Communications in Plant Sciences, vol 9, p. 36-40, 2019 (2019006)
Flowering of the endemic cactus Tacinga palmadora: a relation between floral production and age
Ayslan Trindade Lima*, Adryanne Arcanjo Costa and Marcos Vinícius Meiado
*Correspondence to: firstname.lastname@example.org
Abstract: Plant age is a factor that influences production of flowers in some species. In some cacti, new cladodes and flowers buds grow from areolar meristems located in the cladodes. It is possible to determine the age of the cactus by counting the maximum number of cladodes present in a branch. Among the species of cacti that present annual vegetative growth determined by the climatic seasons is the species Tacinga palmadora. The objective of this study was to determine the initial reproductive age of this species and to evaluate the relation between the age of T. palmadora individuals and the number of flowers produced. The study was conducted at the Grota do Angico Natural Monument, in the municipality of Poço Redondo in Sergipe state in September 2017. Two hundred and seventeen individuals of T. palmadora were analyzed in the study area. In each individual, where counted the number of flowers and the number of cladodes present in the largest branch from the base, thus estimating the age of each individual. A positive and significant relation was observed between average number of flowers produced and age of individuals of T. palmadora in the evaluated population.
Tacinga palmadora presents a greater number of flowers in older individuals due to the greater number of cladodes.
Keywords: Cladodes, Plant reproduction, Reproductive age, Quipá, Caatinga.
Flowering is a crucial event in plants life cycle and favorable conditions are required to maximize reproductive success and thus the survival of species in their natural environment (Capovilla et al. 2015). Conversion of vegetative meristems into reproductive structures is one of the most complex events in this cycle. Floral induction is related to events that signal to plant the alteration of its development program and, consequently, vegetative meristems are restructured to produce floral primordium (Yant et al. 2010; Wellmer and Riechmann 2010). Inducing stimulus for this reproductive event may be related to plant endogenous conditions or to abiotic conditions of the ecosystem in which plants are established (Huijser and Schmid 2011). Environmental stimulus induces flowering of older plants, whereas younger plants of the same species remain vegetative under the same conditions (Bergonzi et al. 2013).
Light is an abiotic condition that is related to flowering of many species, where days length and light quality are a stimulating factor for flowering seasonality (Searle and Coupland 2004; Song et al. 2013; Fernández et al. 2016; Sams et al. 2016). Temperature is also an important environmental stimulus that contributes to floral production of many plant species (Capovilla et al. 2015; Seaton et al. 2015). Another factor that may influence plants reproduction is plant age (Hanzawa and Kalisz 1993; Ehlers and Olesen, 2004).
In most of cacti species, new cladodes and flower buds grow from areolar meristems located in cladodes (Bowers 1996); however, this meristem only differentiates once (Gibson and Nobel 1986). Thus, Bowers (1996) pointed out that for some cacti, reproductive success of a year depends on vegetative growth in rainy period of the previous year. Among the species of cacti that present annual vegetative growth determined by climatic seasons is Tacinga palmadora (Britton & Rose) N.P. Taylor & Stuppy. T. palmadora is a species that belongs to the family Cactaceae and the subfamily Opuntioideae (Taylor and Zappi 2004). Endemic to Caatinga, a Tropical Dry Forest, T. palmadora is distributed throughout the Northeastern region of Brazil, except for Maranhão state, and is popularly known as quipá-de-espinho or palmatória (Taylor and Zappi 2004; Zappi et al. 2015). This species shows shrub habit and can reach 2 m in height. It occurs on sandy substrates or on rocks, in areas of 200 to 1,020 m of altitude (Zappi et al. 2015). In contrast to most Caatinga cacti, T. palmadora produces flowers during the dry season and its flowers, with daytime anthesis, are pollinated by hummingbirds (Locatelli and Machado 1999). Flowers grow from cladodes areolar meristem and are tubular with red perianth and floral tube with glochids (Locatelli and Machado 1999). At each rainy season, new cladodes are produced from areolar meristem present in the cladodes formed in the previous rainy seasons (Meiado 2012). In addition, size and number of cladodes in the main branch may be related to the climatic conditions of growing season (Meiado 2012). Thus, it is possible to determine cactus age by counting the maximum number of cladodes present in a branch.
