A new tetraploid species of Tacinga (Cactaceae) from Ceará, Northeastern Brazil

Abstract

A new species of cactus, Tacinga mirim (Cactaceae: Opuntioideae), is described and illustrated. Tacinga mirim is like a miniature version of T. palmadora, as far as is known, endemic to the state of Ceará, Northeastern Brazil. Although some populations of the new species have been known since 2009, they had been wrongly identified as T. palmadora. The description of the new species was made based on morphological and karyotypic analysis. Morphologically, it differs from T. palmadora by the much smaller size, semi-prostrate habit, smaller and deciduous stem-segments, lower density of spines, slightly larger and wide-open flowers, smooth pericarpel, and the globose to obovoid, purplish ripe fruit. The karyotype of T. mirim differs from T. palmadora in being tetraploid (not diploid), by presenting chromosomes that are twice as large, eight of which are submetacentric (differing from the fully metacentric standard karyotype of T. palmadora). The distribution of the new species is associated with the Caatinga of the crystalline basement of the northwestern hinterland of Ceará, found at relatively low altitudes (190-360 m). The IUCN category of threat for the new taxon was preliminary assessed. Both EOO and AOO indicate that the species is endangered (EN-B1-2ab).

Key words:
biodiversity; Caatinga; cytotaxonomy; endemic; semiarid

Resumo

Uma nova espécie de cacto, Tacinga mirim (Cactacaeae: Opuntioideae), é descrita e ilustrada. Tacinga mirim é como uma miniatura de T. palmadora, até onde se sabe, endêmica do estado do Ceará, nordeste do Brasil. Apesar de algumas populações da nova espécie serem conhecidas desde 2009, elas vinham sendo erroneamente identificadas como T. palmadora. A descrição da nova espécie foi feita a partir de análise morfológica e cariotípica. Morfologicamente defere de T. palmadora pelo tamanho muito menor, o hábito semiprostrado, os segmentos menores e decíduos, a menor densidade de espinhos, flores um pouco maiores e com grande angulo de abertura, pericarpelo liso e o fruto globoso a obovóide, roxo quando maduro. O cariótipo de T. mirim difere de T. palmadora por ser tetraploide (ao invés de diplóide), por apresentar cromossomos duas vezes maiores, dos quais oito são submetacêntricos (diferindo do padrão cariotípico totalmente metacêntrico de T. palmadora). A distribuição da nova espécie está associada à Caatinga do embasamento cristalino do interior do Ceará, em altitudes relativamente baixas (190-360 m). A categoria de ameaça do novo táxon segundo a IUCN foi avaliada preliminarmente. Tanto a EOO como a AOO indicam que a espécie é ameaçada (EN-B1-2ab).

Palavras-chave:
biodiversidade; Caatinga; citotaxonomia; endêmica; semiárido

Introduction

The traditional circumscription of the genus Tacinga Britton & Rose comprised only two species, both endemic to eastern Brazil: T. funalis Britton & Rose and T. braunii E. Esteves Pereira (Taylor et al. 2002). Based on morphological characteristics of the flower, pollen, and seed, Taylor et al. (2002) transferred four more species and a hybrid (all endemic to eastern Brazil) from Opuntia to Tacinga: T. inamoena (K. Schum.) N.P. Taylor & Stuppy, T. palmadora (Britton & Rose) N.P. Taylor & Stuppy, T. werneri (Eggli) N.P. Taylor & Stuppy, T. saxatalis (F. Ritter) N.P. Taylor & Stuppy, and T. × quipa (F.A.C. Weber) N.P. Taylor & Stuppy. In the two decades that followed, one more species was recombined from Opuntia: Tacinga lilae (Trujillo & M. Ponce) Majure & R. Puente, and five more were described, including two nothospecies: T. subcylindrica (M. Machado & N.P. Taylor) M. Machado & N.P. Taylor, T. armata J.G. Freitas & E.M. Almeida, T. gladispina J.G. Freitas & E.M. Almeida, T. × flamea J.G. Freitas & E.M. Almeida, and T. × grandiflora N.P. Taylor & Zappi (Machado & Taylor 2003; Majure et al. 2013; Freitas et al. 2021; Taylor et al. 2023).

Except for T. lilae, which is from Venezuela (Majure et al. 2013), all the species of the genus are endemic to Eastern Brazil (Machado & Taylor 2003; Taylor & Zappi 2004; Freitas et al. 2021; Taylor et al. 2023). The range of most of the species is associated with the Caatinga biome (Taylor & Zappi 2004), but there are also some records in the Cerrado - only on limestone outcrops associated with semi-deciduous forests (Taylor & Zappi 2004; Gonzaga et al. 2023). In terms of evolution, there are still no molecular analyses covering all species in the genus, but preliminary data indicate the T. palmadora + T. lilae complex as a likely basal group. On the other hand, species with unique morphological characteristics (T. funalis and T. braunii), and the polyploids (T. inamoena and T. subcylindrica) appear to constitute more derived groups (Majure & Puente 2014; Martins 2022; Barrios-Leal et al. 2024).

