First records of Opuntia monacantha (Willd.) Haw. and Opuntia tomentosa Salm-Dyck (Cactaceae) from Algeria

We report here the first occurrences of two alien cacti species from Algeria. During field surveys from 2016 to 2022 in the Skikda region (north-eastern Algeria), ten populations of Opuntia monacantha (Willd.) Haw. were recorded. This species is reported here as naturalized alien species for the first time for Algeria and the second time for mainland North Africa. The same surveys also yielded three localities of Opuntia tomentosa Salm-Dyck, reported here as casual species for the first time for Algeria and mainland North Africa. Both species colonize various habitats (coastal dune, maquis, cliffs, roofs, gutters, tree trunks) and they propagate by stem fragments. However, O. tomentosa also reproduces from seeds, and birds seem to play a role in the dispersal of this species. We discuss the potential of both species for further spread in Algeria, and argue that increased botanical surveys may lead to the recording of further alien cacti species.


Introduction
Since the discovery of the Americas, hundreds of Cactaceae species have been introduced to (semi-)arid regions all over the world. The family is divided into four subfamilies, of which the Opuntioideae can be easily recognized by their flattened, broadened stem segments (cladodes), specialized glochidia and arillate seeds (Simpson 2010). The Opuntioideae has particularly attracted the attention of scientists because it contains several species that are useful for humans (e.g. providing food for humans and fodder for farm animals). The genus Opuntia with approximately 300 species is the most important one for human use given the many possibilities of exploitation (Rodriguez-Lopez et al. 2020). However, several species of this genus are also notorious in terms of their high invasive potential (Novoa et al. 2015) and their often substantial negative impacts on the environment.
In Algeria, several species of Opuntia were introduced, particularly during the colonial period, mainly as ornamental plants or fodder (Chevalier 1947). Opuntia ficus-indica (L.) Mill, introduced already before the French colonization, is currently widely cultivated. Despite being classified as an invasive alien plant, it has also been used for some years for rehabilitation purposes in the green dam project that was designed to halt the advance of the Sahara towards the north of the country. It has also been classified as a species capable of providing a sustainable livelihood for rural populations, especially those located in arid and semi-arid areas.
Despite their wide range throughout the country and their abundant presence in gardens and public greens, only a few Opuntia species have escaped these localities, most of which were reported by Véla (2013).
Between 2016 and 2022, the first author of this paper has carried out extensive botanical surveys in the Skikda region (north-eastern Algeria). This work resulted in recording escaped populations of two further Opuntia species that were not reported before in Algeria, i.e. O. monacantha (Willd.) Haw. and O. tomentosa Salm-Dyck. Here, we present these localities and provide further information on biological and ecological characteristics of the study species in Algeria. Such information is essential for monitoring or managing the study species in the future. In addition, we provide a list of all Opuntia species having been reported to date as alien in mainland North Africa.

Materials and methods
During floristic surveys carried out by the first author of this paper between 2016 and 2022 in several municipalities in the center and east of the wilaya (= district) of Skikda (north-eastern Algeria), escaped populations of Opuntia monacantha and O. tomentosa were discovered. During a total of 35 field trips, the geographical coordinates, the colonized habitats and the degree of naturalization (according to Pyšek et al. 2004) was assessed. Species identification was done by consulting Britton and Rose (1919) and Véliz (2008).
In addition, we performed a bibliographic search on the focal species distribution in North Africa; in particular, we consulted the checklist of the alien flora of Algeria (Meddour et al. 2020), the Global Biodiversity Information Facility (GBIF 2022), African Plant Database (APD 2022) and Plants Of the World Online (POWO: http://plantsoftheworldonline.org). Further, all localities were revisited several times during different seasons for studying the phenology and the mode of reproduction of the species.
It should be noted that the surveys were done in two different ways: either by car following main or secondary roads, or by foot for inspecting areas that are inaccessible by car such as wastelands, abandoned gardens, edges of orchards and fields, semi-natural habitats and the coastal maquis

Localities and population size
Field surveys yielded, spread over a large perimeter of the study area, ten localities for Opuntia monacantha and three localities for O. tomentosa ( Figure 1). However, the populations of the former are larger than those of O. tomentosa. The different records, including the description of the colonized habitats and the degree of naturalization of the two species, are given below.

