On Opuntia spinulifera and O. streptacantha (Cactaceae), new to Spain, and the status of O. huajuapensis in that country

Opuntia spinulifera and O. streptacantha are reported for the first time from Spain. Both are more or less naturalized in scattered localities in Ayamonte (province of Huelva, SW Spain) where they were previously confused with O. huajuapensis. Claims of the latter from other Spanish regions are shown to be also erroneous. These three species, as well as O. leucotricha, have apparently been confused. Distinguishing features useful for their separation are discussed and the species that are present in Spain are illustrated.


Introduction
Opuntia huajuapensis Bravo is a species endemic to Mexico (Puebla, Oaxaca, Tecamachalco), described from Huajuapan de León (Bravo-Hollis, 1954, 1978. It is probably not widely cultivated as ornamental, if at all; at least it is not cited as such in standard works such as Huxley (1999), Sánchez de Lorenzo Cáceres (2000) or Hunt (2011). Nonetheless, it has been reported on several occasions as an escape from cultivation in various parts of Spain. Sanz-Elorza et al. (2004) reported about a small population in the Alforja riverlet basin in Cambrils (province of Tarragona). Subsequently, Pyke (2008) cited two populations from Collserola (province of Barcelona). Finally, Sánchez Gullón et al. (2014; erroneously as 'huajapensis') reported about the finding of this species in Ayamonte (province of Huelva). Based on these records O. huajuapensis was included in a worldwide list of invasive cacti (Novoa et al., 2015), albeit only from Spain.
In September 2018 the first author did fieldwork in dried out riverbeds in the Cambrils area where O. huajuapensis had been reported for the first time in Spain. This area is considered to host the highest diversity of cacti on the European continent (Sanz-Elorza et al., 2004 and several additional species were recorded during our own fieldwork, including potentially or genuinely invasive species (Verloove & Guiggi, 2019). However, O. huajuapensis was not recorded on that occasion. Instead, the morphologically similar O. leucotricha was regularly seen in rather numerous localities. Despite being fairly frequent this species was not mentioned by Sanz-Elorza et al. (2004. On closer examination the species depicted in Figure 1i in Sanz-Elorza et al. (2004) (Walters et al., 2011;Novoa et al., 2015;Sheehan et al., 2017). Apparently neither has been recorded before from Spain. They were thought to be also absent from the rest of Europe and the Mediterranean area (Korotkova & Raab-Straube, 2017). However, both are known as local escapes from cultivation in Italy (Guiggi, 2008;Galasso et al., 2018).
In this paper distinguishing characters useful for the separation of Opuntia huajuapensis, O. leucotricha, O. spinulifera and O. streptacantha are discussed and the latter three species are illustrated. A key for the identification of these species is presented. An overview of the known localities of O. spinulifera and O. streptacantha in Spain is provided. The different application of some of these binomials in the native and invaded area is also explained.  (Bravo-Hollis, 1978). Backeberg (1982) accommodated O. spinulifera in series Piliferae Backeb.

Morphological characters useful for the separation of
Out of these four species, Opuntia streptacantha ( Figure 1) is the most easily separated. It is tree-like (up to 5 m tall at maturity) with greenish (not glaucousgreen) obovate cladodes with a glabrous epidermis. Areoles are less closely spaced than in the other species (ca. 30 mm apart). Fruits are nearly always dark red (Bravo-Hollis, 1978;Scheinvar et al., 2010).
Opuntia leucotricha (Figure 2 A-C) is readily distinguished based on the following characters: plant tree-like (3−5 m tall at maturity) with a definite trunk that is covered in up to 8 cm long, white-greyish hair-like spines, cladodes are greyish-green, oblong ca. 14-28 × 11-15 cm, with a distinctly velvety indumentum and areoles are not impressed, fruits are usually yellowish white (rarely purplish red) (Scheinvar, 1974;Bravo-Hollis, 1978;Walters et al., 2011).   (Walters et al., 2011). Therefore the name O. leucotricha is now applied in a broader concept outside of its native range.
Opuntia spinulifera (as here delimited) (Figure 2 D-E) is a non-arborescent species rarely exceeding 1.5-2 m in height, with glaucous-green and glabrous, nearly orbicular cladodes that are often slightly retuse at apex, 20-25 (or up to 40) cm in diameter. Areoles are distinctly sunken and dense (8-20 mm apart). Spines 1-2(-9), up to c. 15-20 mm long, thin, rigid, reflexed, whitish. Fruits are widely barrel-shaped or globose, c. 3 cm in diameter, yellow (Bravo-Hollis, 1978;Walters et al., 2011). Impressed areoles and nearly orbicular cladodes are very characteristic features of O. spinulifera. In the density of the areoles this species resembles O. leucotricha, but it has much wider cladodes, and lacks the velvety stem epidermis, as well as the trunk with long and flexuose, filiform spines.
The classification of Bravo-Hollis (1978) and Britton & Rose (1919−1923 is followed here in the application of this binomial. Some Mexican authors apply the name O. spinulifera for O. leucotricha plants with long, hair-like spines on fruit and trunk (Scheinvar, 1982;Scheinvar et al., 2009). Scheinvar (1974) described O. heliabravoana Scheinvar this appears to be the same entity as O. spinulifera; and it is here treated as a synonym.
Opuntia huajuapensis is shrub-to almost tree-like (up to 2 m tall) with a more or less distinct trunk. Cladodes are obovate to orbicular, glaucous-green with slightly papillose epidermis. Areoles are ca. 20-30 mm apart, with long and abundant hairs. Spines are subulate, ascending to reflexed and bright or dark yellow, 6-14 in number. Fruits are yellow (Bravo-Hollis, 1978, Arias et al., 2012, Arreola-Nava et al., 2017. A good photo of this species was presented by Bravo-Hollis l.c. (p. 318, figure 172). It has been suggested that perhaps this is just a yellowflowered form of O. pilifera (Hunt et al., 2006).

