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;

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 Sta- stem is erect and branched with sessile leaves, slightly tion). Precipitation patterns determine the well-defined auriculated at the base, arranged in a spiral (linear-lance- dry (November–April) and rainy (May–October) seasons. olate) and measuring 1–4.5 cm in length. The apex is hir- In the early 1980s, the lower part of PECM suffered sute and acute or obtuse, and it is red or orange with severe disturbances from urban sprawling that caused dentate lobes. The flowers are arranged in racemose the removal of plants and the alteration of a large part of inflorescences, with red or slightly orange bracts; it has a the vegetation and the basaltic substrate of a primary calyx of 2–3 cm in length; the corolla is yellow or green scrub, producing different degrees of disturbance in its and reaches up to 4.5 cm in length. Fruits are capsular remnants (Bonfil, Rodríguez, & Peña, 2000). Following and produce brown ellipsoidal seeds 1.8 mm long its designation as a protected area, a recolonization pro- (Rzedowski & Rzedowski, 2001). cess was naturally initiated in the lava field by secondary, early successional species, including C. tenuiflora (Mendoza-Hernández et al., 2013; Soberón, De la Maza, 2.3 | Identification of potential hosts Hernández, Bonfil, & Careaga, 1991; Soberón, De la Meza, & Jiménez, 1991), that only grows in disturbed Under field conditions, hosts of other parasitic plants sites and has been successful on the lava fields affected have usually been identified according to the root length by the above-mentioned disturbance (Mendoza- of the parasitic plant (Gibson & Watkinson, 1992; Hernández et al., 2013). Montes-Hernández et al., 2015; Suetsugu, Kawakita, & Plant communities in the park have a patchy distribu- Kato, 2008). Following these authors, and due to the lack tion due to the lava flow and include forests of Quercus of information about the rhizosphere and its under- spp., Pinus-Quercus and Abies spp., as well as a xerophi- ground structure in the lava field, 26 individuals of lous scrub, developed on the basaltic substrate formed as C. tenuiflora were randomly collected in the rainy season a result of the above-mentioned eruption of the Xitle vol- of 2016 and the length of their roots was measured. The cano (González-Hidalgo, 1996; Mendoza-Hernández collected individuals had different numbers of branches et al., 2013; Soberón, De la Maza, et al., 1991). This study and different heights, and some had flowers and/or fruits. took place in a disturbed part of this scrub, that has an The longest root of each of the collected individuals was irregular substrate. To describe the plant community and measured, and an average root length was calculated and the characteristics the potential hosts have in it, in used in this first approach as a criterion to determine the October 2016 (end of the rainy season and period of max- maximum distance to potential hosts, assuming that imum richness in the PECM, Alcantar & Pisanty, C. tenuiflora could not reach the roots of plants placed unpublished data), 50 1 × 1 m plots were randomly further away. The length of the roots of potential hosts placed along three parallel transects of 50 × 2 m each, was measured when samples were taken for scanning, in oriented from North to South. In each of the plots, indi- order to avoid a major disturbance of the site. Except for vidual plant cover of all the plants was measured, and Opuntia robusta, which occasionally showed roots longer species composition, cover, frequency and abundance than 50 cm, all other potential hosts have radicular sys- were obtained (Table S1). In the plant community, the tems that either grow almost without ramifications, like most abundant plant species are Piqueria trinervia P. roseus, or grow more horizontally for a short distance, (Asteraceae), C. tenuiflora (Orobanchaceae), Manrrubio similar to or smaller than the roots of C. tenuiflora, like spp. (Lamiaceae), Penstemon roseus (Plantaginaceae), the rhizome of C. kalfussii (L. Granados-Hernández & Cheilanthes kaulfussii and C. bonariensis (Pteridaceae) I. Pisanty, pers. obs.). (Table S1). Based on data obtained from the average root length of C. tenuiflora (18 ± 10 cm, x ± SD), circles of 30 cm in diameter were placed around 250 individuals marked 2.2 | Study species along the transects, in order to identify which of these plants had a potential host and which did not (with and C. tenuiflora Benth. is an herbaceous, perennial, fac- without neighbors within the circle, respectively). All ultative hemiparasitic species of the Orobanchaceae individuals of any species within these circles were con- family (Alvarado-Cárdenas, 2008). It is distributed sidered as potential hosts. from northern Mexico to Central America, growing in To verify the parasite–host interaction, we identified disturbed areas of Quercus forests and xerophilous the connection between C. tenuiflora and some of its 4 GRANADOS-HERNANDEZ ET AL. potential hosts using first a stereoscopic microscope and recorded this condition without measuring height. We then a scanning electron microscope (JSM 5310 LV also quantified the production of fruits to calculate the JEOL). For this, we collected five individuals of fecundity. Mortality of individuals with and without C. tenuiflora, one of which had no neighboring potential hosts was recorded in both transects on an annual basis. hosts (control) while the rest did have them. The col- Then, we defined six categories: (a) seeds that germinated lected samples were washed with water. Once the roots in controlled chambers, (b) seedlings in the experimental were clean, segments with a physical connection between boxes and individuals of 1–20.9 cm in height, C. tenuiflora and a host were identified with a stereo- (c) individuals of 21–35.9 cm in height, (d) individuals of scopic microscope and selected for further processing. 36–49.9 in height, (e) individuals >50 cm in height and Small segments including the connections were prepared (f) individuals with dry aerial tissue. for observation under the microscope by fixing in FAA We defined the probability of transition of seeds to cat- (formaldehyde, acetic acid, ethanol and water, 2:1:10:7) egory 2 using the percentage of seeds that germinated for 48 hr. Afterwards, the samples were rinsed for 1 hr in under natural and controlled conditions in a previous water and then dehydrated for a further hour in different experiment (Granados-Hernández, 2015), in which 4,750 concentrations of ethyl alcohol (30, 50, 70, 85, 96 and seeds of C. tenuiflora were collected in the study area in 100%). The samples were then dehydrated to a critical 2013. To obtain the germination percentage under natural point in a CPD-30 BAL-tec desiccator and bathed in gold conditions, 50 seeds were sown on soil collected in situ in in a Desk-II ionizer and observed under the scanning each of 95 field experimental boxes (8x8x8 cm) in the electron microscope (Goldstein et al., 2003). study area. The number of germinated seeds was recorded monthly, and seeds that did not germinate were recovered and placed in petri dishes of 8.8 cm in diameter with Agar 2.4 | Demographic analysis (10%) in germination chambers (photoperiod 12/12, temperature 25–35C) with an equal number of control seeds. 2.4.1 | Matrix construction Germination of both the recovered and control seeds was recorded daily. Recruitment was quantified by counting We constructed four annual population projection matri- the new individuals in the study site. The fecundity value ces, each with six categories, for C. tenuiflora, two of for each matrix was obtained as shown in Equation (1). them for the period 2016–2017, one with hosts and the other without hosts and other two for the period SF × FC × SV × PG f = , ð1Þ 2017–2018, again one of them with hosts and the other n without them. To illustrate their transitions graphically, we built a life cycle diagram with the values of the aver- where f = fecundity, SF = average number of seeds per age matrix for plants with and without potential hosts. fruit, FC = number of fruits in each category, SV = seed We also built matrices with P. trinervia, P. roseus, viability, PG = percentage of germination and n = total Eupatorium glabratum and C. kaulfussii; species with number of individuals in each category. which C. tenuiflora was frequently associated in both Seed viability (SV) of C. tenuiflora was determined by years. All matrices were calculated based on vital rates analyzing a sample of 100 randomly selected seeds, col- (Figure 1 and Tables S2–S5). lected in the PECM, with X-rays (Ultrafocus Digital Radi- We measured plant height (cm) for a period of 2 years ography System, Tucson, AZ). Percentage of germination (June 2016 to June 2018) in all the individuals (250) along (PG) was obtained with the germination data under natu- the transects for C. tenuiflora with and without potential ral cFonditions and from the recovered seeds that germi- hosts. When only dry aerial tissue was present, we nated in the germination chambers.

