Jean-Baptiste Camps

Marguerite Vernet

Handling Heavily Abbreviated Manuscripts: HTR engines vs text normalisation approaches

Keywords: Abbreviations, Handwritten Text Recognition, Medieval Western Manuscripts

Although abbreviations are fairly common in handwritten sources, particularly in medieval and modern Western manuscripts, previous research dealing with computational approaches to their expansion is scarce. Yet abbreviations present particular challenges to computational approaches such as handwritten text recognition and natural language processing tasks. Often, pre-processing ultimately aims to lead from a digitised image of the source to a normalised text, which includes expansion of the abbreviations. We explore different setups to obtain such a normalised text, either directly, by training HTR engines on normalised (i.e., expanded, disabbreviated) text, or by decomposing the process into discrete steps, each making use of specialist models for recognition, word segmentation and normalisation. The case studies considered here are drawn from the medieval Latin tradition.

Introduction

Abbreviations in Western Medieval Manuscripts

In medieval Latin manuscripts, abbreviations are fairly common and follow a practice that was established, by and large, during the first centuries A.D., reserved for a time to administrative and everyday written production and then extended to literary manuscripts [START_REF] Hasenohr | Écrire en latin, écrire en roman: réflexions sur la pratique des abréviations dans les manuscrits français des XII e et XIII e siècles[END_REF][START_REF] Hasenohr | Abréviations et frontières de mots[END_REF]. They mostly derive from two antique conventional systems: notae antiquae, on the one hand, that proceed by suspension, superscript letters or tachygraphic signs, and mostly affect grammatical morphemes such as inflections, adverbs, prepositions, pronouns and the forms of the verb esse; Christian nomina sacra, on the other, abbreviations of holy names, by contraction [START_REF] Bischoff | Paläographie des römischen Altertums und des abendländischen Mittelalters[END_REF]. Extended by Irish monks, with the addition of new (insular) signs such as ÷ (est) and then standardised and generalised by the Carolingian renovatio, this system forms the basis for abbreviation practices in medieval Latin manuscripts, but also for the abbreviations of many vernaculars. They were notably adapted to Old French by Anglo-Norman scribes [START_REF] Hasenohr | Abréviations et frontières de mots[END_REF]. Inherited from this history are abbreviations that can be categorised as tachygraphic sign e.g. Tironian ⁊ (et) or ꝯ (cum, con-, com-,…). superscript letter e.g. superscript a for ua or ra in qͣ (qua), tͣ ns (trans). suspension e.g. ẽ (est). contraction e.g. D ̃S (Deus).

In the 12 th and 13 th centuries, the intellectual flourishing and the development of schools and universities caused a heavy demand for written artefacts. The copying of manuscripts expanded beyond the sole framework of monastic scriptoria and spread to the city in professional workshops and lay scriptoria. The development of a larger literate milieu of students and masters, and the growth of book production led to modifications in intellectual practices and ultimately in the processes of reading and writing. A switch, at least in scholastic milieus, from slow syllabic reading to faster, expert modes of reading, based on the global perception of each word, led to a very significant increase in word-level abbreviations, and, specifically, abbreviations by contraction [START_REF] Hasenohr | Abréviations et frontières de mots[END_REF]. They display much variety and include: simple contraction using letters from the original word (with a marker to make the presence of the abbreviation explicit) that can be relatively unambiguous, e.g. eccl ̃a (ecclesia), rōe (ratione) or ambiguous, e.g. ıͣ for ita, illa or infra, or even sometimes prima or una, depending on the context. composite contraction combining other conventional devices with the contraction itself, for instance ꝑͣ (persona).

In Latin manuscripts, we already encounter a great versatility of signs and many homographic abbreviations (or alternative expansions), a situation that is made even more uncertain in vernacular manuscripts, due to spelling variation.

Expanding abbreviations

Expanding abbreviations is not a trivial task because there is no unambiguous character-, syllable-or word-level mapping between abbreviation and expansion: the same abbreviation can correspond to several expanded forms, and an expanded form can have several abbreviations. In addition, the same sign can fulfil alternative functions on different levels. Attempts to model the relationship between abbreviations and expanded forms exist on a theoretical level in linguistic research [START_REF] Mazziotta | Traiter les abréviations du français médiéval: théorie de l'écriture et pratiques d'encodage[END_REF], but the situation remains complex. In graph theory terms, the binary relation between the set of abbreviations, and the set of expanded forms can be characterised as a many-to-many relation and not as a function. The same is also true at the level of the sequence of signs, that can have one expanded form e.g., rõe → ratione (Latin). many expanded forms ıͣ → ita, illa, infra, prima, una… (Latin).

The same sign can enter into different relations both in isolation and as part of groups. A good example of this plasticity is given by the common abbreviative mark known as 'titulus' or 'tittle': alone, it can be used to stand for a nasal consonant (-m-or -n-), while it is also the most common marker to indicate that a word is globally abbreviated, having, in that case no explicit character value per itself, for instance in the aforementioned rõe example. The actual incidence of abbreviation polyvalence varies in time, between languages and language variants, as well as per types of documents or texts, and ultimately, scribes.

Computational approaches

Handling abbreviations is a general problem with manuscripts, especially medieval manuscripts, but we find relatively few studies dealing with computational approaches to their expansion. The problem of homograph abbreviations and the versatility of signs seems to call for a representation of context. In practice, two main kinds of approaches have been used: HTR systems trained on normalised data on one hand; treating abbreviation expansion as a text normalisation task on the other.

HTR approaches can include some representation of token context, because state-of-the-art HTR systems usually take into account the full text line. From a pragmatic perspective, this makes the creation of ground truth easier, because it facilitates the reuse of existing transcriptions and has been investigated for this very reason, yet tended to show relatively high character error rate (CER), where 'deletions' (including letters that should have been added as part of abbreviation expansion) represent more than half of the errors [START_REF] Villegas | Exploiting existing modern transcripts for historical handwritten text recognition[END_REF][START_REF] Bluche | Preparatory kws experiments for large-scale indexing of a vast medieval manuscript collection in the Himanis project[END_REF].

Alternatively, normalisation can be treated as a separate (posterior) normalisation task, based on the output of the HTR phase. The literature concerning historical text normalisation is considerably larger, and includes approaches based on substitution lists, rules, as well as distance-based, statistical approaches (in particular, character-based neural machine translation) and more recently neural models [START_REF] Bollmann | A Large-Scale Comparison of Historical Text Normalization Systems[END_REF]. To include a modelling of context, normalisation systems can reuse deep-learning architectures originally intended for neural machine translation [START_REF] Bollmann | A Large-Scale Comparison of Historical Text Normalization Systems[END_REF][START_REF] Gabay | Traduction automatique pour la normalisation du français du XVIIe siècle[END_REF] or lemmatisation [START_REF] Camps | Stylometry for Noisy Medieval Data: Evaluating Paul Meyer's Hagiographic Hypothesis[END_REF][START_REF] Manjavacas | Improving lemmatization of nonstandard languages with joint learning[END_REF].

In this paper, we plan to explore two approaches to expand abbreviations in Latin manuscripts, with and without post-processing. Evaluations are carried out with a small dataset in order to highlight benefits of each approach within the scope of an under-resourced language.

MS BnF lat. 14525

For this work, we used MS BnF lat. 14525, the subject of an ongoing master's thesis [START_REF] Vernet | Un Manuscrit victorin au service de la pastorale du XIIIe siècle. Mas[END_REF]. It belonged to the library of Saint-Victor of Paris, a canonical Abbey that played a central role in the intellectual life of Paris, especially during the 12 th century, and was situated at the intersection between the monastic and Parisian worlds. BnF lat. 14525 was produced for the library of Saint-Victor in the first half of the 13 th century. It is not made up of a single codicological unit, but was completed and improved about ten years later. This manuscript of 305 folios brings together various texts from different origins (Victorian, Cistercian, Parisian schools) and includes spiritual treatises, works on practical theology, numerous sermons, Constitutions of the Fourth Lateran Council or synodal constitutions, and even particular material and spiritual privileges. Despite this heterogeneity, it is a very useful item for a better understanding of Saint-Victor during this time. About ten different hands wrote it, though the handwriting is quite similar. We are dealing here with a script akin to scholastic writing, with a few broken stems, a reduced module, as well as numerous abbreviations.