This study aims determine initial reproductive age of T. palmadora and to evaluate the relation between individuals age and the number of flowers produced by these plants, testing the hypothesis that the number of flowers is positively related to the age of this cactus.
MATERIAL AND METHODS
T. palmadora is a species that belongs to the family Cactaceae and the subfamily Opuntioideae (Taylor and Zappi, 2004). Endemic to Caatinga, a Tropical Dry Forest, T. palmadora is distributed throughout the Northeastern region of Brazil, except for Maranhão state, and is popularly known as quipá-de-espinho or palmatória (Taylor and Zappi 2004; Zappi et al. 2015). This species shows shrub habit and can reach 2 m in height. It occurs on sandy substrates or on rocks, in areas of 200 to 1,020 m of altitude (Zappi et al. 2015). In contrast to most Caatinga cacti, T. palmadora produces flowers during the dry season and its flowers, with daytime anthesis, are pollinated by hummingbirds (Locatelli and Machado 1999). Flowers grow from cladodes areolar meristem and are tubular with red perianth and floral tube with glochids (Locatelli and Machado 1999).
The study was conducted at the Grota do Angico Natural Monument, in the municipality of Poço Redondo in Sergipe state in September 2017. According to Köppen and Geiger classification, this region climate is BSh. The annual rainfall is low, with an average of 548 mm and the average annual temperature is 25 ºC (Climate Data 2017). In the study area, we analyzed 217 individuals of T. palmadora and all these plants had flowers (Figure 1). In each individual, where counted the number of flowers and the number of cladodes present in the largest branch from the base, thus estimating the age of each individual (Meiado 2012). Individuals were grouped into age categories and an average number of flowers per age was calculated. Subsequently, to analyze the relation between age of the individuals and floral production, a linear regression was performed on STATISTICA® 13 software with α = 5% (Statsoft 2016).
Figure 1. A: Tacinga palmadora (Britton & Rose) N.P. Taylor & Stuppy (Cactaceae) during flowering period in Grota do Angico Natural Monument, in the municipality of Poço Redondo in Sergipe state. B: T. palmadora cladode and flowers. Photo: Ayslan T. Lima.
RESULTS AND DISCUSSION
In T. palmadora population evaluated, individuals with flowers were present in an age range of 8 to 31 years of age (Figure 2). In each age category, we observed an average of 12 individuals, ranging from 1 to 29 individuals by age category. The highest frequency of individuals with flowers was observed in the group of 12 to 16 years of age (Figure 3). A positive and significant relation was observed between average number of flowers produced and age of individuals of T. palmadora in the evaluated population (p < 0.0001) (Figure 2). These results corroborate the hypothesis that flowers number is positively related to cactus age.
Figure 2. Frequency (%) of individuals of Tacinga palmadora (Britton & Rose) N.P. Taylor & Stuppy (Cactaceae) with flowers in relation to age (years).
Figure 3. Average number of flowers per individual of Tacinga palmadora (Britton & Rose) N.P. Taylor & Stuppy (Cactaceae) in relation to age (years).
In spite of older individuals showed the highest number of flowers, they appeared less frequently in the evaluated population, a large number of specimens producing flowers were found in the age range of 12 to 16 years. Since this is the most frequent age group, individuals that present age inserted in this range are those that contribute most with the genetic variability of this population. This contribution is maximized by the presence of pollinators that visit different individuals during flowering period. Locatelli and Machado (1999) pointed out that the hummingbird Chlorostilbon lucidus (Shaw 1812) (Apodiformes: Trochilidae) is the main pollinator of T. palmadora and Ruiz-Esparza et al. (2011) pointed out that C. lucidus is distributed in the studied population area. The low number of plants in the largest age categories is justified by the fact that the area where we developed this study was recently assigned to creation of a conservation unit. Previously, this area was a private property used as pasture and monoculture planting area. After creation of the conservation unit, the area was expropriated and assigned to State of Sergipe government which develops actions for natural regeneration of native vegetation in the region, such as protection and non-exploitation of natural resources (Semarh 2017). These actions have provided the reappearance of several species over the last decades and the reestablishment of native populations such as T. palmadora.
