are an underestimated damage.