We focus here on one of these hands, which occupies a quarter of the manuscript, i. e. 79 fols, copied on two columns of 42 ruled lines (the first of which also carries writing), most likely between 1215 and 1225, on parchment of relatively good quality despite some defects. The copy is neat with few errors, and corrections by expunctuation or crossing out, as well as some interlinear or marginal additions. Hyphens and dotted 'i's are also present, although irregularly. The writing itself is very regular and skilled, and the use of abbreviations is quite essential. The density of abbreviations, measured as the ratio of words with at least one abbreviation, is around 47%, not out of the ordinary for this type of manuscript, but much larger than what is found for instance for contemporary Old French epic manuscripts, with figures in the 10 to 20% range [START_REF] Camps | La 'Chanson d'Otinel': édition complète du corpus manuscrit et prolégomènes à l'édition critique[END_REF]. We find the systematic abbreviation of et in two forms: & and ⁊. The copyist uses different tittles: ͛ mostly er, while ̄stands for nasals or signals suspensions or contractions. ᷑ is used for ur and ᷒ for us. Superscript letters are also abundantly used, in particular a, o and i. This frequent use of abbreviations is typical of the kind of scholastic writing whose use was widespread from the mid-13 th century in university circles.

Images of the manuscript are available on Gallica as a grayscale digitisation of the microfilm [START_REF]BnF: Petrus Pictaviensis, Tractatus de confessione (…)[END_REF].

Experiments and results

The paper aims to compare two approaches to decipher Latin abbreviations, and HTR experiments have been carried out with two neural architectures. The first one (HTR-CB) is proposed by Kraken [START_REF] Kiessling | Important new developments in arabographic optical character recognition (ocr)[END_REF].The results produced by this architecture serve as a baseline for pure character-level recognition of this manuscript and are provided to other modules in the defined pipeline (see infra 3.3). The second architecture (HTR-WB) is an adaptation of that proposed on Calfa Vision [START_REF] Vidal-Gorène | A Modular and Automated Annotation Platform for Handwritings: Evaluation on Under-resourced Languages[END_REF], originally developed for the reading of medieval Armenian manuscripts and the management of abbreviations and ideograms specific to this language and which cannot be recognised at the character level [START_REF] Vidal-Gorène | A Computational Approach of Armenian Paleography[END_REF]. Character recognition is preceded by a word-based system, to which we first provide an exhaustive list of abbreviations encountered in the manuscript. The results of this architecture serve as a point of comparison.

Ground truth creation

Training and testing data have been annotated with a layout analysis and a baseline model, and manually proofread via eScriptorium [START_REF] Kiessling | eScriptorium: An open source platform for historical document analysis[END_REF][START_REF] Kiessling | A modular region and text line layout analysis system[END_REF]. The dataset is composed of 1.861 lines of text (1,524 reserved for training, 168 for validation and 169 for testing). We built a total of four datasets:

1. D-exp, consisting of a transcription with full expansion of the abbreviations.

We consider two variants, D-exp1 with inter-word spaces restored (separation of words according to Latin grammar and not the spacing present in the manuscript), and D-exp2 without spaces. These datasets are respectively composed of 34 and 33 classes. The number of classes has been limited to include enough samples in each. This can lead to strong intra-class inertia, due in particular to the unsystematic grouping of upper-and lower-case letters for the less endowed classes. 2. D-abb, composed of transcriptions registering the abbreviation system used in this manuscript (see supra 1.1). We also consider two variants, D-abb1 with inter-word spaces, and D-abb2 without spaces. These datasets are respectively composed of 60 and 59 classes. In detail, we have 36 classes representing alphanumeric characters and punctuation marks, 10 classes specific to Latin paleography to represent certain abbreviations according to the same scheme as the Oriflamms project (e.g. ƀ and ꝙ; see infra), and 13

classes made up of combining signs (written above or below one or more letters). These last 13 classes can be difficult to identify for an HTR engine.

Moreover, additional data was used for some of the trainings:

1. Oriflamms diplomatic and allographetic transcriptions provided by D. Stutzmann and team [START_REF] Stutzmann | Recueil des actes de l'abbaye de Fontenay. TELMA[END_REF][START_REF] Ceccherini | Evaluating Deep Learning Methods for Word Segmentation of Scripta Continua Texts in Old French and Latin[END_REF][START_REF] Muzerelle | Modern vs diplomatic transcripts for historical handwritten text recognition[END_REF][START_REF] Stutzmann | Psautiers: Transcriptions de différents manuscrits[END_REF]. 2. PL 216 volumes of normalised editions from Migne's Patrologia latina [START_REF]Patrologiae cursus completus[END_REF].

HTR on abbreviated and expanded data

Common parameters have been chosen for training steps of HTR-CB and HTR-WB. Line images provided as input are resized to 64px in height and have varying widths. No Unicode normalisation or data augmentation is applied. A repolygonisation has been performed to equalise polygons of first and last rows of each text columns [START_REF] Vidal-Gorène | A Modular and Automated Annotation Platform for Handwritings: Evaluation on Under-resourced Languages[END_REF]. Due to the small size of the dataset and to avoid overfitting, training steps are carried out with a dynamic learning rate starting at 0.001 -to which a coefficient of 0.75 is applied every 10 epochs -, and we use a batch of one image for each iteration. We have limited training to 30 epochs. First results are summarised in Table 1. The two architectures give equivalent results on the two variants of the Dabb dataset. At identical initial parameters, we do not observe any significant difference, except that HTR-CB converges twice as fast as HTR-WB. A dynamic learning rate brings a real benefit for both of two architectures (stagnation of the CER until epoch 10 then gradual reduction). Epoch 30 is never reached. 20% of the errors of HTR-CB are focused on combining signs, but it generally recognises combined letters well. It also mistakes close classes as ꝑ and p, or ꝗ and q, but the lack of data can be a good explanation of this phenomenon.

There is a clear benefit to using a word-based approach for the management of abbreviations directly within the HTR process. If it seems quite logical that the absence of spaces, an ambiguous notion in manuscripts, can really benefit to text recognition, there is however only a marginal gain between D-abb1 and D-abb2. On the other hand, the HTR-WB model takes advantage of the lack of spaces. Most errors are focused on small and independent abbreviations, generally limited to one single character (e.g. m ͦ > modo), but also on long abbreviated words (e.g. micd ̃ia > misericordia) for which we do not have enough samples in the training set (e.g. only one sample of misericordia). We give in Table 2 an example of predictions. For the rest of the paper, we consider the HTR-CB output, as shown in Table 2.

GT-exp1

pro domo domini nos opponere non curamus. ti HTR-WB prodomo domini nos oponere non curamus. ti GT-abb2 ꝓdomodñinosoppoñeñcuram ᷒ .ti HTR-CB ꝓdomodñinosoppoñeñcuram ᷒ .tiẽ

Text normalisation approach

The modular text normalisation approach uses several consecutive steps, with specialised tools each necessitating a training of its own [START_REF] Camps | Stylometry for Noisy Medieval Data: Evaluating Paul Meyer's Hagiographic Hypothesis[END_REF], as follows (fig. 2):

1. HTR (see above). Word segmentation A neural word segmentor, Boudams, was trained using the best known configuration: convolutional encoder without position embeddings (Embedding 256, KernelSize 5, Dropout 0.25, Layers 10) [8]. Three datasets were used: for abbreviated text, D-abb (with word separation and line hyphenations normalised) alone, and with the addition of Oriflamms data; for normalised version, D-exp (with word separation and line endings normalised) with the addition of PL data. Three models were trained for each setting, and the best of the three (based on F-statistic) was selected. Results are shown in Table 3. Word normalisation For abbreviation expansion, the neural tagger Pie was trained [START_REF] Manjavacas | Improving lemmatization of nonstandard languages with joint learning[END_REF], following a setup already used for Old French [START_REF] Camps | Stylometry for Noisy Medieval Data: Evaluating Paul Meyer's Hagiographic Hypothesis[END_REF]. It was trained on an aligned version of the previous D-abb and D-exp (with word separation and line hyphenations normalised) alone, and with the addition of the Oriflamms data. Results are shown in Table 4.

