Structure and floristic composition associated with an endangered species Beta patula Aiton (Amaranthaceae) in the Islands of Madeira Archipelago

Abstract Background Twenty-two native Crop Wild Relatives (CWR) occur in specific dry environments of Madeira Archipelago, like Desembarcadouro islet in Ponta de São Lourenço and Chão islet in Desertas Islands. Nine of them share the same gene pool with crop species included in Annex I of the International Treaty on Plant Genetic Resources for Food and Agriculture. Amongst them, Beta patula Aiton, an IUCN Critically Endangered species, has been studied in detail for in situ and ex situ conservation. The present paper summarises the information recorded during the Beta patula population assessment. Valuable information on plant communities associated with this species was obtained. New information The data provides information of a vegetation census spanning 7 years, from 2014 to 2020, in two uninhabited islets where Beta patula occurs, Desembarcadouro and Chão islets. The collected dataset consists of 1,786 vegetation descriptions, where 31 species were recorded. All generated data have been published and will be used towards the implementation of conservation actions and to establish a middle term management protocol for Beta patula and other CWR in situ conservation in the framework of a genetic reserve. This work is part of a EU LIFE Project, LIFE RECOVER NATURA and was conducted by members of the ISOPlexis Center, University of Madeira.


Introduction
Beta patula has been classified as a Critically Endangered species by the International Union for Conservation of Nature (IUCN) in the Red List of Threatened Species (Pinheiro de Carvalho and Frese 2011), with an extent of occurrence of only 1.0 km² and its area of occupancy less than 0.80 km². In nature, the species is endemic to the Madeira Archipelago (Fig. 1a), more specifically occurring only in the Desembarcadouro and Chão islets. The Madeira Archipelago is part of the Macaronesia Region (Fig. 1b), a biogeographic area composed of four archipelagos in the North Atlantic Ocean (Azores, Canary Islands, Cape Verde and Madeira). From a geological point of view, all Macaronesian archipelagos are the consequences of mountain-forming and volcanic forces that occurred 60-70 million years ago (Fernández-Palacios et al. 2011). The contrasting landscapes and mild climate have created an ideal environment for a particularly rich biodiversity. The list of sites of community importance for the Macaronesian biogeographical region included in the Natura 2000 network, was the first to be adopted in December of 2001 and is updated every year. It contains 208 sites of community importance, covering over 5000 km² of land and sea. The list of sites of community importance for the Macaronesian biogeographical region can be found at: http://ec. europa.eu/environment/nature/natura2000/biogeog_regions/macaronesian/index_en.htm.
Amongst these sites are the Chão islet, included in the Desertas Islands (Natura 2000 site PTDES0001) and the Desembarcadouro islet, part of the Ponta de São Lourenço Peninsula (Natura 2000 site PTMAD0003). The habitat type classification of Desembarcadouro islet and Desertas Islands belongs to: a) vegetated sea cliffs with endemic flora from Macaronesian coast (EUNIS code 1250) and b) thermo-Mediterranean and pre-desert shrub (EUNIS code 5330) (EUNIS, European Nature Information System) (source: http://eunis.eea.europa.eu/sites/PTMAD0003; https://eunis.eea.europa.eu/sites/ PTDES0001). Both ecosystems are of extreme importance, according to the Habitats Directive (Fig. 2). These areas harbour a wide variety of endemic and native plant species, some of them being crop wild relatives of relevant crops. More specifically, Beta patula is a crop wild relative of fodder, root and sugar beet crops. These species are included in Annex I of the International Threat for Genetic Resources for Food and Agriculture, for being important plant resources, ensuring world food security. Beet CWR have contributed to the breeding of sugar beet varieties, adding genes for resistance to biotic and abiotic stresses (Luterbacher et al. 2004;Panella et al. 2012;Capistrano-Gossmann et al. 2016). The source of these genes was obtained from accessions of CWR populations (Hajjar and Hodgkin 2007;Capistrano-Gossmann et al. 2016) showing their importance for in situ and ex situ conservation. In a recent work, Monteiro et al. 2018) pointed out the introgression of traits from CWR for decreasing biotic stresses constraints in sugar beets, namely using Beta and Patellifolia species, both having disease-resistant characteristics. Although Beta patula occurs in protected islets, it is threatened by introduced animals, particularly by rabbits and seagull populations, possibly causing a severe fragmentation of the population and a continuous decline in the extent and quality of its habitat. Therefore, there was a need for the development and implementation of a species action plan and a special site management plan . Consequently, B. patula was one of the target species of AEGRO project (An Integrated European In Situ Management Work Plan: Implementing Genetic Reserves and On Farm Concepts -AGRI GENRES 057), whereupon the ISOPlexis team started, in 2008, the study to establish B. patula distribution, population baseline and to set up appropriate strategies for this CWR conservation. The project also included the monitoring of ecogeographic conditions (habitat description; altitudinal gradient; soil type and edaphic conditions, climatic parameters) that can limit the species distribution or be a factor of plant diversity differentiation. The plant population survey aims to set up its boundaries and estimate the patches of plant coverage and population sizes. Since then, a continuing effort has been made to validate B. patula a b c d Figure 2.
General aspects of the studied habitats. The Chão islet has a flat plateau format arising from the sea (a and b); Desembarcadouro islet has an irregular terrain and a strong influence from North trade winds in its habitat. conservation in situ and ex situ by the storage of accessions (ISOP 2512 andISOP 1911) in the ISOPlexis Gene Bank, at the University of Madeira and to validate population sizes and dynamics. These studies include a complete floristic analysis at the selected occurrence locations of B. patula in Desembarcadouro islet (DI) and Chão islet (CI). This work was financed by LIFE RECOVER NATURA -LIFE12 NAT / PT / 000195 coordinated by the Madeira Forestry and Nature Conservation Institute IP-RAM (IFCN IP-RAM). The results of a monitoring system to control the conservation status of Beta patula were published in Nóbrega et al. 2020.
This work condenses the results of a 7 year floristic study of all species associated with B. patula. The floristics analysis is still ongoing and it will continue, thus contributing to the permanent monitoring that aims to determine any signs of change in the diversity of these sites, due to climate change, animal pressure or any other interference in habitat that may affect diversity and long-term conservation of the endangered B. patula and other important endemisms in its distribution areas.