Wild and introduced distribution of Opuntia spinulifera and O. streptacantha
Opuntia spinulifera was described from unsourced sterile material and long thought to be absent in the wild (Walters et al., 2011). A type is missing and the species was considered to be of uncertain taxonomic status by Hunt et al. (2006). However, O. heliabravoana Scheinvar was described from wild populations in the northeastern part of Valle de Mexico (with type from Hidalgo) (Scheinvar, 1974) and this is now often believed to be conspecific with O. spinulifera. At present, it is known to occur naturally (or partly naturalized?) in Valle de Mexico in the states of Hidalgo, Mexico, Puebla and Tlaxcala (Scheinvar et al., 2009).
It was introduced as ornamental to climatologically suitable areas elsewhere in the world, including Spain (Sánchez de Lorenzo Cáceres, 2000). Like many other opuntioids it was able to escape and naturalize. In South Africa it is a declared weed and a potential transformer species that invades savanna and grassland. It was first reported from Katrivier basin and more recently also from Bergville and Pietermaritzburg districts in Kwazulu-Natal (Walters et al., 2011). In similar conditions it is known from Australia (Novoa et al., 2015) and it is in the early stage of invasion in Namibia where it is spreading in the Windhoek townlands (Environmental Information Service Namibia, 2018). It also occurs as alien in Argentina and Brazil (Kiesling, 2005). In Europe it was introduced a long time ago already in the Hanbury Gardens on the Italian Riviera (Backeberg, 1982) from where it was able to escape. At present it is naturalized in scattered localities there, e.g. in Capo Nero, La Mortola and Bordighera (Guiggi, 2008;Galasso et al., 2018). To our knowledge and to date these were the only known feral populations in Europe.
Since 1989 its scattered presence was detected in coastal dune systems that are dominated by Retama monosperma Boiss. between Ayamonte and Punta del Moral (province of Huelva, Spain) (Sánchez Gullón et al., 2014;sub O. huajuapensis). In this area O. spinulifera apparently was formerly planted as hedge plant for dividing private farms. As such it extends for about four kilometers next to the road H-9021. In this area individuals were able to escape and now form scattered wild populations in psammophilous vegetation. At present the species is considered a naturalized but non-invasive species in the following localities: SPAIN, province of Huelva, Ayamonte, Avenida de la Playa at Isla Canela Golf, 37°11'41.62"N, 7°23'47.29"W, 6 m asl, several individuals over two kilometers, E. Sánchez Gullón obs.; SPAIN, province of Huelva, Ayamonte, Avenida del Real, 37°11'20.71"N, 7°20'47.33"W, 4 m asl, a single individual, E. Sánchez Gullón obs.
Opuntia streptacantha is a very common species in the Mexican table-lands, especially in the deserts of San Luis Potosí (Britton & Rose, 1919−1923Bravo-Hollis, 1978), where it is one of the most characteristic opuntias. It is also considered native in Guatemala where it is found in Sacatepequez, Chimaltenango and Quiche, at altitudes ranging between 1,600−2,500 m.a.s.l. (Véliz Pérez, 2008). It was formerly introduced to Australia where it has become an environmental weed in some states, for instance in New South Wales and Queensland (Novoa et al., 2015;Sheehan et al., 2017).
In Spain it has been known from a single locality in Ayamonte, where it was first referred to O. huajuapensis by one of us (ESG). A population of ca. 20−30 m 2 was detected in 2017 in degraded grassland with scattered Retama bushes and other cacti (Austrocylindropuntia subulata, Opuntia ficus-indica, etc.) in a vacant lot in a residential area: SPAIN, province of Huelva, Ayamonte, angle of Calle Guatemala and Calle Ecuador, 37°13'17.59"N, 7°23'51.15"W, 41 m asl, E. Sánchez Gullón obs.