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Better Alone? a Demographic Case Study of the Hemiparasite Castilleja Tenuiflora (Orobanchaceae): a First Approximation

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Better Alone? a Demographic Case Study of the Hemiparasite Castilleja Tenuiflora (Orobanchaceae): a First Approximation Received: 18 March 2020 Revised: 17 August 2020 Accepted: 3 November 2020 DOI: 10.1002/1438-390X.12076 ORIGINAL ARTICLE Better alone? A demographic case study of the hemiparasite Castilleja tenuiflora (Orobanchaceae): A first approximation Luisa A. Granados-Hernández1 | Irene Pisanty1 | José Raventós2 | Judith Márquez-Guzmán3 | María C. Mandujano4 1Departamento de Ecología y Recursos Naturales, Facultad de Ciencias, Abstract Universidad Nacional Autónoma de Castilleja tenuiflora is a facultative root hemiparasitic plant that has colonized México, Mexico City, Mexico a disturbed lava field in central Mexico. To determine the effects of 2 Departamento de Ecología, Universidad hemiparasitism on the population dynamics of the parasite, we identified a set de Alicante, Alicante, Spain of potential hosts and quantified their effects on the vital rates of C. tenuiflora 3Departamento de Biología Comparada, Facultad de Ciencias, Universidad during 2016–2018. Connections between the roots of the hemiparasite and the Nacional Autónoma de México, Mexico hosts were confirmed with a scanning electron microscope. Annual matrices City, Mexico considering two conditions (with and without potential hosts) were built based 4Departamento de Ecología de la λ Biodiversidad, Instituto de Ecología, on vital rates for each year, and annual stochastic finite rate growth rates ( s) Universidad Nacional Autónoma de were calculated. Plants produced more reproductive structures with hosts than México, Mexico City, Mexico without hosts. A Life Table Response Experiment (LTRE) was performed to Correspondence compare the contributions of vital rates between conditions. We identified Irene Pisanty, Departamento de Ecología 19 species of potential hosts for this generalist hemiparasite. Stochastic lambda y Recursos Naturales, Facultad de with hosts λ = 1.02 (CI = 0.9999, 1.1) tended to be higher than without them Ciencias, Universidad Nacional s Autónoma de México, Av. Universidad λs = 0.9503 (CI = 0.9055, 0.9981). The highest elasticity values correspond to 3000, Cd. Universitaria, Coyoacán, 04510 survival. LTRE indicated that the most important parameters are survival and Mexico City, Mexico. Email: [email protected] fecundity; the total contribution of fecundity (0.0192) to the difference in growth was three times lower than that of survival (0.0603). Piqueria trinervia Funding information was the most abundant host, and C. tenuiflora had a higher lambda with it Universidad Nacional Autónoma de México; Programa de Apoyo a Estudiantes than with other species. Individuals can grow alone, but hosts can have a posi- de Posgrado; Consejo Nacional de Ciencia tive effect on the vital parameters of C. tenuiflora and on λ. y Tecnología, Grant/Award Number: 432340 KEYWORDS Castilleja tenuiflora, elasticity, hemiparasitism, LTRE, vital rates 1 | INTRODUCTION nutrients from the vascular system of their hosts through structures known as haustoria (Lambers, Stuart Chapin Parasitic plants occur in all climatic zones and on all III, & Pons, 1998; Salcedo-Morales, Jiménez-Aparicio, continents except Antarctica (Hartley et al., 2015; Press & Cruz-Sosa, & Trejo-Tapia, 2014; Watkinson & Gibson, Phoenix, 2005) and are often considered key species in 1987). Parasitic plants can be holo or hemiparasites, with their community (Matthies, 2017). Parasitism is found in about 90% of the species belonging to the latter (Joel about 1% of all seed plants, in 270–275 genera, and 60% et al., 2013). Hemiparasites extract water and mineral of all parasitic plants are root parasites (Joel, Gressel, & salts from their hosts but, unlike the holoparasites, they Musselman, 2013; Thorne, 2002). Parasitic plants obtain are photosynthetically self-sufficient (Douglas, 1973; Population Ecology. 2021;1–13. wileyonlinelibrary.com/journal/pope © 2021 The Society of Population Ecology 1 2 GRANADOS-HERNANDEZ ET AL. Salcedo-Morales et al., 2014; Watkinson & conferta have been reported as hosts of C. tenuiflora in Gibson, 1987). another location (Montes-Hernández, Sandoval- Most parasitic plants are generalists, that is, they do Zapotitla, Bermúdez-Torres, Trejo-Espino, & Trejo- not parasitize a specific host (Marquardt & Tapia, 2019; Montes-Hernández, Sandoval-Zapotitla, Pennings, 2011; Pennings & Callaway, 2002), and one Bermúndez-Torres, & Trejo-Tapia, 2015), and the connec- individual can infest several hosts of different species at tion between its roots has been proved at a micromorpho- the same time (Fibich, Leps, & Berec, 2010; Pennings & logical level, which allowed the identification of small Callaway, 2002). However, not all plant species