General description
Purpose: The LIFE RECOVER NATURA -Beta patula population assessment consisted in the use of previous information obtained during AEGRO project to monitor the populations dynamics and validate the established species baseline with the ultimate goal of implementing a genetic reserve and its management plan. With this work, it was also possible to make a vegetation classification, species trend analysis, distribution maps of plant communities and Natura 2000 habitat types for the occurrence areas of Beta patula (Suppl. material 1).

Sampling methods
Sampling description: To collect the floristic data, 15 areas were selected, taking into consideration that these areas are within the Beta patula distribution range and have a good resolution for herbaceous and small bush plants, being that the floristic composition falls in such criteria (Fig. 3), 12 in the Desembarcadouro islet (DI01; DI02; DI03…DI12) and three in the Chão islet (CI01; CI02 and CI03). These areas are quadrats with 16 m (4 x 4 m) facing North (so replicability could be ensured for each successive sampling) displayed along three parallel transects defined in Desembarcadouro. Inside each quadrat, a full counting and identification of all individuals was carried out in four randomly-selected square metres, using the Research Randomizer Generated Numbers software (Urbaniak and Plous 2013). Sampling effort was dependent on plant density. Plant identification was done according to Pires and Fontinha (2008), Aguiar et al. (2004) and Press and Short (1994). The assigned names of all taxa cited in this work follow the nomenclature given by the Plant List (http://www.theplantlist.org/). Soil types in the Desembarcadouro islet are according to Pinto et al. (1992). No information on the soil types in Chão islet exists in literature.
2 Figure 3. The 16 m plots were set up at a minimum distance from each other of approximately 50 m. Final specimen counts represent the average results of two separate counts per site. If both counts were significantly different, a re-count was made. Each sampling plot was also marked with a coloured steel rod and geographic coordinates were taken with the help of a Global Positioning System (GPS) to facilitate the identification and retrieval of the plots for future monitoring. The target species B. patula and other beet CWR were particularly marked, as well as the Madeiran and Macaronesian endemisms. The species occurrence, floristic composition and structure were studied. The floristic composition of DI and CI sites are similar, due to geographic proximity and similar climate and soil conditions. Plant species were grouped in 13 families. Thirty-one distinct plant species were recorded during the study; 25 species were found in DI and 12 in CI. Five of these species, excluding the target species, B. patula, were common to both sites and recorded in occupancy areas, namely Mesembryanthemum crystallinum L., Mesembryanthemum nodiflorum L., Suaeda vera Forssk. ex J.F. Gmel, Spergula fallax (Lowe) E.H.L. Krause and Crepis divaricata (Lowe) F.W. Schultz. The species were also classified as introduced or probably introduced (three taxa) and native or probably native (19 taxa). Amongst the endemic species, nine taxa were present. Of those, five taxa are endemic to Madeira Islands and four taxa are endemic to the Macaronesia Region (Suppl. material 1). Fig. 4 shows the summary number of species occurrence in the 15 sampling sites and its annual variation, in the time period between 2014 and 2020. The graph shows that 2017 was the year with the highest number of species accounted, followed very closely by the year 2018.
The tree map analyses the floristic composition and structure of the habitats where Beta patula occurs. Fig. 5 shows the relative species frequence occurring in Desembarcadouro and Chão islets. The frequency and dominance were established, based on total account of specimens. The Mesembryanthemum crystallinum is the most predominant species in both islets, while Beta patula is the third most common.

Geographic coverage
Description: The general coverage area comprises two islets that are part of the Madeira Archipelago, Portugal. The Desembarcadouro islet is located on the eastern peninsula of Madeira Island (Ponta de São Lourenço) and the Chão islet is one of the three islets that compose the Desertas Islands.

Taxonomic coverage
Description: The floristic composition of Desembarcadouro islet (DI) and Chão islet (CI) both Macaronesian sites, have similarities, due to their geographic proximity and similarity of soil composition and climate conditions. The flora composition of Desembarcadouro islet is part of the Mayteno umbellatae-Oleion maderensis Vegetation Series Complex (Aguiar et al. 2004, Costa et al. 2012.) It is characterised as a dry infra-mediterranean series, exclusive of southern rocky cliffs, restricted to 0-200 m above sea level. On the sampling a b c d Figure 7.
Endemic species of Madeira Archipelago found in Desembarcadouro and Chão islets. The name of the continent in which the location occurs. country The name of the country in which the location occurs. countryCode The ISO 3166-1-alpha-2 country code.
islandGroup The name of the island group in which the location occurs. island The name of the island in which the location occurs.
stateProvince The first-level administrative subdivision of the country in which the observation occurred.

municipality
The name of the municipality in which the location occurs. locality The name of the locality in which the location occurs.
decimalLatitude The geographic latitude in decimal degrees of the geographic centre of a location.
decimalLongitude The geographic longitude in decimal degrees of the geographic centre of a location.
geodeticDatum The ellipsoid, geodetic datum or spatial reference system (SRS) upon which the geographic coordinates given in decimalLatitude and decimalLongitude are based.