Results

The full pipeline was evaluated globally on the normalised transcription of one folio of the manuscript, with expanded abbreviations, normalised word segmentation and line hyphenations. The metrics used were character error rate (CER) and word error rate (WER) in the Python fastwer implementation [START_REF] Wang | fastwer[END_REF]. Results are shown in Table 5.

Norm. Test

The simple use of an HTR engine, trained on a normalised transcription with normalised spaces and expanded abbreviations actually provides a strong baseline. This is particularly true of the word-based HTR, and in terms of character error rate. Yet, they are overperformed by the more refined setups, either in terms of character error rate or word error rate. The best scores (Table 5) are obtained, for the character error rate, by the HTR-WB trained on normalised transcriptions whose output is then resegmented by a word segmentor trained on the Patrologia latina; for the word error rate, by the HTR-CB trained on abbreviated transcriptions, whose output is then resegmented and normalised with models trained using the additional Oriflamms data.

Discussion and further research

Results seem to confirm the importance of the word level rather than the character level, with word-based overperforming character-based HTR, and with character-based HTR results being improved by adding tools dealing with wordlevel tokens and context, in particular for a small dataset. In this regard, artificial intelligence can be compared to human intelligence and seems to confirm the practice of global reading and global perception of the words rather than individual letters, reflected in the use of abbreviations in Latin (especially scholastic) manuscripts. Future research should investigate differences with vernacular manuscripts, for instance literature in Old French, where reading and the use of abbreviations are supposed to have remained mostly syllabic.

Another conclusion of this paper is that, given the nature of spacing in medieval manuscripts, the word error rate regarding normalised words can be greatly reduced by using a dedicated word segmentor, for which (normalised) training data can be easily collected (since all that is needed are normalised editions). In our experiments, this proved to be the best performing setup in terms of character error-rate.

Thirdly, a fully modular approach combining HTR on abbreviated data with a word segmentor and a text normalisation tool is the best performing in terms of word error rate. It would be possible to improve further the results of this approach by improving first the word-based approach -that still suffer of a lack of data to manage with the word level -, and then the segmentation and normalisation steps with additional data, yet the limit to this approach is the availability of adequate training material, i.e., editions recording abbreviations, that are much harder to come by than normalised editions.

Another future line of research should pursue the comparison with the vernacular, where the ambivalence of abbreviations, due to the variety of written norms and alternative spellings, should make the automated production of a normalised text more difficult. It should also investigate the impact of data augmentation techniques, particularly easy for the word segmentation training that could, for instance, include random character substitutions as to emulate HTR effect [8].

Fig. 1 .

 1 Fig. 1. Folio 45v, MS BnF lat. 14525

2 .Fig. 2 .

 22 Fig.2. Workflow for the full modular approach[START_REF] Camps | Stylometry for Noisy Medieval Data: Evaluating Paul Meyer's Hagiographic Hypothesis[END_REF]. The digital image is segmented in lines that are submitted to recognition, and the recognised text then goes through word segmentation and normalisation (abbreviation expansion).

Table 1 .

 1 Evaluation of character-based and word-based HTR system on datasets with and without expanded abbreviations.

		CER (%)
	D-exp1 D-exp2 D-abb1 D-abb2
	HTR-CB 10.59 9.69	4.89	4.55
	HTR-WB 3.76	2.96	5.57	4.83

Table 2 .

 2 Example of predictions with and without abbreviations.

Table 3 .

 3 Results for training of the word segmentor Boudams

			n-lines	test scores
	dataset	type	train dev test F-s. Prec. Recl.
	D-abb	abbr.	1 962 196 200 95.1 96.1 94.1
	D-abb+Oriflamms abbr.	17 139 196 200 97.3 97.4 97.1
	D-exp+PL	norm. 3 891 929 196 200 98.8 98.6 98.9

Table 4 .

 4 Results for the training of Pie for abbreviation expansion

		Test accuracy (%)
	dataset	all known unkn. ambig. unkn. targ.
	D-abb/D-exp	94.04 95.37 92.42 89.58	91.23
	D-abb/D-exp+Oriflamms 97.02 98.65 95.02 97.92	92.86

Table 5 .

 5 Results of the application of the full pipeline for a selection of the most accurate setups, with or without additional data.

		Setups	Scores
	HTR	Segment.

Table 6 .

 6 Facsimile and ground truth with sample predictions of the three best performing setups (word with content or segmentation errors in bold), from the beginning of fol. 45v (see fig. 1). amore uite temporalis. adefensione iusticie et ueritatis non flectitur. sedquis est hodie. qui animam suam ponatpro ouibus suis : cadit asella uicini. et piculo . amore uite temprus . a de sensione iusticie et ueritatis non flectitur . sed quis est hodie . qui animam suam ponat pro ouibus suis : cadit asella uicini . et 3b pculo . amoreure temporauis ; a defsasione iusticie et ueritatis non flectitur . sedquas st hodie . qui animam suam ponat pro ouibus suis : cadita sella uicini . et

	Facsimile	GT
		periculo . amore uite temporalis . a defen-
		sione iusticie et ueritatis non flectitur . sed
		quis est hodie . qui animam suam ponat
		pro ouibus suis : cadit asella uicini . et
	1b	2b
	piculo.

Acknowledgements

We thank the École nationale des chartes and the DIM STCN for the computing power and GPU server used for training, as well as INRIA and Calfa. We also thank Marc H. Smith for his keen review of our draft. Any remaining mistakes are only attributable to us.

Datasets availability

Datasets produced for this paper and evaluation scripts are available at DOI 10.5281/zenodo.5071963.

Data Soft. Data Soft. Data Soft CER WER 1a D-exp1 CB (HTR-CB) 15.63 82.38 1b D-exp1 WB (HTR-WB) 7.46 54.68 2a D-exp2 CB (HTR-CB) D-exp1+PL Boudams 12.65 50.83 2b D-exp2 WB (HTR-WB) D-exp1+PL Boudams 6.89 34.01 3a D-abb2 CB (HTR-CB) D-abb1 Boudams D-abb/exp Pie 10.89 41.28 3b D-abb2 CB (HTR-CB) +Orifl. Boudams +Orifl. Pie 8.60 31.81


domain: sdv sde sde.be

text:
Yong-Ming Chen

Xing-Ran Qu

Tian-Hao Li

Asim Iqbal

Xingeng Wang

Zhi-Yong Ren

Nicolas Desneux

Lian-Sheng Zang

Xin-Ran Qu

M Traugott

Performances of six eupelmid egg parasitoids from China on Japanese giant silkworm Caligula japonica with different host age regimes

Keywords: Anastatus, Mesocomys, Host age preference, Host suitability, Biological control

ou non, émanant des établissements d'enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