Here we describe another species, that was first collected in 2009 by the first author, along with Nigel Taylor, Marlon C. Machado, Domingos Cardoso, Marcelo F. Moro, and Antônio Sérgio F. Castro, during a systematic survey of Cactaceae in the state of Ceará (Menezes et al. 2011). The plant was first found in Santa Quitéria and later in several other municipalities (Menezes et al. 2011, 2013). At the time, the most obvious features that differentiate the new species from T. palmadora (Britton & Rose) N.P. Taylor & Stuppy (reduced size, smaller stem-segments, and less spines) were interpreted as local peculiarities of the population due to the effects of vegetation management and livestock. Thus, it had been initially treated as T. palmadora (Menezes et al. 2011, 2013; Menezes & Ribeiro-Silva 2015).

Recently, in the second update to “Cacti of Eastern Brazil”, Taylor et al. (2022) revised some features of the genus and drew attention to the differences between the plant described here and the typical form of T. palmadora, recommending further studies. The typical form of T. palmadora, found in other Northeastern states (Rio Grande do Norte, Paraíba, Pernambuco, Alagoas, Sergipe, and Bahia), is a tall erect shrub, with flower morphology resembling that of T. werneri. However, the plants from Ceará are much smaller and have a flower morphology that resembles T. subcylindrica. Thus, new collections were made and the same population of Santa Quitéria was revisited to carefully assess the peculiarities of this Tacinga from Ceará.

Material and Methods

Fieldwork

Fieldwork was carried out on December 2022, in Santa Quitéria, Canindé, and surrounding areas (Ceará, Brazil). The main previously known population, from the locality of Piabas (municipality of Santa Quitéria, Ceará, Brazil), was the first one visited for this study. A second important population was discovered in the Reserva Imburanas da Volta - a private protected area in the municipality of Canindé. Additional occurrence points were also recorded in Canindé, in the surroundings of the Reserva Imburanas da Volta. The position of each population was recorded with GPS for later mapping.

Morphological analysis

Morphological descriptions, measurements, and photographs were taken from live specimens in the field. Some samples were collected as vouchers and others were cultivated until anthesis or fruit ripening. All samples were deposited in the Prisco Bezerra Herbarium (EAC). Additional specimens from EAC were also analyzed. The general botanic terminology follows Harris & Harris (2001). For unique Cactaceae features the standards of Hunt et al. (2006) were used. All the measurements were taken with a caliper and follow the order length × width (for plain structures) or length × diameter (for solid structures).

Karyotype analysis

Chromosome Preparation - stem-segments of four individuals (M.O.T. Menezes, 437, 438, 443, and 444) were cultivated for karyotype analysis. Tips of young roots were pre-treated with 8-hydroxyquinoline (8HQ) for 20 hours at 4 °C. They were then fixed in Carnoy 3:1 (ethanol: acetic acid) for 2 to 24 hours at room temperature and stored at -20 °C in the fixative. For staining with fluorochromes, the young roots fixed with Carnoy were washed in distilled water and digested with an enzymatic solution (3% cellulase / 1% pectolyase). The cell dissociation of the root apical meristem was performed following the protocol established by Alves et al. (unpublished data). The cell dissociation of the meristem was carried out using an ultrasonic cleaner (power between 30W or 50W) for 1 minute. For this purpose, 0.5 ml microtubes containing digested root tips were used and rapidly washed in 100 µL of 3:1 fixative solution (methanol: acetic acid), which was then removed and added back to the microtube. The glass slides were preheated and 10 µL of the cell suspension was pipetted onto each slide. After completely drying at room temperature, the slides were briefly dipped in 60% acetic acid and incubated in a laboratory oven at 37 °C for 30 minutes.

ND-FISH and CMA/DAPI Staining - After three days the glass slides were fixed in Carnoy for 15 minutes, then dehydrated in an alcohol series: 70% alcohol for 3 minutes, followed by 100% alcohol for 3 minutes. The glass slides were then incubated in the laboratory oven at 60 °C for 30 minutes and cooled at room temperature for 10 minutes. The hybridization mix was prepared containing 2x SSC and 5S probe. 20 µL of the mix was used per slide, which was covered with a 22 x 22 mm coverslip. Hybridization was carried out in a humid chamber in the laboratory oven at 37 °C for 2 hours. After hybridization, coverslips were removed with a 2x SSC wash and rinsed in 4x SSC for 10 minutes without agitation (Cuadrado et al. 2009). After drying, the slides were stained with 10 µL of CMA3 (0.1 mg/mL) for one hour, washed in 2x SSC, air-dried, and mounted with 10 µL of McIlvaine/glycerol buffer (pH 7.0) (1:1, v/v) containing DAPI (1 μg/mL). The best cells were imaged using an Axion Imager A2® microscope with ZEN® software and the images were subsequently edited using Adobe Photoshop CS3® version 10.0.

Geographic distribution and evaluation of conservation status

The maps were prepared with QGIS (Sherman et al. 2011), using the geographic coordinates obtained in field and data from SpeciesLink (<https://specieslink.net/>). The geographic data were compared with the distribution of Tacinga palmadora (occurrence points obtained from SpeciesLink).

Geographic coordinates of the populations were also used to assess the conservation status of the new species, using the Geospatial Conservation Assessment Tool - GeoCAT (Bachman et al. 2011; Kew Gardens 2023), which evaluates the conservation status based on the extent of occurrence (EOO) and the area of occupancy (AOO). For this we used the standard 2 km cell. The habitat loss was assessed through the publicly available MapBiomas Project (2024), which monitors Brazil’s deforestation based on the classification of images from the Landsat satellite (Sousa Jr. et al. 2020). Based on these data, we evaluated the loss of natural vegetation between 1985 and 2022 in the municipalities in which the new species occurs.