Evaluations carried out by Meiado (2012) about the structuring of three populations of T. palmadora in different areas of Caatinga showed that individuals started reproductive phase in the age group of seven to eight years of age. In the present study, eight years was also the minimum age of individuals with flowers. Thus, having the adult reproductive phase started between seventh and eighth years may be a pattern in T. palmadora, even among populations established in different areas of Caatinga, indicating that this is the minimum age range where this species reallocates its energy also for development of reproductive structures. Thus, the results that we observe in this study reinforce the need for the creation of conservation units in Caatinga and the effective protection of these areas for native species conservation, reestablishment of their populations and the beginning of their reproductive process (Siqueira Filho et al. 2012). Some species, such as T. palmadora, will establish themselves in this protected area, and in a few years will begin their reproductive process, being keystone species for the natural regeneration of the environment by providing the attraction of pollinating animals and seed dispersers that will bring with it diaspores of other native species (Hale and Koprowski 2018).
As in the present study with Cactaceae, a positive relation between number of flowers produced and age of the individuals was also observed in Corydalis intermedia (L.) Mérat (Papaveraceae) (Ehlers and Olesen 2004) and Trillium grandiflorum (Michx.) Salisb. (Melanthiaceae) (Hanzwa and Kalisz 1993). Rojas-Sandoval and Meléndez-Ackerman (2011) observed that reproductive output is positively correlated with plant size in Harrisia portoricensis Britt. (Cactaceae). According to the authors, this positive correlation is justified by the greater number of branches and areolas present in these plants, which allows a greater number of flowers and a higher production of fruits and seeds consequently. Ehlers and Olesen (2004) pointed out that positive relation between flower production and age of individuals is related to the change in strategy throughout plant life cycle, where, over time, there is a greater allocation of energy to floral production after reach reproductive age.
In addition to the fact that older individuals have a greater number of branches and these branches provide a higher production of flowers as we observed in this study, these larger and more branched individuals also have an increase in the photosynthetic surface, which will increase photoassimilates production and storage by the plant. Consequently, these plants will have more reproductive resources and can produce a greater number of flowers and maximize their seed production (Drezner 2014; Inglese et al. 2017). Drezner (2014) reported that the greater number of branches in Carnegiea gigantea (Engelm.) Britton & Rose (Cactaceae) not only increases photosynthetic surface of plants, but also its reproductive potential, since new branches offer more areolar meristems, from where flowers are produced. This relation can also be applied to T. palmadora, since flowers and new cladodes grow from areolar meristems (Locatelli and Machado 1999). Thus, the results demonstrated that T. palmadora presents a greater number of flowers in older individuals due to the greater number of cladodes.
Authors are thankful to the Coordination for the Improvement of Higher Education Personnel (CAPES) and the Foundation of Support to Research and Technological Innovation of the State of Sergipe (FAPITEC / SE) for financial support. This study was carried out as part of the activities of the Field Course of Ecology of the Caatinga, promoted by the Post-Graduation Program in Ecology and Conservation of the Federal University of Sergipe.
- Bergonzi S et al. 2013. Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science 340:1094-1097.
- Bowers JE. 1996. More flowers or new cladodes? Environmental correlates and biological Consequences of sexual reproduction in a Sonoran desert prickly pear cactus, Opuntia engelmannii. Bulletin of the Torrey Botanical Club 123:34-40.