1 3

Introduction

The Japanese giant silkworm (JGS) Caligula japonica Moore (Lepidoptera: Saturniidae) is a defoliator pest of forest and fruit trees in East Asia [START_REF] Qiao | Occurrence reasons and control measures of Caligula japonica in Longnan city of China[END_REF][START_REF] Abarenkov | Life Sciences EUO[END_REF][START_REF] Nashiki | Insect specimens of Komatsu City Museum. Version 1.1[END_REF]. In China, 38 plant species belonging to 30 genera in 20 families have been reported as hosts of this pest, including various important fruit trees such as walnut (Juglans regia L.), chestnut (Castanea mollissima Blume), ginkgo (Ginkgo biloba L.), plums (Prunus spp.), pears (Pyrus spp.), apple (Malus pumila Mill.) and sumac [Toxicodendron vernicifluum (Stokes)] (Yang et al. 2008a;[START_REF] Qiao | Occurrence reasons and control measures of Caligula japonica in Longnan city of China[END_REF]. Since it was first reported in 2006 in Kangxian, Gansu Province (northwestern China), JGS has rapidly spread and emerged as a major pest of walnut trees. About 27,330 hectares of walnut trees were infested by JGS in 2011 in Kangxian alone, causing an estimated economic loss of $20 million [START_REF] Qiao | Occurrence reasons and control measures of Caligula japonica in Longnan city of China[END_REF]. There is a high possibility of further outbreaks of this pest (Yang et al. 2008b;[START_REF] Qiao | Occurrence reasons and control measures of Caligula japonica in Longnan city of China[END_REF]. In other regions in East Asia, JGS was also reported as a serious pest of deciduous forest and shade trees such as plums, chestnuts, camphor (Cinnamomum sp.) and birch (Betula maximowicziana Regel.) in Japan [START_REF] Clausen | The bionomics of Anastatus albitarsis Ashm., parasitic in the eggs of Dictyoploca japonica Moore (Hymen.)[END_REF][START_REF] Kawasaki | The tanning agent in the silk of the Japanese giant silkmoth, Dictyoploca japonica Butler[END_REF][START_REF] Ohno | Variation in shoot mortality within crowns of severely defoliated Betula maximowicziana trees in Hokkaido, northern Japan[END_REF].

Currently, control strategies against JGS rely on the application of broad-spectrum insecticides in China [START_REF] Dong | Toxicity determination and control effect of several pesticides against Dictyoploca japonica Butler[END_REF]. Unfortunately, insecticides are often not applied in a timely manner or applied repeatedly, leading to the development of pesticide resistance in the pest [START_REF] Wang | Pharmacodynamic study on different insecticide for Caligula japonica Moore[END_REF]. Furthermore, pesticide applications could disrupt established IPM for other pests, increase chemical residues, negatively affect pollinators and other beneficial or non-target organisms, and cause harm to the environment and human health [START_REF] Weisenburger | Human health effects of agrichemical use[END_REF][START_REF] Desneux | The sublethal effects of pesticides on beneficial arthropods[END_REF][START_REF] Qu | Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines[END_REF]. Although some entomopathogenic fungi, bacteria and viruses have been tested for the control of this pest, these pathogens yielded unsatisfactory results [START_REF] Tetsu | Electron microscope observations on the maturation process of the Nucleopolyhedrosis 1 3 viruses of the oriental tussock moth, Euproctis subflava Bremer and the Japanese giant silkworm, Dictyoploca japonica Butler[END_REF][START_REF] Liu | Application of Beauveria bassiana (Balsamo) Vuillemin for the control of Dictyoploca japonica Moore[END_REF]. Under this scenario, it is urgently needed to develop effective but also environmentally friendly control strategies for this pest.

Biological control with insect parasitoids to control forest pests has been practiced from a long time [START_REF] Fischbein | Classical biological control of an invasive forest pest: a world perspective of the management of Sirex noctilio using the parasitoid Ibalia leucospoides (Hymenoptera: Ibaliidae)[END_REF]. Among insect natural enemies, egg parasitoids would be ideal agents for the control of insect pests as they kill host pests before the pests cause potential damage to host plants. Indeed, many egg parasitoids such as trichogrammatids have been widely massproduced and released for the control of Lepidopteran pests globally including China [START_REF] Smith | Biological control with Trichogramma: advances, success, and potential of their use[END_REF][START_REF] Mills | Egg parasitoids in biological control and integrated pest management[END_REF][START_REF] Huang | Long-term, large-scale releases of Trichogramma promotes pesticide decrease in maize in Jilin province, Northern China[END_REF][START_REF] Zang | Biological control with Trichogramma in China: history, present status and perspectives[END_REF]. For example, the egg parasitoid Anastatus japonicus Ashmead (Hymenoptera: Eupelmidae) (later identified as A. fulloi Sheng & Wang) has been mass-produced and released annually to control the litchi stink bug Tessaratoma papillosa Stål (Hemiptera: Tessaratomidae) in China since the late 1960s [START_REF] Li | Biological control of insect pests in litchi orchards in China[END_REF]. Recently, the egg parasitoids Trissolcus japonicus Ashmead (Hymenoptera: Scelionidae) and A. bifasciatus Geoffroy are considered as candidate biological control agents for inundative releases against the invasive brown marmorated stink bug Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in North America and Europe [START_REF] Talamas | Trissolcus japonicus (Ashmead) emerges in North America[END_REF]Stahl et al. 2018a, b;[START_REF] Abram | First detection of the samurai wasp, Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae), in Canada[END_REF] [START_REF] Chen | An investigation of Caligula japonica (Lepidoptera: Saturniidae) egg distribution and associated parasitoids on walnut trees (Juglans regia L.) in northwestern China[END_REF]. Parasitism rates of JGS egg masses (individual eggs) ranged from 0.55% (0.01%) to 30.41% (3.59%) in the fields [START_REF] Chen | An investigation of Caligula japonica (Lepidoptera: Saturniidae) egg distribution and associated parasitoids on walnut trees (Juglans regia L.) in northwestern China[END_REF]). Among them, A. fulloi is a widely distributed and well-studied species as a biological control agent of various lepidopteran and pentatomid (Hemiptera) eggs [START_REF] Li | Biological control of insect pests in litchi orchards in China[END_REF]. Mesocomys albitarsis was reported as a major egg parasitoid of JGS in Japan [START_REF] Clausen | The bionomics of Anastatus albitarsis Ashm., parasitic in the eggs of Dictyoploca japonica Moore (Hymen.)[END_REF]. All of them were newly reported on JGS in northwestern China, and A. gansuensis was a newly described species [START_REF] Chen | Anastatus Motschulsky (Hymenoptera, Eupelmidae): egg parasitoids of Caligula japonica Moore (Lepidoptera, Saturniidae) in China[END_REF]. This field survey indicated the potential of these locally occurring egg parasitoids for the biological control of JGS. Indigenous parasitoids have already adapted to local ecological conditions and if they can adapt to newly emerging or invading pests, they may be manipulated to suppress the pests through conservative and augmentative biological control [START_REF] Yuan | Performance of four Chinese Trichogramma species as biocontrol agents of the rice striped stem borer, Chilo suppressalis, under various temperature and humidity regimes[END_REF][START_REF] Fischbein | Modelling the distribution of forest pest natural enemies across invaded areas: towards understanding the influence of climate on parasitoid establishment success[END_REF]. One of such examples is the fall webworm moth Hyphantria cunea Drury (Lepidoptera: Erebidae), an exotic and invasive pest that has been successfully controlled by the indigenous pupal parasitoid Chouioia cunea Yang (Hymenoptera: Eulophidae) in China [START_REF] Yang | Mass rearing and augmentative releases of the native parasitoid Chouioia cunea for biological control of the introduced fall webworm Hyphantria cunea in China[END_REF].