Results and Discussion

We found eight populations / occurrence points in field, from where we collected five specimens with flowers and/or fruits (Menezes 435, 437, 439, 443, and 444). These samples we used as original material (holotype and paratypes). The examination of herbarium collections returned seven records previously identified as T. palmadora for Ceará. Five of them were indeed T. mirim and were used as paratypes (see additional material examined). However, two of them were not determined, as they lacked reproductive parts and/or diagnostic traits. The first is the collection M.O.T. Menezes 242 (EAC 48813), from Viçosa do Ceará (in the extreme northwest of Ceará), that may be a hybrid of T. inamoena with some spiny Tacinga (probably not T. palmadora, considering its distribution). The second is the collection J.R. Andrade 156 (PEUFR 50295) from Milagres, in the very southeast of the state. Considering the density of spines (up to 5-6 per areole) and the size of the stem-segment, this specimen is certainly not T. mirim. However, the herbarium-sheet consists of only a single vegetative stem-segment and lacks diagnostic traits to determine the species. Thus, although it might belong to T. palmadora, it could represent any other spiny species of the genus, therefore the occurrence of T. palmadora in Ceará is yet to be confirmed.

Among the most distinctive morphological traits of T. mirim, we highlight the reduced height, the number of stigma lobes (4-5), deciduous stem-segments, wide-open flowers, purplish fruits when fully ripe, and the narrow floral tube, causing the stamens to be almost parallel to the pistil (Figs. 1-2). The typical form of T. palmadora, found in other Northeastern states (Rio Grande do Norte, Paraíba, Pernambuco, Alagoas, Sergipe, and Bahia), is an erect shrub, reaching up to 4 m tall (Hunt et al. 2006a; Taylor & Albuquerque-Lima 2020), with conspicuously tuberculate pericarpel, and a perianth that does not strongly diverge from the floral axis, resembling the flower of T. werneri (Taylor & Zappi 2004 - Fig. 6.3; Hunt et al. 2006b - Fig. 438.5; Taylor et al. 2022 - Fig. 6). The plants from Ceará differ by having a semi-prostrate habit with rather small and almost terete stem-segments, a smooth pericarpel, and a wide-open flower, resembling T. subcylindrica. However, T. mirim differs from the latter by the presence of spines, flat stem-segments, and the purplish fruit, which is also bigger.

Figure 1
a-g. General aspect of Tacinga mirim - a. flat stem-segments with spines and flowerbud; b. growth habit, with less than 50 cm height; c. M.O.T. Menezes collecting data on a young individual of T. mirim; d. growing on rocks along the Curu river, in mun. Canindé-CE; e. flat stem-segments with immature fruit; f. small individual showing roots; g. aggregated areoles in the apex of a young stem. (a,e. Menezes 435; b. Menezes 437; g. Menezes 437, cultivated). Photos: a,b,e,g. M.O.T. Menezes; c,d,f. L.J. Carvalho.

The flowers of T. mirim and T. palmadora have similar size, but remarkably different morphology. Locatelli & Machado (1999) recorded that T. palmadora is pollinated by the hummingbird Chlorostilbon lucidus (Shaw 1812), which visits the flower hovering in the air (no landing platform needed). Indeed, the flowers of T. palmadora are narrow (1.5-2.0 cm wide) and do not form a landing platform. Regarding anthesis, the flowers of T. palmadora open mainly around 05:30h (with some flowers opening around 15:00h) and the anthesis lasts for about 48 hours (Locatelli & Machado 1999). In the case of T. mirim the flowers are wide-open and may reach up to 3.3 cm in diameter, building a possible landing platform to flower visitors such as bees and butterflies. However, no observations were made on this matter, so further studies on anthesis and flower visitors of T. mirim are still needed. Additionally, with no systematic observations having been carried out yet, it is only known that its flowers open at dawn and close around 13:00h.

The clonal reproduction through the pericarpel of fallen fruits plays an important role in the propagation of T. lilae (Trujillo & Ponce 1990 apud.Majure et al. 2013), T. palmadora (Meiado 2012), and T. armata (Freitas et al. 2021). It was also recorded for T. mirim (Fig. 2a). Additionally, T. mirim also exhibits clonal reproduction by abscission of terminal stem-segments. These two ways of clonal reproduction play an important part in the formation of dense thickets up to 2 m in diameter found in this species (Fig. 1b).

Tacinga mirim has a karyotype of 2n = 44 (Fig. 3a), primarily composed of relatively symmetrical metacentric chromosomes and few submetacentric (36M and 8SM), with sizes ranging from 1.89 to 3.37 μm. Additionally, it presents four CMA+ heterochromatic bands and four 5S rDNA sites. Two of the four CMA+ bands and two of the four 5S sites are located in the interstitial region on the long arm of chromosome pair 21. The other two 5S sites, as well as the CMA+ bands, are located in the terminal region of the short arm of chromosome pairs 6 and 9, respectively (Fig. 3b). This karyotype differs remarkably from the one of T. palmadora, which is diploid (2n = 22), composed of metacentric chromosomes (22M) with sizes ranging from 0.80 to 1.11 μm (Alves et al. 2019), and exhibits only one chromosome pair with visible terminal CMA⁺ bands and two interstitial 5S rDNA sites (Fig. 1c-d).

With this karyotype, we confidently dismiss the hypothesis of T. mirim being a nothospecies. We base this conclusion on the observations that nothospecies generally emerge in regions where parental species co-occur, exhibiting resemblances to them (Freitas et al. 2021; Taylor et al. 2023). The only other species of the genus present throughout the state of Ceará are T. inamoena and T. subcylindrica. Although both are also tetraploid, they have a remarkably different morphology from T. mirim. Also, a hybrid between these species should have 3 submetacentric chromosomes, be thornless, and have red, orange or yellow fruits. However, T. mirim does not have any of these features.

Tacinga mirim and the other tetraploid species of the genus (e.g., T. inamoena, T. subcylindrica, T. gladispina, and Tacinga × flammea) share some cytogenetic characteristics, such as the chromosomal number (2n = 44), the prevailing presence of metacentric chromosomes, and the recurrent presence of terminal CMA heterochromatic bands and interstitial 5S rDNA sites (Alves et al. 2019). However, these species diverge in other aspects, including the karyotypic formula, chromosome size, and the number and location of CMA bands and 5S rDNA sites (Alves et al. 2019; Freitas et al. 2021). Until now, T. mirim seems to be the only taxon presenting a karyotypic formula of 36M + 8SM and CMA⁺ bands = 2i+2t (Tab. 1).

The tetraploid species are usually the smaller plants in the genus Tacinga, reaching height of no more than 35-60 cm (diploid and hexaploid species are bigger - Tab. 1). Except for T. gladispina, which is erect (Freitas et al. 2021), all the tetraploid are semi-prostrate, forming clumps of mats (Tab. 1). Either the reduced habit is an ancestral trait inherited from a putative tetraploid ancestor or the tetraploidy represents a homoplasic trait possibly related to the low height of these plants (which may affect pollination).

Figure 2
a-i. Reproductive aspects of Tacinga mirim - a. vegetative propagation by fallen fruits; b-c. flower in anthesis; d. flower and immature fruit in the apex of the stem-segment; e. post anthesis flowers; f. flowers in longitudinal section; g. fruits at different stages of maturation; h. open fruit; i. fully developed x undeveloped seeds. (b-f. Menezes 437; g. respectively, Menezes 444, 439, 435, and 444; h. Menezes 444; i. Menezes 437 and 444, mixed). Bars: 1 cm. Photos: M.O.T. Menezes.

Tacinga mirim is the second endemic cactus taxon to be recorded in the state. The other one is Pilosocereus chrysostele subsp. cearensis. These two endemics may be a consequence of the extensive highlands that surround the state (Serra da Ibiapaba, Chapada do Araripe, Chapada do Apodi), acting as biogeographical barriers and promoting reproductive isolation during Pleistocene and Holocene. This hypothesis is supported by some cases of long distance vicariance in other Cactaceae (Menezes et al. 2012). Unfortunately, there are no genetic studies evaluating this hypothesis for Tacinga yet.

Taxonomic treatment

Tacinga mirim M.O.T. Menezes sp. nov. Type: BRAZIL. CEARÁ: Santa Quitéria, Piabas, 30.XII.2022, fl. and fr., M.O.T. Menezes 437 (holotype EAC 67017).

Tacinga mirim is a semi-prostrate cactus forming clusters no more than 50 cm tall and up to 200 cm wide with stem-segments flat to terete, small, spiny, and deciduous near the apex; wide-open flowers, dark orange to red; fruits globose to obovoid, purplish epicarp. It differs from Tacinga palmadora in several aspects: the small size, the semi-prostrate habit, the smaller stem-segments (half the size), which may be flat to oblong, smaller areoles with less spines (max. 3, usually 1-2), which are also thicker. Additionally, it features slightly larger flowers, with wide-open perianth-segments, a pericarpel with an almost smooth surface (with tubercles scarcely pronounced only when the plant is dehydrated), fruits globose to slightly obovoid (orange to purplish when mature and with occasional spines). Also, the species is tetraploid (2n = 44), unlike T. palmadora, which is diploid (2n = 22). Its size, growth habit, and the wide-open flowers resemble those of T. subcylindrica, however, the plant is spiny, its pericarpel is larger, and fruits have different color, size, and shape.

Subshrub, with taproot, semi-prostrate, 35-50 cm tall, usually growing in clusters 60-90(-200) cm wide due to vegetative propagation, irregular sympodial branching; stem-segments flat to terete, elliptical to obovate, 4.4-8.5(-11) × 2.4-4.0 cm, epidermis olive to dark green, bearing areoles with glochids and spines (sometimes spineless in the lower half), segments usually deciduous near the apex (at least in the dry season); Areoles 1-1.5 cm apart, 32-38 per segment face, round, 2-3 mm in diameter, bearing white felt (greyish when old), glochids and deciduous vestigial leaves (in young stem-segments) or spines (in mature stem-segments); glochids golden yellow, c. 1 mm; spines acicular, yellow when young, turning white to grey when old, (0-)1-2(-3) per areole, (7-)10-26(-35) × 0.5-1.0 mm; Flowers arising in the distal third of the stem-segments, 3.1-3.6(-4.1) × 2.6-3.3 cm, pericarpel pyriform, smooth to slightly tuberculate, 1.7-2.1 cm, olive-green, bearing areoles with glochids and occasional spines (seen only in fruit), outer perianth-segments narrowly lanceolate, pink with orange lateral edges, inner perianth-segments ovate and mucronate, dark orange to red, stamens erect, surrounding the style (almost parallel to it), anthers yellow, inner filaments yellow, outermost ones reddish orange, style yellow with 4-5 white stigma-lobes, which are fully projected beyond the stamens; Fruits deciduous when ripe, globose to obovoid, with a sunken apex, funiculus slightly depressed, 1.7-2.5 × 1.4-1.7 cm, bearing 21-25(-28) areoles with white felt, golden yellow glochids, bristles, and rarely spines (< 1 cm), pericarp orange turning purplish when fully ripe, funicular pulp translucent; Seeds, c. 14 per fruit, some aborted, 4 × 3 mm when fully developed.

Figure 3
a-d. Metaphase cells with double staining CMA/DAPI and ND-Fish, and karyogram organized by chromosomal type, Metacentric (M) and Submetacentric (SM) - a-b. Tacinga mirim, tetraploid with 2n = 44; c-d. T. palmadora, diploid with 2n = 22. Bar: 10 μm. Photos: L.I.F. Alves.

Table 1
Compared morphology and karyotype of the known species of the genus Tacinga.

Species	Habit / height	Stem-segments	Spines	Inner perianth segments	Fruit	Karyotype	Karyotypic formula
Tacinga braunii 1	shrubby or semi-scandent (< 600 cm)	cylindric to flat	-	pale green to purplish	narrowly urceolate; greenish; spineless	2n = 22 (A19)	20M + 2SM (A19)
Tacinga funalis 1	shrubby, decumbent or scandent (< 1200 cm)	cylindric	-	pale green	Bottle-shaped; greenish to reddish or purple; spineless	2n = 22 (C13)	22M (A19)
Tacinga saxatilis 1	shrubby, forming clumps (< 400 cm)	flat	acicular*	yellow to orange	globose to depressed-globose; brownish green to wine-red; spineless?	2n = 22 (M12)	?
Tacinga palmadora 1,6	shrubby, forming clumps (< 400 cm)	flat	acicular*	orange	turbinate to obovoid; greenish to reddish or purple; spineless?	2n = 22 (C13)	22M (A19)
Tacinga inamoena 1	shrubby, forming clumps (< 50 cm)	flat	-	orange	globose to depressed-globose; yellow to orange; spineless	2n = 44 (M12)	44M 40M + 4SM 32M + 12SM 12SM + 32M (A19)
Tacinga subcylindrica 2	subshrub, usually forming dense mats (< 35cm)	oblong	-	orange-red	globose; dark orange to red; spineless	2n = 44 (A19)	42M + 2SM (A19)
Tacinga gladispina 4	erect shrub (< 60 cm)	flat	acicular, flat base	orange	depressed-globose; depressed-globose; spineless	2n = 44 (F21)	40M + 4SM (F21)
Tacinga mirim	semi-prostrate subshrub (< 50 cm)	flat to oblong	acicular	dark orange to red	globose to slightly obovoid; dark orange to purplish; rarely spiny	2n = 44 (TW)	36M + 8SM (TW)
Tacinga lilae 3,7	erect shrub (<120 cm)	flat*	acicular*	red*	Barrel-shaped; purple	2n = 66 (M12)	?
Tacinga werneri 1	shrubby (< 100 cm)	flat	acicular*	bright red	elongate ovoid; pale greenish white to white; spineless	2n = 66 (A19)	52M + 14SM (A19)
Tacinga armata 4	erect shrub (< 80 cm)	flat	acicular	red	oblong to globose; dark green to pinkish; spiny	2n = 66 (F21)	42M + 2SM (F21)
Tacinga × quipa 5	spreading subshrub (< 35cm)	flat or curved	inconstant / contorted	orange-red	“resembling those of T. inamoena”	Expected to be 2n = 33	?
Tacinga × flammea 4	erect shrub (< 50 cm)	flat	acicular	orange with red edges	oblong; reddish orange; spineless	2n = 55 (F21)	49M + 6SM (F21)
Tacinga × grandiflora 5	Subshrub (< 40cm)	flat / elliptic-oblong	-	lustrous greenish gold	“resembling those of T. funalis”	Expected to be 2n = 33	?

• ^Notes:
  Source of morphological traits: 1 = Hunt et al. (2006a; 2006b); 2 = Machado & Taylor (2003); 3 = Majure et al. (2013); 4 = Freitas et al. (2021); 5 = Taylor et al. (2023); 6 = Taylor & Albuquerque-Lima (2020); 7 = Majure (personal communication). Source of karyotypes: A19 = Alves et al. (2019); C13 = Castro et al. (2013); F21 = Freitas et al. (2021); M12 = Majure et al. (2012); TW = This Work. * = trait obtained from the photographs of the cited publications.

Additional material examined (paratypes): BRAZIL. Ceará: Canindé, Reserva Imburanas da Volta, 30.XII.2022, M.O.T. Menezes 443, 444 (EAC 67019; EAC 67020). Catunda, 24.I.2011, M.O.T. Menezes 268 (EAC 48810). Santa Quitéria, Piabas, 22.I.2009, M.O.T. Menezes 170, 172 (EAC 44394; EAC 44395); 30.XII.2022, M.O.T. Menezes 435, 439 (EAC 67016; EAC 67018); Serra do Pajé, 8.V.1997, L.W. Lima-Verde (EAC 25522). Sobral, Taperuaba, VII.2017, E.B. Souza; F.F. Araújo 4755 (EAC 61320).

This species was collected with flower-buds and open flowers in July, December, and January; with fruits in December and January.

The epithet comes from Nheengatu mi’ri, which means small (Miranda 1946), in allusion to its reduced dimensions. It is a tribute to the native language of the indigenous people from Pindorama, who suffered genocide with the invasion of European colonialists from the 16th century onward (Ribeiro 1995). The word is still used today in Brazil with the meaning of small or childlike.

The distribution of T. mirim is restricted to northern Ceará state and completely disjunct from the distribution of Tacinga palmadora (Fig. 4). The currently known range of T. mirim is also dozens to hundreds of kilometers apart from the core distribution of T. palmadora, which includes the states of Bahia, Pernambuco, Sergipe, Alagoas, Paraíba, and Rio Grande do Norte. Tacinga mirim is found in the northwestern inland lowlands (“depressão sertaneja”) of Ceará, from 190 to 360 m above sea level¹ (Fig. 5). The terrain is mostly flat, with a crystalline basement and shallow rocky substrate, where rock outcrops are very common. The climate is tropical semiarid (Aw / Bsh), with a mean annual temperature of 26-28 °C and precipitation of 600-900 mm / year (Climate-Data.org 2023). The rainy season occurs during autumn and summer, especially between January and May. The dry season lasts for six to eight months (Nimer 1972), and vegetation usually becomes dormant (IBGE 2012). The species inhabits deciduous and semideciduous shrublands and forests (and probably other kinds of vegetation associated with the Caatinga - Fig. 5). It grows on sandy, clayey or stony substrates (including rocky outcrops) and develops well both under full sun and partial shade (in savanna) or in the shade of trees (in dry forests). It often grows in the dry riverbeds of intermittent streams. In the savanna, it occurs associated with Calliandra spinosa Ducke, Cenostigma pyramidale (Tul.) Gagnon & G.P.Lewis, Cereus jamacaru DC., Croton jacobinensis Baill., Melocactus zehntneri (Britton & Rose) Luetzelb., Mimosa tenuiflora (Willd.) Poir., Pilosocereus chrysostele subsp. cearensis P.J.Braun & Esteves, Xiquexique gounellei (F.A.C. Weber) Lavor & Calvente, among other typical Caatinga elements. In the dry forests, it is associated with the occurrence of Amburana cearensis (Allemão) A.C.Sm., Cenostigma pyramidale (Tul.) Gagnon & G.P.Lewis, Cereus jamacaru DC., Commiphora leptophloeos (Mart.) J.B.Gillett, Cordia oncocalyx Allemão, Croton blanchetianus Baill., Erythrina velutina Willd., Mimosa arenosa (Willd.) Poir., Pseudobombax marginatum (A.St.-Hil., Juss. & Cambess.) A.Robyns, Xiquexique gounellei (F.A.C.Weber) Lavor & Calvente among others.

The extent of occurrence (EOO) of Tacinga mirim is 3,033.22 km², while the area of occupation (AOO) is 36.00 km². Thus, they both fit the range criteria for the Endangered category of the IUCN Red List (B1 and B2). Two conditions for geographic threaten are also observed. First, there are only five locations of occurrence (see Material examined) - meeting the condition “a” for endangered. Second, the habitat of the new species is in decline - meeting the condition “b” for endangered. According to the MapBiomas Project (2024), the municipalities in which the T. mirim occurs suffered natural vegetation loss ranging from 4 to 16% of their extent between 1985 and 2022 (Fig. 6). The deforestation is associated mostly with farming and livestock (Vieira et al. 2017) - activities that were also seen in fieldwork. In the type locality, in Santa Quitéria, the habitat loss in worrying, since 71,46% of the extent of the municipality has some degree of environmental disturbance (Vieira et al. 2017). Furthermore, in 2020, the state government signed an agreement with a consortium formed by two large companies to implement a huge mining project in Santa Quitéria (Brazilian Ministry of Mines and Energy 2024). According to the environmental impact assessment (Tetra Mais Consultoria 2022), the so called ‘Santa Quitéria Project’ will benefit from an investment of 460 million dollars to mine phosphate and uranium, near the border with Canindé (Fig. 6). When fully working it aims an estimated production of 1,050,000 tons/year of phosphate fertilizers, 220,000 tons/year of dicalcium phosphate, and 2,300 tons/year of uranium (Tetra Mais Consultoria 2022). The impact assessment presented by the mining corporates mentions the presence of Tacinga palmadora (probably T. mirim) in the area under the direct influence of the project (Tetra Mais Consultoria 2021, p. 917; 927). However, as no voucher is mentioned, the occurrence of populations in the immediate surroundings of the mining is uncertain. In any case, the closest populations, from Canindé and Piabas/Santa Quitéria (type locality), are just 29 and 32 km away, respectively. Therefore, considering the severity and extent of the direct and indirect impacts caused by mining, these populations may suffer impacts with the installation of the project. Rigorous studies are necessary in the proposed mining area in order to confirm the presence of T. mirim in the region and, if needed, reevaluate the environmental impacts.

Figure 4
a-b. Distribution of - a. Tacinga mirim and T. palmadora in Northeastern Brazil; b. detailed distribution of Tacinga mirim in Ceará. Maps: M.O.T. Menezes.

Figure 5
a-f. Habitat and growth habit of Tacinga mirim - a. landscape of the area of occurrence; b. habitat at the type locality (Savana); c. habitat in the Reserva Imburanas da Volta (Dry Forest); d. growing in association with Xiquexique gounellei (Piabas); e. growing in rocky soil (Piabas); f. growing in a litter rich soil in the dry forest (Reserva Imburanas da Volta). Photos: M.O.T. Menezes.

Figure 6
Habitat loss in the area of occurrence of Tacinga mirim between 1985 and 2022, highlighting the surroundings of the known populations.

Acknowledgements

The authors would like to express gratitude to Fundação de Apoio à Pesquisa do Estado da Paraíba (FAPESQ) and to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the financial support for the cytogenetic analyses; to Leonardo Jales Carvalho, for his photographs and the companionship during the field expeditions; to Antônio Sergio F. Castro, for his company and hospitality at the Reserva Imburanas da Volta; to Diego Santos and Carlinhos Pinheiro, for the photographs of the herbarium-sheet from PEUFR collection; and to Nigel P. Taylor, for his opinion and considerations on the draft of this manuscript.

Data availability statement

In accordance with Open Science communication practices, the authors inform that all data used in this manuscript is publicly available.

References

• Alves JCF, Batista FRC, Neves JAL, Alves LIF, Almeida EM & Zappi DC (2019) Cytogenetics characterization of Tacinga Britton & Rose (Opuntioideae-Cactaceae). In: Zuffo AM (ed.) As regiões semiáridas e suas especificidades 2: 43-51.
• Bachman S, Moat J, Hill A, de la Torre J & Scott B (2011) Supporting Red List threat assessments with GeoCAT: geospatial conservation assessment tool. ZooKeys 150: 117-126.
• Barrios-Leal DY, Menezes RST, Zappi D & Manfrin MH (2024) Unravelling the genetic diversity and population dynamics of three Tacinga species (Cactaceae: Opuntioideae) in the Caatinga. Botanical Journal of the Linnean Society 204: 256-266.
• Brazilian Ministry of Mines and Energy (2024) Projeto Santa Quitéria e governo do Ceará assinam Memorando de Entendimento. Availabe at < Availabe at https://www.gov.br/mme/pt-br/assuntos/noticias/projeto-santa-quiteria-e-governo-do-ceara-assinam-memorando-de-entendimento >. Access on 6 February 2024.
  » https://www.gov.br/mme/pt-br/assuntos/noticias/projeto-santa-quiteria-e-governo-do-ceara-assinam-memorando-de-entendimento
• Castro JP, Souza LGR, Alves LF, Silva AEB, Guerra M & Felix LP (2013) IAPT/IOPB chromossome data 15. Taxon 62: E1-E34.
• Climate-Data.Org (2023) Climate: Ceará. Available at <Available at https://en.climate-data.org/south-america/brazil/ceara-212/ >. Access on 17 February 2023.
  » https://en.climate-data.org/south-america/brazil/ceara-212/
• Cuadrado A, Golczyk H & Jouve N (2009) A novel simple and rapid nondenaturing FISH (ND-FISH) technique for the detection of plant telomeres. Potential used and possible target structures detected. Chromosome Research 17: 755-762.
• Freitas JG, Alves LIF, Zappi DC, Almeida EM, Peraza-Flores LN, Amaral DOJ, Araújo DBP & Batista RFC (2021) Novelties in Cactaceae from Eastern Brazil: adding two new species and one new nothospecies to Tacinga (Opuntioideae). Phytotaxa 490: 239-252.
• Gonzaga DR, Pereira FO, Almeida TMH, Pires ACM & Menini-Neto L (2023) New and revised records of Tacinga from Goiás and Tocantins States Brazil. Hoehnea 50: e292023.
• Harris JG & Harris MV (2001) Plant identification terminology: an illustrated glossary. Spring Lake Publishing, Payson. 216p.
• Hunt D, Taylor N & Charles G (2006a) The new cactus lexicon. Text volume. Dh Books, Milborne Port. 373p.
• Hunt D, Taylor N & Charles G (2006b). Atlas of illustrations. Dh Books, Milborne Port. 526p.
• IBGE (2012) Manual técnico da vegetação brasileira. IBGE, Rio de Janeiro. 275p.
• IUCN (2012) IUCN Red List Categories and Criteria. Version 3.1. IUCN Species Survival Commission, Gland and Cambridge. 32p.
• Kew Gardens (2023) GeoCAT - Geospatial Conservation Assessment Tool. Available at <Available at https://geocat.kew.org/ >. Access on 6 November 2023.
  » https://geocat.kew.org/
• Locatelli E & Machado ICS (1999) Comparative study of the floral biology in two ornithophilous species of Cactaceae: Melocactus zehntneri and Opuntia palmadora Bradleya 17: 75-85.
• MapBiomas Project (2024) Coleção 8.0 da série anual de mapas de uso e cobertura da terra do Brasil. Available at <Available at https://brasil.mapbiomas.org/ >. Access on 3 February 2024.
  » https://brasil.mapbiomas.org/
• Machado MC & Taylor NP (2003) A new subspecies of Tacinga inamoena (Cactaceae) from eastern Bahia Brazil. Bradleya 21: 13-16.
• Majure LC & Puente R (2014) Phylogenetic relationships and morphological evolution in Opuntia s.str. and closely related members of tribe Opuntieae. In: Hunt D (ed.) Further studies in the Opuntioideae. Succulent Plant Research 8: 9-30.
• Majure LC, Puente R, Griffith MP, Soltis DE & Judd WS (2013) Opuntia lilae, another Tacinga hidden in Opuntia s.l. (Cactaceae). Systematic Botany 38: 444-450.
• Majure LC, Puente R & Pinkava DJ (2012) Miscellaneous chromosome counts in Opuntieae (Cactaceae) with a compilation of counts for the group. Haseltonia 18: 67-78.
• Martins JS (2022) Espécies brasileiras de Tacinga Britton & Rose (Cactaceae): morfoanatomia e estratégias reprodutivas. Dissertação de Mestrado. Universidade de São Paulo, Piracicaba. 119p.
• Meiado MV (2012) Propagação sexual e assexual estruturando populações de Tacinga palmadora (Britton & Rose) N.P. Taylor & Stuppy, um cacto endêmico da caatinga. Revista de Biologia Neotropical 9: 6-13.
• Menezes MOT & Ribeiro-Siva S (2015) Cactáceas do Ceará Brasil: prioridades para a conservação. Gaia Scientia 9: 67-76.
• Menezes MOT, Taylor N & Castro ASF (2012) New disjunct record of Melocactus violaceus in Ceará northeastern Brazil. Bradleya 30: 151-154.
• Menezes MOT, Taylor NP & Loiola MIB (2013) Flora do Ceará Brasil: Cactaceae. Rodriguésia 64: 757-774.
• Menezes MOT, Taylor N, Machado MC, Coelho PJA & Correia D (2011) Diversity and distribution of Cactaceae in Ceará state North-eastern Brazil. Bradleya 29: 13-42.
• Miranda VC (1946) Estudos sôbre o Nhêengatú. Imprensa Nacional, Rio de Janeiro. 127p.
• Nimer E (1972) Climatologia da Região Nordeste do Brasil. Revista Brasileira de Geografia 34: 3-51.
• Ribeiro D (1995) O povo brasileiro: a formação e o sentido do Brasil. Cia. das Letras, São Paulo. 480p.
• Sherman GE, Sutton T, Blazek R, Holl S, Dassau O, Morley B, Mitchell T & Luthman L (2011) Quantum GIS user guide - Version 1.7 “Wroclaw”. Available at <Available at http://download.osgeo.org/qgis/doc/manual/qgis-1.7.0_user_guide_en.pdf >. Access on 3 March 2023.
  » http://download.osgeo.org/qgis/doc/manual/qgis-1.7.0_user_guide_en.pdf
• Souza Jr. CM, Shimbo JZ, Rosa MR, Parente LL, Alencar AA, Rudorff BFT, Hasenack H, Matsumoto M, Ferreira LG, Souza-Filho PWM, Oliveira SW, Rocha WF, Fonseca AV, Marques CB, Diniz CG, Costa D, Monteiro D, Rosa ER, Vélez-Martin E, Weber EJ, Lenti FEB, Paternost FF, Pareyn FGC, Siqueira JV, Viera JL, Ferreira-Neto LC, Saraiva MM, Sales MH, Salgado MPG, Vasconcelos R, Galano S, Mesquita VV & Azevedo T (2020) Reconstructing three decades of land use and land cover changes in Brazilian biomes with landsat archive and earth engine. Remote Sensing 12: 10.3390/rs12172735.
• Taylor NP & Albuquerque-Lima S (2020) Annotated checklist of Cactaceae in the Catimbau National Park, Pernambuco, Brazil. Bradleya 38: 231-246.
• Taylor NP, Albuquerque-Lima S, Telhe M & Zappi DC (2022) Further additions and corrections to Cacti of Eastern Brazil. Bradleya 40: 61-92.
• Taylor NP, Stuppy W & Barthlott W (2002) Realignment and revision of the Opuntioideae of Eastern Brazil. In: Hunt D & Taylor NP (eds.) Studies in the Opuntioideae (Cactaceae). Succulent Plant Research 6: 99-132.
• Taylor NP & Zappi DC (2004) Cacti of Eastern Brazil. Royal Botanic Gardens Kew, Richmond. 499p.
• Taylor NP, Zappi DC, Olsthoorn G, Lowry M & Pereira FO (2023) Additions and corrections to Cacti of Eastern Brazil (3). Bradleya 41: 17-138.
• Tetra Mais Consultoria (2021) Estudo de impacto ambiental (EIA): projeto Santa Quitéria. Volume II-B. Available at <Available at https://consorciosantaquiteria.com.br/eia-rima/ >. Access on 6 February 2024.
  » https://consorciosantaquiteria.com.br/eia-rima/
• Tetra Mais Consultoria (2022) Relatório de impacto ambiental (RIMA): projeto Santa Quitéria. Available at <Available at https://consorciosantaquiteria.com.br/eia-rima/ >. Access on 6 February 2024.
  » https://consorciosantaquiteria.com.br/eia-rima/
• Vieira AT, Magalhães MF & Silva MVC (2017) Uso da terra como facilitador da degradação ambiental no município de Santa Quitéria, Ceará. Revista Brasileira de Geografia Física 10: 1329-1345.

• 1
  A single collection was found with a higher elevation: Menezes 268 (EAC 48810), with 978 m.

Edited by

Area Editor:

Dra. Cassia Sakuragui

Publication Dates

• Publication in this collection
  22 July 2024
• Date of issue
  2024

History

• Received
  12 Dec 2023
• Accepted
  06 Mar 2024