- Capovilla G et al. 2015. Control of flowering by ambient temperature. Journal of Experimental Botany 66: 59-69.
- Climate Data. 2017. Dados climáticos para cidades mundiais. Available at https://pt.climate-data.org. Accessed on Oct. 18, 2017.
- Drezner TD. 2014. Regional branching relationships in Carnegiea gigantea, a keystone cactus. Western North American Naturalist 72:155-161.
- Ehlers BK and Olesen JM. 2004. Flower production in relation to individual plant age and leaf production among different patches of Corydalis intermedia. Plant Ecology 174:71-78.
- Fernández V et al. 2016. Photoperiodic and thermosensory pathways interact through CONSTANS to promote flowering at high temperature under short days. The Plant Journal 86: 426-440.
- Gibson AC and Nobel PS. 1986. The cactus primer. Harvard University Press: Cambridge.
- Hale SL and Koprowski JL. 2018. Ecosystem-level effects of keystone species reintroduction: a literature review. Restoration Ecology 26:439-445.
- Hanzawa FM and Kalisz S. 1993. The relationship between age, size, and reproduction in Trilliu grandiflorum (Liliaceae). American Journal of Botany 80:405-410.
- Huijser P and Schmid M. 2011. The control of developmental phase transitions in plants. Development 138:4117-4129.
- Inglese P et al. 2017. Ecophysiology and reproductive biology of cultivated cacti. In: Inglese P et al. (Eds.). Crop ecology, cultivation and uses of cactus pear. FAO: Rome. pp.29-42.
- Locatelli E and Machado ICS. 1999. Comparative study of the floral biology of two ornithophilous species of Cactaceae: Melocactus zehntneri and Opuntia palmadora. Bradleya 17:75-85.
- 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.
- Rojas-Sandoval J and Meléndez-Ackerman M. 2011. Reproductive phenology of the Caribbean cactus Harrisia portoricensis: rainfall and temperature associations. Botany 89:861-871.
- Ruiz-Esparza J et al. 2011. Birds of the Grota do Angico Natural Monument in the semi-arid Caatinga scrublands of northeastern Brazil. Biota Neotropica 11:1-8.
- Sams CE et al. 2016. Light quality impacts on growth, flowering, mineral uptake and petal pigmentation of marigold. Acta Horticulturae 1134:139-146.
- Searle I and Coupland G. 2004. Induction of flowering by seasonal changes in photoperiod. The Embo Journal 23: 1217-1222.
- Seaton DD et al. 2015. Linked circadian outputs control elongation growth and flowering in response to photoperiod and temperature. Molecular Systems Biology 11:1-19.
- Semarh 2017. Plano de Manejo do Monumento Natural Grota do Angico. Secretaria do Estado do Meio Ambiente e dos Recursos Hídricos. Available at https://www.semarh.se.gov.br/wp-content/uploads/2017/02/PlanodeManejoMONA.pdf. Accessed on Jul. 10, 2019.
- Siqueira Filho JA et al. 2012. Unidades de Conservação na Caatinga: a realidade da conservação de um ecossistema semiárido no Nordeste do Brasil. In: Lima GS et al. (Org.). Gestão, Pesquisa e Conservação em Áreas Protegidas. Universidade Federal de Viçosa: Viçosa. pp.171-191.
- Song YH et al. 2013. Flowering time regulation: photoperiod- and temperature-sensing in leaves. Trends in Plant Science 18:575-583.
- Statsoft. 2016. STATISTICA 13. StatSoft South America. Available at http://www.statsoft.com.br. Accessed on Oct. 18, 2017.
- Taylor N and Zappi D. 2004. Cacti of Eastern Brazil. Kew: The Royal Botanic Gardens.
- Wellmer F and Riechmann JL. 2010. Gene networks controlling the initiation of flower development. Trends in genetics 26:519-527.
- Yant L et al. 2010. Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. The Plant Cell 22: 2156-2170.
- Zappi et al. 2015. Cactaceae. In: Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro.