All taxa biodiversity inventory of the Bois de Bouis estate (Var, France): a 10-year public-private partnership

Abstract Background This data paper describes the results of a 10-year scientific investigation of a biodiversity-rich private golf estate in south-eastern France in partnership with PatriNat (Office français de la biodiversité/Centre national de la recherche scientifique/Muséum national d'Histoire naturelle, Institut de Recherche pour le Développement). In total, 3,160 species and subspecies, including 1,796 arthropods and 1,049 flora, were inventoried and 65 habitat types were surveyed and mapped. This project is the first All taxa biodiversity inventory (ATBI) in a private property in France with all information available in open data. New information The 20 datasets of fauna, flora, lichens and habitat types from the Bois de Bouis estate are now publicly available. Between 2012 and 2022, more than 22,000 occurrences were recorded, checked and published in the INPN information system. All this information is available in open access in the French portal OpenObs, operated by PatriNat and in the Global Biodiversity Information Facility (GBIF). This data paper provides an overview of the project, its main results and its contribution to the French National Inventory of Natural Heritage (INPN). This data paper presents a list eight species never previously recorded to France; three Hymenoptera: Charitopesleucobasis Townes, 1983 (Ichneumonidae), Dryinustussaci Olmi, 1989 (Dryinidae) and Sparasionmunitus Kozlov & Kononova, 1990 (Sparasionidae) and five Diptera: Clusiodesapicalis (Zetterstedt, 1848) (Clusiidae), Dicraeusvagans (Meigen, 1838) (Chloropidae), Stilponintermedius Raffone, 1994, Stilponsubnubilus Chvala, 1988 and Tachydromiaundulata (Strobl, 1906) (Hybotidae). It also includes a table comparing the project to 18 All-taxa biodiversity inventories in France and Belgium and published for the first time.


Introduction
The Bois de Bouis estate is located in one of the hotspots of biodiversity in the Mediterranean Region (Médail and Quézel 1999), in the heart of the Plaine des Maures and partly integrated into the Plaine des Maures National Nature Reserve. It has a surface of 955 hectares including 829 hectares of semi-natural spaces open to the public and 126 hectares fenced golf course with a hamlet.
In 2007, the owner created a corporate foundation, Fondation d'Entreprise du Golf de Vidauban pour l'Environnement (FEGVE), to take care of the management of the Bois de Bouis estate. In 2011, the FEGVE and PatriNat (Office français de la biodiversité (OFB) Centre national de la recherche scientifique (CNRS)/Muséum national d'Histoire naturelle (MNHN)/Institut de Recherche pour le Développement (IRD)) began a collaboration to characterise the biodiversity of the Bois de Bouis estate and the Vidauban golf course (Delzons and Rault 2013a. In the context of biodiversity erosion (Cowie et al. 2022), this kind of partnership is all the more important because it improves general knowledge of biodiversity, informs owners and stakeholders of the ecological processes at stake and provides relevant technical and scientific support for management and decision-making.
The site's responsibility in terms of nature conservation is major for various reasons. The estate is included in different protected areas, such as Natura 2000 (Site of Community Importance n°FR9301622 and Special Protection Areas n°FR9310110) and a National Nature Reserve (n°FR3600171) and in four areas of ecological importance, 'natural zone of ecological, faunistic or floristic value' (Zone Naturelle d'Intérêt Écologique, Faunistique et Floristique -ZNIEFF) which is in France a natural area, regionally known for its remarkable ecological characteristics (type 1 n°930020473, type 2 n°930012553, type 2 n°930012516 and type 2 n°930020307, see Lepareur et al. (2022)) (See Fig.1). The estate also hosts habitats and species of community interest (e.g. siliceous slabs, temporary Mediterranean ponds, Serapia grasslands, Isoetes velata and I. durieii) and IUCN Red List threatened species, such as the ocellated lizard (Timon lepidus (Daudin, 1802)) and the Hermann's tortoise (Testudo hermanni Gmelin, 1789). For the latter, the Plaine des Maures population is of European importance (Couturier et al. 2014). The discovery of a population of endemic land snail Urticicola suberinus (Bérenguier, 1882) in 2016 was a contribution to the site ecological importance (Léonard et al. 2016).
The objective of the partnership between PatriNat and the foundation was to tend towards a comprehensive inventory of the natural heritage to improve the management of both natural and golf areas. A biodiversity management plan was drawn up in 2016 for the estate as a continuation of the nature reserve management plan ).  Map of the Bois de Bouis estate and its environment. Map describing the ecological environment (biodiversity area) in which the Bois de Bouis estate and the golf course are integrated. ZNIEFF type 1 and 2: Natural zone of ecological, faunistic and floristic interest.