Opuntia monacantha (Willd.) Haw.
This species has been observed at several places for several years. In the Larbi Ben M'Hidi city, located east of the city of Skikda, two small populations were observed for the first time in 2016 and then re-observed several times until January 2022. The populations of O. monacantha are mostly confined to edges of sandy paths or to uncultivated land. One population consisted of five well-formed young individuals and two or three smaller ones that were developing from fallen cladodes. These individuals are often trampled by sheep or cows preventing their further growth (Table 1, Population no. 6). The other population includes three old individuals of 2.5 m height that flower and bear fruit regularly (Table 1 These records encouraged us to carefully prospect the nearby coastal maquis in search of Opuntia monacantha. The field surveys led to the discovery of a large population consisting of about thirty old fruit-bearing individuals From January 2019 to January 2021, a small population, comprising five or six well-developed and fruit-bearing individuals, was observed at the edge of the maritime sands of Filfilla beach, not far from the mouth of Wadi Righa. There, O. monacantha grows amidst Anthemis maritima subsp. maritima (Table 1, Population no. 10).
From 2020 until January 2022, a medium-sized population of 10 to 15 old individuals, some of which reach 2 m in height, was recorded in the maquis among olive trees and mastic trees on clay soil in Ramdan Djamel, located south of the city of Skikda, at the edge of the roundabout leading to Château Morel (Table 1, Population no. 8).
In 2021, new localities of O. monacantha were recorded, notably in Stora where the species was found in a sea cliff on at the edge of the road leading to the port of the village, among native species such as Ampelodesmos mauritanicus (Poir.) Durand and Schinz. and Chamaerops humilis. The small population consisting of five or six old fruit-bearing individuals ( Table 1, Population no. 9).
In January 2021, the species was observed in the city of Skikda, where an individual about 1 m tall was found growing on the slab of the main entrance of a building in the city ( Figure 2B). In September 2021, it had considerably grown and occupied the entire slab of c. 4.5 m² size (Table 1, Population no. 7).
In Algeria, O. monacantha flowers and fruits abundantly from June to August. However, the fruits can persist on the plant for several months. Seed germination has never been recorded but vegetative propagation from stem fragments, which root easily especially in sandy soils, has been observed at several localities.
According to the criteria proposed by Pyšek et al. (2004), O. monacantha can be considered as naturalized in Algeria, as it persisted at the locality of Larbi Ben M'Hidi for at least 15 years (according to the testimony of the inhabitants). At other localities, populations have recently spread considerably.

Opuntia tomentosa Salm-Dyck
This species was first observed in the gardens of the "Service Commun de Recherche, Pôle de Vulgarisation Botanique" located at the University of Skikda. In April 2018, a 70 cm tall individual was found there clinging to the trunk of Phoenix canariensis Chabaud. Then, further 17 young individuals which vary in size from 0.1 to 1 m were observed in May 2018 in the same green space on the gutter of a 3 m tall greenhouse which were still alive in February 2022 ( Figure 2D) ( Table 1, Population no. 3). Two further young individuals, 1 m tall and growing on the ground, were observed close to the greenhouse. The species is cultivated nearby and the planted individuals are up to 7 m tall.
A second locality of O. tomentosa is located in Ramdan Djamel at the edge of the roundabout leading to Château Morel; there a population of more than 20 individuals, some of which are 3 m tall, was observed from 2020 to January 2022 ( Figure 2C) At the presented sites, O. tomentosa flowers and sets fruits abundantly. It flowers from March to July, fruits ripen in August but can persist on the plant until autumn (October-November). Seed germination was observed several times in the field ( Figure 2E).
According to the criteria proposed by Pyšek et al. (2004), O. tomentosa should be classified as a casual alien species in Algeria as it does not yet show substantial spread to adjacent environments, despite its persistence in the three recorded localities.

Discussion
To our knowledge, the reported occurrences of Opuntia monacantha and O. tomentosa are the first ones for Algeria, as no reports are given in the databases consulted (APD 2022; GBIF 2022) nor in the most up to date checklist of alien plants of Algeria (Meddour et al. 2020).
In North Africa, O. monacantha has so far been reported as naturalized only for the Canary Islands (Verloove et al. 2017) and Tunisia , so this record is the second one for mainland North Africa. Conversely, O. tomentosa has so far only been reported from the Canary Islands (Dobignard and Chatelain 2011), making our records the first for mainland North Africa.
Based on our surveys, O. tomentosa should be added to the list of alien Opuntia species reported for mainland North Africa which are fewer than those of the northern part of the Mediterranean area (see Galasso et al. 2018;Aymerich and Sáez 2019). So far, only eight species have been reported from mainland North Africa (if O. stricta is considered conspecific with O. dillenii, Table 2). However, it is likely that further surveys will record additional alien Opuntia species for North Africa, as shown by our study.
Opuntia monacantha is native to Argentina (Chevalier 1947), Brazil, Paraguay and Uruguay, and has been introduced into different regions of the world as an ornamental plant. The escaped populations in Algeria are characterized by a bright and shiny green color of the cladodes and one or two spines per areole with often a spine larger than the other, the longest reaching up to 4 cm, with yellow base and brown top. The species has escaped  Opuntia monacantha colonizes a range of different habitats (e.g. coastal dunes, coastal maquis, maritime cliffs, clay soils and slabs of buildings in urban environments), and has an extensive record of successful invasions in the Mediterranean region, particularly in France (Corsica), Italy and Spain (Novoa et al. 2015;Puddu et al. 2016) and in regions with a Mediterranean climate such as South Africa where it colonizes coastal dunes (Moran et al. 2013). Thus, we argue that O. monacantha has a high risk of further spread in Algeria, and possibly it could become invasive such as O. ficus-indica and O. stricta. Therefore, we recommend that the occurrences of this species should be monitored.
The  (Sakhraoui et al. 2020). It forms a protective belt for the internal dune but has been considerably disturbed and altered in recent years by land development projects which are constantly increasing on the coast east of the city of Skikda including the beaches of Larbi Ben M'Hidi and Filfilla. These anthropogenic disturbances have probably favored the appearance and spread of several alien species including O. monacantha. The protection of the remaining natural maquis could therefore prevent further plant invasions and will undoubtedly have positive repercussions on the ecosystem. Despite all the efforts made so far within the framework of the national coastal protection project, the degradation of coastal habitats is ongoing, requiring the application of much more rigorous measures.
Opuntia tomentosa is native to Guatemala, Honduras and Mexico (Véliz 2008;Villaseñor 2016); it can easily be identified based on the velvety appearance of its cladodes that are entirely covered with very fine hairs. This species has been introduced in several regions of the world as an ornamental plant where it has escaped from cultivation (e.g. Australia). Alien occurrences are particularly reported from regions with a Mediterranean climate such as Spain, Italy and South Africa (Smith and Figueiredo 2012;Galasso et al. 2018;Aymerich and Sáez 2019). In the Canary Islands, the species is considered to be invasive (Acebes Ginovés et al. 2010).
The spread of individuals of O. tomentosa on roofs and trees indicates that birds are involved in the dispersal of the species and that reproduction via seeds plays an important role. This has also been observed in the field (e.g. at the Service Commun de Recherche, Pôle de Vulgarisation Botanique) where we recorded the presence of small individuals resulting from the germination of seeds.
Like several other Opuntioideae, the seeds of O. tomentosa possess physiological dormancy (Olvera-Carrillo et al. 2003) and have a very hard coating. In addition to their role in spread, digestion of seeds by birds probably also has positive effect on seed germination of this species as demonstrated in O. ficus-indica and O. robusta (Mokotjomela et al. 2021). In the future, the biogeographic status of the species is therefore likely to change, favored by its mode of reproduction (vegetative and sexual) and seed dispersal (zoochory); the latter facilitates the spread of seeds across large distances, thus further spread and establishment seems probably. This species also hybridizes with O. ficus-indica. Two hybrids of this parentage are currently known in Spain: O. × elisae (Guillot and Van Der Meer 2004;Ferrer-Gallego et al. 2014) and O. ficus-indica × tomentosa, the latter reported recently from the Canary Islands (Verloove et al. 2017). These hybrids might also be found in Algeria in the future, especially since O. ficus-indica has a wide distribution in this country.
The use of Cactaceae as living fences contributes enormously to the spread of several species of this family in Algeria and elsewhere. Opuntia ficus-indica remains the most popular species for this purpose in Algeria, but certain regions have distinguished themselves by selecting other species such as the village of Dem El Bagrat (municipality of Ben Azzouz, wilaya of Skikda), where Austrocylindropuntia subulata (Muehlenpf.) Backeb. is widely used, the Larbi Ben M'Hidi city where O. monacantha is widely used on the outskirts of citrus orchards and the region between Oued Fragha and Bouchegouf (wilaya of Guelma), where O. robusta is widely used. We believe that it will be necessary to inform rural people on the risks of this practice to limit the further spread of Cactaceae species in Algeria.
Finally, we recommend that occurrences of the two study species should be searched for in other regions of Algeria, particularly in the vicinity of old farms and colonial villas, from which we believe several of the reported populations escaped. These most often were surrounded by exotic gardens where several introduced species, including cacti, were grown.