are haustoria (Montes-Hernández et al., 2019). C. tenuiflora potential hosts for parasitic plants (Cameron & is a secondary species, common in successional processes Seel, 2007; Cameron, White, & Antonovics, 2009). The following natural or anthropogenic disturbance most frequent families of potential hosts for all parasitic (Rzedowski & Rzedowski, 2001). In this study, we ana- plants include Poaceae, Rosaceae, Fabaceae, Labiatae, lyze a population that has colonized a lava field of the Asteraceae and Cyperaceae (Pennings & Simpson, 2008; Ecological Park of Mexico City (PECM, by its Spanish Weber, 1976). acronym), a natural area embedded in this huge metro- The performance of parasitic plants is affected by host politan area (Ezcurra, 2003; Pisanty, Mazari, & species in different ways (Borowicz, Walder, & Ezcurra, 2009; Romero & Velázquez, 1999; Siebe, Armstrong, 2019; Pennings & Callaway, 2002). For exam- Mendoza-Hernández, Juárez-Orozco, Vázquéz-Selem, & ple, the parasitic species Triphysaria pusilla and Cram, 2016; Soto, Mazarí, & Bojórquez, 2000). C. T. eriantla (Orobanchaceae) produce more fruits when tenuiflora's success as a colonizer in these sites, which are they infest members of the Poaceae family than when variable in space and time, is probably related to the ben- they parasitize Lupinus nanus (Fabaceae) or Hypochaeris efits it obtains from parasitizing the roots of its hosts glabra (Asteraceae) (Marvier, 1998). Some parasitic plants (Matthies, 1995, 1997). In this paper, we identified the can obtain collateral benefits from their hosts, for exam- potential hosts of C. tenuiflora in the disturbed lava field ple, defense against herbivory because they acquire the in the PECM of Mexico City, in central Mexico, and ana- secondary metabolites that protect the host, as has been lyzed the population dynamics of the species with and observed in the hemiparasite Castilleja indivisa without hosts through a comparative demographic study. (Adler, 2003). Moreover, Marquardt and Pennings (2011) Our hypothesis is that C. tenuiflora will perform better in observed that the holoparasite Cuscuta indecora the presence of hosts and that this improvement will be (Convolvulaceae) produced more final biomass when its evident in its vital rates, population dynamics and popu- host Iva frutescens (Asteraceae) is more abundant. lation growth rate. We studied the effects of hosts on the Very little is known of the demographic effects of vital parameters (growth, survival and reproduction) of hosts on the populations of plant root parasites and on this hemiparasite using a population matrix approach their vital parameters, with few exceptions (Borowicz and a Life Table Response Experiment (LTRE). We aim et al., 2019; Menges, 1990). In general, facultative hem- to (a) identify the potential hosts of C. tenuiflora in the iparasitic plants grow and reproduce better in presence of disturbed scrub of the PECM, (b) compare the stochastic hosts (Marvier, 1998; Matthies, 2002; Yong-Quan, Kai- population growth rates (λs) with and without hosts and Yun, Ai-Rong, Xiao-Jian, & Zhang, 2010), so host abun- (c) identify the contributions of vital rates to population dance and availability can influence population size and growth rates on the different host conditions and years dynamics of these parasites (Fibich et al., 2010; we considered. Matthies, 2002; Press & Phoenix, 2005; Yong-Quan et al., 2010). Matthies (1995) showed that growth of Rhinanthus serotinus (Orobanchaceae) increased in the 2 | METHODS presence of its host (Medicago sativa) compared to when growing alone. He also reported that biomass and sur- 2.1 | Study area vival of Castilleja integra (Orobanchaceae) were greater with a host, while both parameters decreased when the PECM is located south of Mexico City (191503200 N and parasite grew alone. Furthermore, C. chromosa has been 991201.900 W) on the Ajusco Ridge, between 2,400 and found to perform better with a host (Matthies, 1997). 2,900 m above sea level (Mendoza-Hernández, Orozco- Castilleja tenuiflora (Orobanchaceae) is a facultative Segovia, Meave, Valverde, & Martínez-Ramos, 2013). The root hemiparasitic species (Heckard, 1962; Alvarado- park covers 727 ha and contains part of the lava forma- Cárdenas, 2008). It is native to Mexico and grows in dis- tion known as Pedregal del Xitle, a large lava field pro- turbed locations, flowering all year round (Rzedowski & duced by an eruption of the Xitle volcano approximately Rzedowski, 2001). Lupinus montanus and Baccharis 1,600 years ago (Cano-Santana et al., 2006). The climate GRANADOS-HERNANDEZ ET AL. 3 is temperate, sub-humid, with a summer rainy season, scrubs (Alvarado-Cárdenas, 2008; Rzedowski & and a cold winter with occasional rains. Spring is typi- Rzedowski, 2001). cally dry and hot. Mean annual temperature is 11C and The plant ranges from 30 cm to 1 m in height, the annual rainfall is 1,000 mm (Ajusco Meteorology
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