General description
Purpose: One of the objectives of the programme is to make the information available to a wide public and to ensure it is always accessible and evolving. Experience from other AFTBIs shows that data management is often underestimated and information loss is a common issue (Langdon et al. 2006, Deharveng et al. 2015, Ichter et al. 2022. Although the quality of the information was an important issue since the beginning of the project, the partners identified the need to allow extra resources for data quality and dissemination. All data and metadata are now structured according to the standards of the national information system for biodiversity (SINP) and the Global Biodiversity Information Facility (GBIF).
Additional information: Before the publication of the datasets, we performed a quantitative and qualitative assessment of all data (see Quality control), an update of metadata and harmonisation of the information and we invited experts to pass on new species identification and relevant information.
The long-term preservation of data is guaranteed both technically and scientifically by PatriNat (OFB/MNHN/CNRS/IRD). According to the French Environmental Code, the MNHN is responsible for the scientific implementation of the national biodiversity inventory (INPN) and the OFB for its technical organisation.

Project description
Personnel: About 92 people actively participated in the project, mostly field biologists, but also taxonomists in their laboratories in France and abroad (see Acknowledgements). As part of the partnership, a full-time project manager was recruited by the MNHN to coordinate the various studies and the fieldwork, exchange with the stakeholders including the partners, manage the data and write the scientific and technical reports. A professional entomologist was tasked with sorting the material from continuous sampling methods (i.e. entomological traps) and sending specimens to the specialists. The preparation of the data paper was an opportunity for a qualitative and quantitive update of the different datasets involving staff from PatriNat and an independent consultant.

Study area description:
The Bois de Bouis estate is located in south-eastern France in a natural region called the Plaine des Maures (WGS84 decimal coordinates 43.3840, 6.4700) (see Fig. 1). Since 2009, the perimeter of the Plaine des Maures National Nature Reserve also includes part of the estate (460 hectares).
The Plaine des Maures is a sandstone depression of 13,000 hectares separating the crystalline Provence to the south from the limestone Provence to the north. The landscape is dominated by a vast mosaic of sclerophyllous shrublands, forests of stone pine (Pinus pinea L., 1753), cork oak (Quercus suber L., 1753) and evergreen oak (Quercus ilex L., 1753) and rocky outcrops in the continuity of the massif des Maures mountain range. The north-western part is mostly covered by agricultural land (mostly viticulture) and urban areas with significant road and rail networks. This alluvial plain is also characterised by a rich, yet seasonal, hydrographic network due to siliceous and impermeable soils, semi-arid climate, low topography and strong winds. The area is subjected to high wildfire frequency (Couturier et al. 2014).
The Bois de Bouis estate is composed of different types of natural, semi-natural and artificial habitats (see Fig. 2 and Chapter habitat type mapping).
Amongst the 126 hectares of golf course, 30 hectares are dedicated to playing areas. The tees (starting point), fairways and greens (with the hole marked with a flag) make up the  real areas for playing golf. These are grassy areas, often monospecific and generally unfavourable to biodiversity. The turf is mowed at different heights depending on the areas of the course: the greens require daily maintenance while the roughs can be much less maintained. Of these 30 hectares, around 6 hectares of high-roughs have been converted to grassland since 2017. The golf course is made up of 18 holes. The other areas of the golf course correspond to a hamlet, a storage and maintenance area and semi-natural habitats.
Design description: For well-known groups, the objective of the project was to achieve a comprehensive survey. Amphibians, birds, butterflies, dragonflies (Barbarin 2008), orthopters, reptiles, vascular flora (Michaud and Offerhaus 2016) and habitats were intensively sampled in the Bois de Bouis estate throughout the 10 years of the project using state-of-the-art methods (see Sampling methods).
The second target of the project was less-known taxonomical groups where one or several experts were available for the fieldwork at optimal observation dates: algae (Couté and  (Hervé 2012, Hervé 2014, Bosmans and Hervé 2015 and lepidoptera (Bachelard 2008, Bachelard 2009). For those groups, the objective was not a complete survey, but a reliable overview of the communities, based on surveyor's experience.
For flying insects, interception traps (see Sampling methods) were set up. They allowed us to complete the fieldwork for some groups (e.g. coleoptera and lepidoptera) and provide material for taxonomists who did not take part in the inventories (e.g. diptera and hymenoptera) (Daugeron 2014, , Rousse 2016, Whiters 2016, Tillier 2019, Quindroit 2020. A combination of standardised (i.e. trapping campaign) and opportunistic surveys is considered one of the most efficient methods to assess flying insect diversity (Deharveng et al. 2015).
An ecological assessment method, the Ecological Quality Index, was also used. As shown by the dataset, seven studies were performed from 2012 to 2021 on different parts of the Bois de Bouis to gather information for management and decision-making (Delzons and Rault 2013a, Delzons and Rault 2013b, Rault and Delzons 2014. The protocol is a transect survey of reptiles, butterflies, birds, amphibians, dragonflies, vascular flora and natural habitats across the natural habitats of the site. One study involved 6 days of fieldwork over four campaigns (including two dawns and one evening) from early spring to late summer in a year. The transect survey is adapted to cover the different habitats of the study site and is repeated on each visit (different from one site to another). This method is designed to allow reproducibility for future assessments (Delzons et al. 2013). It is a semi-standardised protocol because some aspects are standardised and others are adapted according to the context (more details: https://iqe-patrinat.mnhn.fr and https://iqe-patrinat.mnhn.fr/wp-content/uploads/sites/12/ 2022/06/PATRINAT_ZOOM_IQE_ENG.pdf).

Funding:
The project was funded by the Fondation d'Entreprise du Golf de Vidauban pour l'Environnement (FEGVE). This corporate foundation was created in 2007 to better understand and protect the biodiversity of the Bois de Bouis estate and, more generally, to contribute to the sustainable development of the Plaine des Maures and the Massif des Maures through nature conservation actions, the production of scientific knowledge and environmental education.

Sampling methods
Sampling description: Sampling methods and techniques are varied and depend on the target and the type of habitat (Fig. 3). The most frequent techniques for collecting biodiversity data involves visual and auditive contact (e.g. 10 birds count or Orthoptera inventories using transects (Lacoeuilhe et al. 2020)).
The invertebrates provide the most diverse sampling techniques: entomological net, light traps, sieving of litter, mowing of vegetation, the beating of trees and passive interception traps. Two malaise tents were placed between 28 April and 30 June 2014 and from 08 April to 20 July 2015. The first trap was set in an open area on the golf course and the second in undergrowth in the eastern part of the Bois de Bouis estate. Samples were preserved in alcohol to facilitate their management and their sending to specialists. Some specimens were identified by DNA barcoding. Around 28,000 specimens were collected and sorted.
The sampling methods are included in the datasets' metada using the national protocols and methods repository CAMPANULE (Ichter et al. 2014b).
Quality control: The ATBI Bois de Bouis database is managed by PatriNat in the framework of the National Inventory of Natural Heritage (INPN). This information system guarantees the traceability of data and authorship and normalised standards of data and metadata.
A high level of data quality was expected at all stages of the programme, especially in terms of accuracy and precision (Chapman 2005). The species have been directly identified by experts or the data have been checked by experts, which guarantees a good level of reliability of the identifications.
Before data publication, two types of controls were performed. The first category of control is compliance with SINP standard formats. The data must be compliant with both physical and conceptual aspects: mandatory fields, required formats, repositories (including geographical and taxonomical, see Taxonomic coverage), classifications and lists of values. The second category of control is consistency to ensure logical compatibility within the data, the metadata and between the data and the metadata. For instance, the observation start date must be less than or equal to the observation end date.

Geographic coverage
Description: The Bois de Bouis estate is located in the commune of Vidauban (Post Code: 83350) in the Var Department in the Provence-Alpes-Côte d'Azur Region. The estate covers 955 hectares to the northeast of the Plaine des Maures. Most of the estate is a lowland, but the eastern part includes the foothills of the massif des Maures. Elevation ranges from 39 m to 320 m a.s.l.

Taxonomic coverage
Description: The objective of the inventory is to have a comprehensive survey of the wellknown biological groups (plants, birds, mammals, amphibians, reptiles, butterflies, dragonflies and Orthoptera) and at least a preliminary inventory of less-known groups such as Aranea (spiders and pseudoscorpions), myriapods, lichens, snails, nematods and insects (i.e Blattodea, Coleoptera, Collembola, Diptera, Hemiptera, Heteroptera, Hymenoptera, Thysanoptera).
Insects represent the largest group in terms of species number (1537 species  Taxonomic coverage of the inventory: number of species and subspecies per group. All taxa biodiversity inventory of the Bois de Bouis estate (Var, France): ...

The scientific names follow taxonomy according to TAXREF v15 (Gargominy et al. 2021).
TAXREF is the national repository for flora, fauna and fungi of metropolitan France and Overseas Territories operated and managed by the Muséum national d'Histoire naturelle. Based on the most recent publications and a community of taxonomists, TAXREF assigns a unique, unambiguous and (whenever possible) consensual scientific name to all species occurring in France. The repository is constantly updated and a new version is published every year. The Bois de Bouis ATBI contributed to TAXREF with eight species not known to France prior to the inventories.   datasetID An identifier for the set of data. May be a global unique identifier or an identifier specific to a collection or institution. kingdom The full scientific name of the kingdom in which the taxon is classified.

class
The full scientific name of the class in which the taxon is classified. order The full scientific name of the order in which the taxon is classified. scientificName The full scientific name, with authorship and date information, if known. taxonRank The name of the taxonomic rank for which the taxon rank value is provided. geodeticDatum The ellipsoid, geodetic datum or spatial reference system (SRS) upon which the geographic coordinates given in decimalLatitude and decimalLongitude are based.
eventID An identifier for the set of information associated with an Event (something that occurs at a place and time). May be a global unique identifier or an identifier specific to the dataset. maximumElevationInMetres The upper limit of the range of elevation (altitude, usually above sea level), in metres. minimumElevationInMetres The lower limit of the range of elevation (altitude, usually above sea level), in metres. locality The specific description of the place.

municipality
The full, unabbreviated name of the next smaller administrative region than county (city, municipality etc.) in which the Location occurs. Do not use this term for a nearby named place that does not contain the actual location. country The name of the country or major administrative unit in which the Location occurs.
countryCode The standard code for the country in which the Location occurs.
taxonID An identifier for the nomenclatural (not taxonomic) details of a scientific name. originalNameUsage The taxon name, with authorship and date information, if known, as it originally appeared when first established under the rules of the associated nomenclaturalCode. nameAccordingTo The reference to the source in which the specific taxon concept circumscription is defined or implied -traditionally signified by the Latin "sensu" or "sec." (from secundum, meaning "according to"). For taxa that result from identifications, a reference to the keys, monographs, experts and other sources should be given. dataGeneralisations Actions taken to make the shared data less specific or complete than in its original form. Suggests that alternative data of higher quality may be available on request.
identificationVerificationStatus A categorical indicator of the extent to which the taxonomic identification has been verified to be correct. family The full scientific name of the family in which the taxon is classified.
maximumDepthInMetres The greater depth of a range of depth below the local surface, in metres (note: empty in this dataset).

minimumDepthInMetres
The lesser depth of a range of depth below the local surface, in metres (note: empty in this dataset).
locationRemarks Comments or notes about the Location (note: empty in this dataset).

InformationWithheld
Additional information that exists, but that has not been shared in the given record  Data set name: Inventaire général de la biodiversité (IGB/ATBI) Domaine Bois deBouis -Données mollusques continentaux/All Taxa Biodiversity Inventory (ATBI) ofBois de Bouis estate -Continental mollusc data. abondance_habitat Relative abundance of the habitat in relation to the geographical unit. Used to enter a relative cover, when an exact cover cannot be estimated.
commentaire Free field for any additional indicative information on the observed habitat.
identite_determinateur Identity (surname, first name) of the person(s) who carried out the habitat determination.
organisme_determinateur The organisation to which the person(s) who carried out the habitat determination is/are attached.

Additional information Key outcomes of the inventories
Thanks to the project, 3,160 species and subspecies are now known from the Bois de Bouis estate. In total, 22,654 data sources were recorded, checked and published in the INPN information system. All this information is now available in open access in the GBIF web site (see Data resources) and in the INPN via the OpenObs portal.
The inventories added 77 species and one subspecies for which no occurrences were previously recorded in the national inventory (INPN). At regional level, the project published 206 species and six subspecies for which no occurrences were previously recorded in the The specimens collected, sorted and sent to specialists helped to improve investigation on taxonomical issues, for example on Empidoidae flies (Daugeron, in prep.) and Ichneumonidae wasps with possible new species for science. Molecular analyses (DNA barcoding) confirm an unexpected diversity in various Aculeata families (Schmid-Egger and Schmidt 2021) and parasitoid wasps of the genus Brachygaster Leach, 1815 (Evaniidae). One specimen of Pseudoscorpions (Arachnida) discovered in the estate is also potential new species for science.

The Bois de Bouis' insect diversity compared to other arthropods inventories in France and Belgium
During the last 20 years, several comprehensive arthropod surveys, or ATBIs, have been realised in France and Belgium (Livory and Stallegger 2007, Stallegger and Chéreau 2008, Herbrecht 2013, Stallegger 2014, Darinot, F (coord.) 2014, Herbrecht et al. 2015, Ichter et al. 2018, Forêt et al. 2022, Grootaert and Drumont 2022, Ichter et al. 2022. We present here for the first time, a summary of the most relevant initiatives with species richness for each order (see Fig. 7 in png format or download as xls sheet in Suppl. material 1). Due to a great variety of areas, climates and ecosystems, the results of the different inventories cannot be directly compared. Apart from natural factors, the success, in particular species richness, of an arthropod survey also depends on the time invested and the diversity of sampling methods and specialists.
To illustrate the complex task of an exhaustive inventory, we can cite the Lac de Remoray National Reserve in the region Bourgogne-Franche-Comté, one of the best studied sites in France. As an example, Diptera diversity (1,926 species) represents 48% of the total number of insects inventoried in the Reserve while representing 20% of insect diversity in France. On the other hand, the Hymenoptera surveyed in the Reserve represents 13% (508 species) of Remoray's insect diversity against 20% at the national level. Experts consider that at least 1900 species of Hymenoptera can be expected on this site.
The Bois de Bouis estate, with 2458 species (including morphospecies), is the seventh most important inventory in terms of arthropod diversity in spite of much lower sampling intensity. Most of the specimens of Coleoptera, Diptera and Hymenoptera were collected The results on species richness are noteworthy considering a much lower sampling intensity and duration than other inventories (e.g. Mercantour National Park, Massane National Reserve, Bois de Païolive). Several insect orders like Coleoptera and, in particular, Hymenoptera are very diverse. Others like Diptera are not reflecting the actual diversity mainly due to the lack of specialists to study them.

Can we call it an All taxa biodiversity inventory ?
The concept of an All Taxa Biodiversity Inventory was invented by the American ecologist, Daniel Janzen, for a project in Costa Rica and implemented for the first time in the Great Smoky Mountains National Park in the USA (Janzen and Hallwachs 1994, Mauz 2011). It can be defined as a comprehensive survey of the species living in a natural (or seminatural) area, including data on their environment, their abundance, behaviour and genetic diversity (Deharveng et al. 2015, Ichter et al. 2022. In 2017, the MNHN and the Mercantour National Park reviewed the major ATBIs worldwide, with particular emphasis on the initiatives in France. The final report coauthored by 12 experts proposed the following criteria to define an ATBI (Ichter et al. 2018 ): • the diversity of taxonomic groups inventoried. An ATBI aims to study as many taxonomic groups as possible (including so-called "cryptic" biological compartments, such as arthropods, non-vascular flora and fungi); • coordinated project management and sharing of knowledge. An ATBI implies coordination of the inventories (either centralised or distributed amongst the participants), data and specimens management and the dissemination of results; • improving scientific knowledge. An ATBI aims to advance knowledge of taxonomy, biogeography and ecology. This implies significant sampling pressure and the collection of information on the spatial and temporal distribution of species, their habitats and, where applicable, their abundance and life history traits; • a geographically coherent territory.
We argue that the work carried out on the Bois de Bouis estate responds to the abovementioned criteria and can be considered an All taxa biodiversity inventory. The main arguments are: 1) significant sampling efforts over a large period (most groups have been sampled at least twice), 2) a wide variety of taxonomic groups (including cryptic groups such as Algae, Lichens, Nematodes, Aranea or Hymenoptera), 3) a high level of data quality and dissemination and 4) significant scientific results , Kehlmaier et al. 2019, Tillier 2019.
However, the biodiversity inventory is far from being comprehensive, especially for lesserknown groups like Flies, Worms or Moths. Most Fungi (except Lichens) were not surveyed during the project. In 2009, a first study on the habitats of the Bois de Bouis estate was carried out (Baret 2009). The whole site has been mapped at a scale of 1:5000 (Savio 2015). At this scale, the main issue was mapping habitat mosaics, when two or more vegetation types are found in close proximity, each occupying small areas. These repeating patterns can be explained by vegetation dynamics (communities substitute for each other over time) or by topographical factors due to micromorphology (Ichter et al. 2014a). Habitat mosaics represent more than half of the site (435 hectares).  Last update (2021) of the Vidauban golf course habitat mapping at a scale of 1:5000 using EUNIS habitat typology.

Conclusion
The Bois de Bouis estate inventory is one of a kind for several reasons. First the duration; it is not common to conduct and finance a 10-year survey on private land. Secondly, the scope of the inventories; biodiversity assessments are usually limited to a small number of well-known groups. Finally, the scientific outreach; the specimens collected and barcoded will allow taxonomic advances on poorly-known groups (e.g. Ichneumonidae) and more generally for taxonomic revisions whose scope goes beyond the initial objectives of the inventory and the perimeter of the Plaine des Maures. a b Figure 9.
Bois de Bouis estate habitat mapping at a scale of 1:5000 using EUNIS habitat typology. Our thanks also go to Marie-Claude Serra, Director and Dominique Guicheteau, Scientific Director of the Plaine des Maures Nature Reserve for their support and collaboration, particularly in the study of bats.