The production of natural enemies for use in biological control programs is often rather expensive, where the attempt to acquire a cost-effective production system is the main objective of many biological control programs [START_REF] Watt | Effect of parasitoid: host ratio and group size on fitness of Spathius galinae (Hymenoptera: Braconidae): implications for mass-rearing[END_REF]. The Chinese oak silkworm Antheraea pernyi Guérin-Méneville (Lepidoptera: Saturniidae) has been considered as an ideal factitious host for the mass production of A. fulloi and Pseudanastatus albitarsis (= M. albitarsis) to control T. papillosa and Dendrolimus punctatus Walker (Lepidoptera: Lasiocampidae), respectively [START_REF] Teng | Bionomics of Pseudanastatus albitarsis Ashmead and its utiuzation for control of Dendrolimus punctatus Walker[END_REF][START_REF] Li | Biological control of insect pests in litchi orchards in China[END_REF], because of its high parasitism rates, low rearing costs, and easy storage and transportation (Li 1 3 et al. 2019;[START_REF] Iqbal | Factitious host species impact on the outcome of multiparasitism between egg parasitoids[END_REF]. However, the suitability of A. pernyi eggs as a rearing host for other egg parasitoids has not yet be evaluated. This study aimed to identify the most suitable agents for biological control of JGS among six recently discovered indigenous eupelmid egg parasitoids: A. fulloi, A. gansuensis, A. japonicus, A. meilingensis, M. albitarsis and M. trabalae using A. pernyi egg as a factitious host. The eulophid A. brevipedicellus was not tested because of its low field parasitism on individual JGS eggs (< 1.1%) or egg masses (< 2.2%) during the field surveys [START_REF] Chen | An investigation of Caligula japonica (Lepidoptera: Saturniidae) egg distribution and associated parasitoids on walnut trees (Juglans regia L.) in northwestern China[END_REF]. Specifically, we comparatively evaluated their relative performances on differently aged JGS eggs in terms of the number of parasitized eggs and offspring fitness. Augmentative or inundative release programs rely on not only selection of parasitoid species that preferentially attack target pests and are well adapted to the agroecosystem of the target pests, but also efficient mass-rearing systems to produce large numbers of high-quality parasitoids [START_REF] Smith | Biological control with Trichogramma: advances, success, and potential of their use[END_REF]. Age-related development changes in host, both physiological and morphological, can result in variable host quality and influence a parasitoid's host acceptance for oviposition and suitability for offspring [START_REF] Nurindah | Influence of rearing hosts on host size acceptance by Trichogramma australicum[END_REF][START_REF] Li | Biological control of insect pests in litchi orchards in China[END_REF]Stahl et al. 2018a;[START_REF] Iqbal | Factitious host species impact on the outcome of multiparasitism between egg parasitoids[END_REF]. This is particularly true for parasitoids attacking static developmental stages such as egg and pupa, as the quantity of resources available for the development of parasitoid progeny is determined at the time of parasitism [START_REF] Vinson | Host selection by insect parasitoids[END_REF][START_REF] Pizzol | Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species[END_REF][START_REF] Zhang | Effects of host-egg ages on host selection and suitability of four Chinese Trichogramma species, egg parasitoids of the rice striped stem borer, Chilo suppressalis[END_REF][START_REF] Hou | Effect of oriental armyworm Mythimna separata egg age on the parasitism and host suitability for five Trichogramma species[END_REF]. Therefore, we also compared the effect of host age on the performances of these parasitoids. This information will help select suitable host age for the rearing or timing of field release of these parasitoids.

Materials and methods

Parasitoids

Laboratory colonies of the six eupelmid egg parasitoids (Anastatus fulloi, A. gansuensis, A. japonicus, A. meilingensis, Mesocomys albitarsis and M. trabalae) were established with adult wasps emerged from field-collected and parasitized JGS egg masses in walnut orchards in 2017 in Kangxian (105-106°E, 32.9-33.7°N), northwestern China. Each species was identified based on the morphological characteristics as described by [START_REF] Gibson | Parasitic wasps of the subfamily Eupelminae: classification and revision of world genera (Hymenoptera: Chalcidoidea: Eupelmidae)[END_REF][START_REF] Gibson | Chapter 2. Morphology and Terminology[END_REF][START_REF] Gibson | The species of Eupelmus (Eupelmus) Dalman and Eupelmus (Episolindelia) Girault (Hymenoptera: Eupelmidae) in North America north of Mexico[END_REF] and [START_REF] Gibson | Revision of the Palaearctic species of Eupelmus (Eupelmus) Dalman (Hymenoptera: Chalcidoidea: Eupelmidae)[END_REF]. All six species were further verified using voucher specimens as identified by Dr. Gibson in 2018. The cytochrome oxidase subunit I gene (COI) sequences of the four Anastatus species were also analyzed according to [START_REF] Hebert | Biological identifications through DNA barcodes[END_REF]. All voucher specimens were deposited in the Institute of Biological Control collection, Jilin Agricultural University at Changchun, China (for additional information of these parasitoids, see Table 1).

Each parasitoid colony was initialed with 30 wasps and maintained on the factitious host A. pernyi eggs under controlled conditions (25 ± 1 °C, 70 ± 5% RH and 14L:10D). Mature A. pernyi moths were dissected to collect host eggs. The eggs were washed with distilled water and then air dried at normal room temperatures [START_REF] Iqbal | Factitious host species impact on the outcome of multiparasitism between egg parasitoids[END_REF]. Fifty eggs were glued on an egg card (5.0 × 1.0 cm) and then exposed to individual females in small glass tubes (10.0 × 1.5 cm) covered with fine mesh for 24 h. Exposed eggs were held until the emergence of wasps. All six eupelmid egg parasitoids had been reared for five generations prior to their use in this study and rejuvenated every three to five generations by transferring them to rear on JGS eggs.

Host insect

JGS is a univoltine species; it lays eggs in the fall and overwinters as eggs in diapause from September to April of the following year in Kangxian, China (Yang et al. 2008b). JGS cocoons were collected in walnut orchards in Kangxian (33° 26′ 33.81″ N, 105° 41′ 52.10″ E) during the middle of June 2019. Approximately, 300 cocoons were collected and placed in a plastic container (25.5 × 25.5 × 5 cm) inside an insect cage (30 × 30 × 30 cm). The cocoons were maintained in an open insectary so that they were exposed to similar field conditions (23-29 °C, 60-85% RH and natural photoperiod) and emerged as field populations did from June 1 3

to September. Newly emerged adults were paired and kept in insect rearing cages (50 × 50 × 50 cm). The adults were monitored daily for oviposition, and newly laid eggs were collected and kept under the same conditions as described above until they reached required ages (see below) for experiments.

Experimental setup

Experiments were conducted under laboratory conditions (25 ± 1 °C, 70 ± 5% RH and 14L:10D). To determine the performance of each of the six egg parasitoids on differentaged JGS eggs, four different ages (0, 10, 20 and 30-d old) of JGS eggs were selected to cover a wide range of aged hosts that could be attacked by these parasitoids in the field.

Because adult JGS females start oviposition in September in Kangxian, China, where monthly field temperatures vary from 8 to 28 °C (mean 15.5 °C) in September and 2 to 21 °C (mean 11.5 °C) in October based on weather data available at https ://www.tianq i.com. Field temperatures drop dramatically after October (≈ 30-d old of early laid JGS eggs) when these parasitoids are likely no longer active in the field [START_REF] Fang | Study on the dynamics of Anastatus albitarsis in the forest[END_REF]. Newly emerged adult wasps (< 6 h old) were collected and held in a group of ten pairs (except for A. gansuensis, which produces by parthenogenesis) in a cylindrical and transparent plastic container (9.0 × 14.0 cm, diameter × height) covered with fine mesh for 3 d to allow mating, with 30% honey solution provided as food for the parasitoids. All tests used 3-d old and mated female wasps. Our preliminary observations found that all the six parasitoids could not parasitize more than 30 eggs per female wasp per 24 h, therefore, female wasps were individually exposed to 50 host eggs of 0, 10, 20 or 30 d-old in a no choice test (i.e., with unlimited access to hosts). The host eggs were glued on a strip-shaped egg card (5.0 × 1.0 cm) and exposed to the parasitoid in a small glass tube (10.0 × 1.5 cm) covered with fine mesh. The test procedures were similar for each parasitoid species at each tested host age.

A replicate was discarded if the wasp was found dead at the end of the 24-h exposure. Following the 24-h exposure, the wasps were removed, and all exposed eggs were checked daily for the emergence of wasps until no wasps emerged for a consecutive of 20 d. Finally, all host eggs without a parasitoid emergence hole were dissected under a stereomicroscope to determine the fate of each egg, i.e., either dead and unparasitized or parasitized with a recognizable dead parasitoid larva, a dead or live parasitoid pupa or a developed but dead adult inside the host egg. Images (examples) were taken for these different scenarios using a Nikon camera and/or Keyence VHX-2000 digital microscope. There were 15 valid replicates for each parasitoid species and host age treatment.

For each treatment replicate, we calculated the number of parasitized eggs (= number of host eggs with a parasitoid emergence hole + number of host eggs containing a parasitoid larva, pupa or adult), percentage of offspring emergence (= number of host eggs with a parasitoid emergence hole × 100/number of parasitized eggs), percentage of female progeny (= number of emerged and unemerged adult females × 100/total number of emerged and unemerged adults) and developmental time (d) of individual wasps from the oviposition to adult emergence. Also, the percentages of offspring died as larvae, undeveloped (dead and diapause) as pupae and dead as adults inside the hosts were calculated by dividing the numbers of dead larvae, undeveloped pupae and dead adults by the total number of parasitized host eggs, respectively.

Data analyses

A two-way analysis of variance (ANOVA) was used to compare the performances of the six egg parasitoids, considering the effects of both parasitoid species (six levels) and host age (four levels), as well as their interaction on the number of parasitized hosts, developmental time, percent offspring emergence, percent female progeny and percentage of offspring dead as larvae, undeveloped as pupae or dead as adults inside the hosts. Prior to the ANOVAs, the percentage data were arcsine square-root-transformed to normalize variances and checked for the normality of residuals and homoscedasticity with Shapiro-Wilk tests. When the ANOVAs revealed significant effects of the factors, means were separated by Tukey's Honestly Significant Difference (HSD) test with an alpha equal to 0.05. All data analyses were performed using the SAS statistical software package (SAS Institute 2010, Cary, NC, USA).

Results

Number of parasitized eggs

All six parasitoids successfully parasitized JGS eggs of four tested ages, but the number of parasitized eggs was affected by parasitoid species, host age and their interaction (Table 2). The numbers of parasitized eggs (averaged from 2.60 to 23.53 eggs) was generally followed (in decreasing order) by A. japonicus, M. albitarsis, M. trabalae, A. fulloi, A. meilingensis and A. gansuensis at each host age (0-d old: F 5,84 = 34.63, P < 0.001; 10-d old: F 5,84 = 22.32, P < 0.001; 20-d old F 5,84 = 61.62, P < 0.001; 30-d old: F 5,84 = 48.87, P < 0.001) (Fig. 1a). All four Anastatus species parasitized more old (30 d, or 20 and 30 d) than younger (0, 10 and 20 d, or 0 and 10 d) eggs (A. fulloi: F 3,56 = 15.62, P < 0.001; A. gansuensis:

1 3 F 3,56 = 13.31, P < 0.001; A. japonicus: F 3,56 = 24.10, P < 0.001; A. meilingensis: F 3,56 = 33.48, P < 0.001) (Fig. 1a). However, M. albitarsis parasitized similar numbers of eggs at various ages, except that it parasitized more 20-d old than 10-d old eggs (F 3,56 = 4.09, P = 0.011), and M. trabalae parasitized more young (0, 10 and 20-d old) than old (30 d) eggs (F 3,56 = 6.28, P = 0.001) (Fig. 1a).

Developmental time

Developmental time from oviposition to adult emergence was also affected by parasitoid species, host age and their interaction (Table 2). It was similar among different host ages for A. fulloi (F 3,56 = 0.94, P = 0.430) and A. gansuensis (F 3,56 = 2.69, P = 0.055), but generally increased with increasing host ages for A. japonicus (F 3,56 = 5.32, P = 0.003), A. meilingensis (F 3,56 = 13.50, P < 0.001), M. albitarsis (F 3,56 = 12.32, P < 0.001) and M. trabalae (F 3,56 = 13.75, P < 0.001) (Table 3). Among parasitoid species, the developmental time was different at each host age (0-d old: F 5,84 = 192.55, P < 0.001; 10-d old: F 5,84 = 49.18, P < 0.001; 20-d old: F 5,84 = 77.35, P < 0.001; 30-d old: F 5,84 = 59.87, P < 0.001). Overall, A. gansuensis developed slowly while M. albitarsis developed fast when compared to other four parasitoid species (Table 3). 1 3

in 10-d old (F 5,84 = 1.64, P = 0.159) eggs among different parasitoid species (Table 3). There was no significant effect of host age, parasitoid species or their interaction on the percentage of unemerged adult wasps (Tables 23). Consequently, offspring emergence was high (> 90%) in all treatments (Fig. 1b). Neither parasitoid species nor host age affected offspring emergence (Table 2). There was, however, an interactive effect between the parasitoid species and host age on the offspring emergence. It was no different for A. fulloi (F 3,56 = 0.19, P = 0.905), A. gansuensis (F 3,56 = 0.75, P = 0.527), A. meilingensis (F 3,56 = 1.23, P = 0.309), M. albitarsis (F 3,56 = 2.41, P = 0.077) or M. trabalae (F 3,56 = 0.91, P = 0.442) among different host ages (Fig. 1b). However, offspring emergence of A. japonicus was lower from the oldest (30-d old) than young (0, 10, or 20-d old) eggs (F 3,56 = 7.03, P = 0.0004) (Fig. 1b), and this was largely due to the diapause of undeveloped pupae.

Offspring sex ratio

Regardless of the host age, all six parasitoids were strongly female biased (> 70% females), except for A. gansuensis which produced 100% female offspring (Fig. 1c). Percentage of female progeny was affected by parasitoid species only (Table 2). It was no different for A. fulloi (F 3,56 = 1.07, P = 0.368), A. gansuensis (F 3,56 = 0.88, P = 0.527), A. japonicus (F 3,56 = 2.14, P = 0.105), A. meilingensis (F 3,56 = 1.38, P = 0.260), or M. trabalae (F 3,56 = 0.13, P = 0.942) among different host ages. However, M. albitarsis produced more female biased progeny from 20-d old than 0 or 10-d-old eggs (F 3,56 = 7.74, P < 0.001). Overall, A. gansuensis, A. japonicus, and M. albitarsis produced more female biased progeny than the other three parasitoid species at all host ages (0-d old: F 5,84 = 6.99, P < 0.001; 10-d old: F 5,84 = 6.57, P < 0.001; 20-d old: F 5,84 = 10.35, P < 0.001; 30-d old: F 5,84 = 14.12, P < 0.001).

Discussion

We compared the relative performances of six indigenous eupelmid egg parasitoids on different-aged JGS eggs, with an effort to identify the best candidate agents for the control of this emerging pest as well as suitable host ages for improving rearing and field release protocols of selected parasitoids. We demonstrated successful parasitism of JGS eggs by all six parasitoids and the suitability of various-aged JGS eggs for these parasitoids.

Eggs (except for diapausing eggs) develop in a short period of time and the quality of a host egg as a resource for an egg parasitoid decreases rapidly as the egg ages. Also, host eggs could become less acceptable due to increased hardness of the eggshell or less detectable due to fading host recognition cues over time [START_REF] Vinson | The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species[END_REF]. Therefore, many egg parasitoids preferentially oviposit in young eggs, and young eggs can be more suitable than old eggs for the development of parasitoid offspring [START_REF] Vinson | The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species[END_REF][START_REF] Zhang | Effects of host-egg ages on host selection and suitability of four Chinese Trichogramma species, egg parasitoids of the rice striped stem borer, Chilo suppressalis[END_REF][START_REF] Hou | Effect of oriental armyworm Mythimna separata egg age on the parasitism and host suitability for five Trichogramma species[END_REF]. For example, Trichogramma ostriniae Pang & Chen, T. japonicum Ashmend, T. dendrolimi Matsumura, and T. chilonis Ishii (all Hymenoptera: Trichogrammatidae) all showed an oviposition preference for young eggs of Chilo suppressalis (Walker) (Lepidoptera: Crambidae) and Mythimna separata (Walker) (Lepidoptera: Noctuidae) [START_REF] Zhang | Effects of host-egg ages on host selection and suitability of four Chinese Trichogramma species, egg parasitoids of the rice striped stem borer, Chilo suppressalis[END_REF][START_REF] Hou | Effect of oriental armyworm Mythimna separata egg age on the parasitism and host suitability for five Trichogramma species[END_REF]. However, in this study, we found (1) the effect JGS egg age on the preference of the six tested egg parasitoids (in terms of the number of parasitized hosts) varied with the species of parasitoid; the four Anastatus species preferred old than young eggs while the two Mesocomys appeared not to show a strong host age preference or preferred less for the oldest eggs; and (2) various-aged eggs seem to be suitable for all six parasitoids, as offspring survival was high (> 90%) and all parasitoids were female-biased at all host ages, although there exist slight variations in these fitness paraments across parasitoid species or host ages.

There may be several reasons why these six parasitoids did not show a strong preference for young JGS eggs and why various-aged eggs were suitable for these parasitoids. First, the JGS eggs used in this study were in diapause. Despite these eggs were differently aged, they likely offered nutrition of similar quality for the development of the parasitoids. Second, JGS egg has a hard surface (Fig. 2), and there must exist variations among the six parasitoid species in their abilities to penetrate the shell of JGS egg. Old JGS eggs could be hard to be penetrated by the Mesocomys, or they may take longer to parasitize the old than young eggs (host handling time); both situations would result in reduced parasitization efficiency on old host eggs. However, this may be not the case for the Anastatus. Instead, it could be an advantage for the Anastatus to accept old rather than young eggs if there is no difference in host handling time among different host eggs and no obvious fitness costs for offspring development in old hosts (as showed here). Because these eggs parasitoids likely overwinter synchronously with their host eggs for several months in the field, old eggs could be more resistant to unpredictable environmental conditions. Similar results were observed in the egg parasitoid Telenomus euproctidis Wilcox (Hymenoptera: Scelionidae), whose offspring had high survival in overwintering eggs of Euproctis pseudoconspersa Strand (Lepidoptera: Erebidae) [START_REF] Ai | A study on natural enemies of Euproctis pseudoconspersa Strand[END_REF]. In general, all six egg parasitoids were still rather flexible in accepting JGS eggs, and this flexibility would allow them to explore a wide range of aged and diapausing JGS eggs. We must point out that it is possible that some individual parasitoids might had died at the egg stage, but they could be unrecognizable in the dead hosts during 1 3 the dissections. Thus, offspring survival could be slightly overestimated. Given the overall low percentages of dead host eggs across all parasitoid species and host age treatments (< 10%), any differences resulting from the overestimation could be negligible.

Relatively, A. gansuensis developed slowly while M. albitarsis developed faster when compared to the other four parasitoid species that had similar developmental times. The developmental time was independent of host age in A. fulloi and A. gansuensis but slightly increased with host age in the other four parasitoids. To maximize their chances of successful parasitism, egg parasitoids often delay host development or speed up progeny development when ovipositing in an older host [START_REF] Vinson | The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species[END_REF]. For example, development of A. bifasciatus was delayed when attacking old eggs of Thaumetopoea solitaria (Freyer) (Lepidoptera: Notodontidae) or H. halys eggs [START_REF] Boyadzhiev | Species of the Genus Ooencyrtus Ashmead, 1900 (Hymenoptera: Encyrtidae), egg parasitoids of Thaumetopoea solitaria (Lepidoptera: Notodontidae) in Bulgaria[END_REF]Stahl et al. 2018b). As discussed above, diapausing JGS eggs may do not undergo significant changes of host quality over time, and for this reason, these parasitoids may be unnecessary to adjust their developmental times. Dead adults of all the six parasitoids were found inside JGS eggs, and this happened apparently because some adult wasps were unable to successfully gnaw a hole out of the eggs. This also occurred in other parasitoids such as T. ostriniae, T. embryophagum Hartig, and T. piceum Dyurich, where adult wasps failed to form an emergence hole for emergence (e.g., [START_REF] Hassan | The oak-silkworm egg Antheraea pernyi (Lepidoptera: Anthelidae) as a mass rearing host for parasitoids of the genus Trichogramma (Hymenoptera: Trichogrammatidae)[END_REF][START_REF] Li | Multiparasitism with Trichogramma dendrolimi on egg of Chinese oak silkworm, Antheraea pernyi, enhances emergence of Trichogramma ostriniae[END_REF]. We suspect that adult wasps of these four species may take longer to emerge from old than young host eggs.

Interestingly, A. gansuensis produced all female offspring on JGS eggs. It could occasionally produce a few male offspring as we recently noticed that this parasitoid had a 113:1 ratio of female to male offspring when reared from A. pernyi eggs (Chen et al. unpubl. data). The parthenogenetic reproduction of A. gansuensis is an advantage if the parasitoid must be mass reared, because it would be cheaper to produce than sexual forms. Most hymenopteran species are haplodiploid, i.e., male (haploid) developed from unfertilized eggs while female (diploid) developed from fertilized eggs [START_REF] Heimpel | Sex determination in the hymenoptera[END_REF]. Female-producing parthenogenesis (thelytoky) can be genetic or due to infections by endosymbiotic bacteria of the genera Cardinium, Wolbachia, and Rickettsia [START_REF] Simon | Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals[END_REF]Rabeling and Kronauer 2013;[START_REF] Monti | No evidence of parthenogenesis-inducing bacteria involved in Thripoctenus javae thelytoky: an unusual finding in Chalcidoidea[END_REF] It is likely that these six egg parasitoids diapause in host eggs when they attack the hosts in later fall. Diapause does occur under a combination of low temperature and short photoperiod in several closely related species such as M. pulchriceps Cameron (Vanden Berg 1971), A. umae Bouček (= A. madagascariensis Risbec) [START_REF] Narasimham | Biology of Anastatus umae (Hymenoptera: Eupelmidae), an oothecal parasite of Neostylopyga rhombifolia[END_REF], and A. bifasciatus (Stahl et al. 2018b). Among the six parasitoid species, A. japonicus was previously reported to enter diapause as pre-pupae in A. pernyi eggs in China [START_REF] Zhao | The study on diapause induction in Anastatus japonicus Ashmead[END_REF] or as mature larvae inside the gypsy moth eggs in Ontario, Canada [START_REF] Sullivan | Low winter temperatures and the potential for establishment of the egg parasite Anastatus disparis (Hymenoptera: Eupelmidae) in Ontario populations of the gypsy moth[END_REF]. The different diapausing stages as reported in the two studies could be due to different adaptions by two different geographical populations to the local environments. However, the tested laboratory conditions in the current study would not favor diapause, still, a small portion of A. japonicus went diapause as pre-pupae. This partial diapause of A. japonicus seems to be induced by the diapausing hosts. This also occurred in other parasitoids. For example, Encarsia scapeata Rivnay entered diapause when it was reared on diapausing host Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) [START_REF] Gerling | Bionomics of Encarsia scapeata Rivnay (Hymenoptera: Aphelinidae), tritrophic relationships and host-induced diapause[END_REF]. Partial diapause could be an adaptive "risk-spreading" strategy for the parasitoid to copy with unpredictable environments [START_REF] Hopper | Risk-spreading and bet-hedging in insect population biology[END_REF].

In conclusion, all the six egg parasitoids have the potential for conservative and augmentative biological control of JGS. Fast development in M. albitarsis, parthenogenetic reproduction in A. gansuensis and partial diapause in A. japonicus all could be important attributes as biological control agents. Overall, A. japonicus, M. albitarsis and M. trabalae are recommended as the best candidate agents. These parasitoids could be mass-reared and released during the fall for the suppression of diapausing JGS eggs. It is also worth of mentioning that these parasitoids can be reared on the factitious host A. pernyi as we showed here that the tested parasitoids reared from A. pernyi eggs effectively parasitized JGS eggs. Antheraea pernyi eggs (104.96 ± 0.57 eggs /g) were about twice larger than JGS eggs (297.62 ± 0.49 eggs /g), and consequently, female parasitoids (e.g., M. trabalae) developed from the A. pernyi eggs (4.657 ± 0.017 um) were about twice larger than those reared from the JGS eggs (2.058 ± 0.015 um) (Chen et al. unpubl. data). In general, the body size of adult parasitoids is often positively correlated with many other fitness components (e.g., [START_REF] Quicke | Parasitic Wasps. Chapman and Hall, London Rabeling C, Kronauer DJ[END_REF][START_REF] Morris | Learning and natal host influence host preference, handling time and sex allocation behaviour in a pupal parasitoid[END_REF][START_REF] Wang | Fitness consequence of body sizedependent host species selection in a generalist ectoparasitoid[END_REF]. However, further detailed studies are needed for a better understanding of the effect of natal host on the parasitoids' demographic parameters (e.g., intrinsic rate of increase) and other fitness attributes. Further studies are also needed to demonstrate the efficiency of these parasitoids against JGS via augmentative release in the field.

Fig. 1

 1 Fig. 1 Effects of host age of C. japonica eggs on the number of parasitized eggs (a), percent emergence (b) and percent female progeny (c) of each of the six eupelmid egg parasitoids. Bars refer to means ± SE. The different lower-case letters above the same patterned bars indicate significant differences among different host ages for each parasitoid species, while the different upper-case letters above the bars indicate significant differences among different parasitoid species at each host age (P < 0.05, Tukey's test)

  . For example, parthenogenetic reproductions in Encarsia formosa Gahan (Hymenoptera: Aphelinidae) (Zchori-Fein et al. 2001), Plagiomerus diaspidis Crawford (Hymenoptera: Encyrtidae) (Zchori-Fein and Perlman 2004) and Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae) (Nugnes et al. 2015) were associated with the infection of Wolbachia, Cardinium, and Rickettsia, respectively. Whether or not the A. gansuensis population was infested by endosymbionts is unknown and this deserves further study.

Fig. 2

 2 Fig. 2 Images of an adult female parasitizing C. japonica egg (a), emerged adults (b), dead larva (c), and alive (in diapause) pre-pupa (d) and pupa (e) of A. japonicus

  ). We surveyed indigenous egg parasitoids associated with JGS in walnut orchards in northwestern China in 2017 and 2018, and collected seven parasitoid species from parasitized JGS eggs, namely Anastatus fulloi Sheng &Wang, A. gansuensis Chen & Zang, A. japonicus, A. meilingensis Sheng & Yu, Mesocomys albitarsis (Ashmead) and M. trabalae Yao, Yang & Zhao (all Hymenoptera: Eupelmidae), and Aprostocetus brevipedicellus Yang and Cao (Hymenoptera: Eulophidae) species

Table 1

 1 Detailed information on six eupelmid egg parasitoid species tested in this study

	Parasitoid species	GenBank acces-	Indigenous host a	Other hosts recorded (references)
		sion number
	A. fulloi	MK604241	Caligula japonica	Erthesina fullo (Sheng et al. 1997)
	A. gansuensis	MK373759	C. japonica
	A. japonicus	MK604240	C. japonica	Antherea pernyi (Zhao et al. 2019)
	A. meilingensis	MK604242	C. japonica	Dendrolimus punctatus, D. kikuchii
				(Sheng and Yu 1998)
	M. albitarsis	-	C. japonica	Dendrolimus spectabilis (Hirose 1964)
	M. trabalae	-	C. japonica	Trabala vishnou (Yao et al. 2009)

a Host species from which the parasitoid was originally collected for this study

[START_REF] Chen | Anastatus Motschulsky (Hymenoptera, Eupelmidae): egg parasitoids of Caligula japonica Moore (Lepidoptera, Saturniidae) in China[END_REF][START_REF] Chen | An investigation of Caligula japonica (Lepidoptera: Saturniidae) egg distribution and associated parasitoids on walnut trees (Juglans regia L.) in northwestern China[END_REF]

Table 2

 2 Results of two-way ANOVAs testing the effects of parasitoid species (PS), host age (HA) of C. japonica egg as well as their interaction on the performances of six eupelmid egg parasitoids in terms of the number of parasitized eggs, offspring emergence, developmental time and percent female progeny and the percentage of offspring dead as larvae, undeveloped as pupae or unemerged (dead) as adults inside the hosts

	Performance parameters	Source Df MS	F	P
	Number of host eggs	PS	5 1696.34 129.14 < 0.001
	parasitized	HA	3	353.68 26.92 < 0.001
		PS × HA 15 156.86 11.94 < 0.001
	Offspring emergence (%) PS	5	169.35		1.21 0.303
		HA	3	102.18		0.73 0.534
		PS × HA 15 273.51		1.96 0.018
	Developmental time (d)	PS	5	323.43 287.60 < 0.001
		HA	3	25.31 22.51 < 0.001
		PS × HA 15	2.57		2.28 0.004
	Female progeny (%)	PS	5 5121.99 31.52 < 0.001
		HA	3	293.36		1.81 0.146
		PS × HA 15 226.96		1.40 0.146
	Dead as larvae (%)	PS	5	66.67		1.02 0.408
		HA	3	18.12		0.28 0.842
		PS × HA 15 127.85		1.95 0.018
	Undeveloped as pupae	PS	5	324.29		7.70 < 0.001
	(%)	HA	3	60.98		1.45 0.229
		PS × HA 15 186.56		4.43 < 0.001
	Dead as unemerged adults	PS	5	10.62		0.51 0.770
	(%)	HA	3	12.34		0.59 0.622
		PS × HA 15	20.57		0.98 0.471

Acknowledgments

We are grateful to Dr. Gary Gibson (Honorary Research Associate, Agriculture and Agri-Food Canada, Canadian National Collection of insects) for the identification of six Eupelmidae species. This research was funded by the National Key R&D Program of China (Nos: 2017YFE0104900 and 2017YFD0201000), and Gansu Provincial Fiscal Science and Technology Award and Compensation Project (2018-01).

Compliance with ethical standards

1 3

Offspring survival and emergence

During the dissections, dead larvae, pupae or adults were found inside the hosts in all parasitoid species, except that all undeveloped A. japonicus were alive (in diapause) and no A. gansuensis and A. meilingensis pupae were dead (Table 3). Overall, percentages of offspring dead as larvae (0.0-9.3%), dead as pupae (0.0-4.7%), diapausing as pupae (1.2-13.1%) or dead as adults (0.0-2.7%) were low in all treatments (Table 3).

The percentage of offspring dead at the larval stage was not affected by parasitoid species and host age but was affected by the interaction of these two factors (Table 2). It was similar for A. fulloi (F 3,56 = 1.56, P = 0.208), A. gansuensis (F 3,56 = 0.87, P = 0.460), A. meilingensis (F 3,56 = 1.31, P = 0.280) and M. trabalae (F 3,56 = 1.75, P = 0.167), but different for A. japonicus (F 3,56 = 3.42, P = 0.023) and M. albitarsis (F 3,56 = 7.72, P < 0.001) among different host ages (Table 3). It was also similar in 0 d (F 5,84 = 1.00, P = 0.423), 10 d (F 5,84 = 1.77, P = 0.127) and 20 d (F 5,84 = 0.77, P = 0.575) old eggs among different parasitoid species (Table 3). However, a higher percentage of M. albitarsis offspring dead as larvae in 30-d old than other aged eggs (F 5,84 = 5.54, P < 0.001) (Table 3).

The percentage of undeveloped pupae was affected by parasitoid species but was not affected by host age or the interaction of these two factors (Table 2). It was similar for A. fulloi (F 3,56 = 1.72, P = 0.174) or M. trabalae (F 3,56 = 1.25, P = 0.300) among different host eggs (Table 3). However, a higher percentage of A. japonicus pupae failed to develop in 30-d old than other aged eggs (F 3,56 = 5.95, P < 0.001), and a lower percentage of M. albitarsis pupae failed to develop in 10-d old than other aged eggs (F 3,56 = 6.72, P < 0.001). The percentage of undeveloped pupae was different in 0-d old (F 5,84 = 2.65, P = 0.029), 20 d-old (F 5,84 = 2.63, P = 0.029) and 30-d old (F 5,84 = 7.31, P < 0.001) eggs, but was similar