FIGURE 1 Symbolic matrix of Castilleja tenuiflora. 1: Seeds that S1(1-G21-G31-G41 G51-G61) S2F2 S3F3 S4F4 S5F5 S6F6 germinated in growth chambers, 2: S1G21 S2(1-G32-G42-G52-G62) S3R23 S4R24 S5R25 S6R26 seedlings in the experimental boxes and S1G31 S2G32 S3(1-G43-G53-G63-R23) S4R34 S5R35 S5R36 individuals of 1–20.9 cm in height, 3:

S1G41 S2G42 S3G43 S3(1-G54-G64-G24-R34) S5R45 S6R46 individuals of 21–35.9 cm in height, 4: – S1G51 S2G52 S3G53 S4G54 S5(1-G65-R45-R35-R25) S6R56 individuals of 36 49.9 in height, 5: individuals >50 cm in height and 6: S1G61 S2G62 S3G63 S4G64 S5G65 S6(1-R56-R46-R36-R26) individuals with dry aerial tissue. S: survival, F: fecundity, G: growth, R: retrogression GRANADOS-HERNANDEZ ET AL. 5

2.4.2 | Estimation of stochastic chose mean annual with host 2016–2018 matrix A(h) as population growth the reference matrix, as most individuals of C. tenuiflora were found with potential hosts. Due to the diverse microenvironmental conditions Using the first term of the expanding λ as a function

C. tenuiflora canfaceinthePECM,weperformedstochastic of the aij used, we predicted the population growth rate simulations to estimate the population growth rate with and of C. tenuiflora with a host (A(h)) with Equation (3) without hosts. We also performed stochastic simulations (Caswell, 2001): with the species with which C. tenuiflora was frequently associated (P. trinervia, P. roseus, E. glabratum and X ∂λ λðÞwh ≈ λðÞh ðÞwh − ðÞh ð Þ C. kaulfussii). In all the above cases, we followed the aij aij , 3 ∂aij i,j 1ðÞAðÞwh + AðÞh approach of Ellis and Crone (2013) to perform replicate sim- 2 ulations of stochastic dynamics for the period 2016–2018 with and without hosts. We simulated 10,000 population tra- where h = with hosts and wh = without hosts; the terms jectories using equal probability selection at each time step, in the summation are the contribution of the aij effect of as well as the 95% confidence limits of this estimate. As a treatment h (with hosts) on population growth. first approach, we used equal numbers of individuals in each stage. We used a burn-in period of 500 years on the projec- ted stochastic population growth to remove the effect of this 3 | RESULTS arbitrary initial condition (Caswell, 2001; Ellis & Crone, 2013). All simulations were performed in MATLAB 3.1 | Identification of potential hosts (version 9.6.0.1114505 (2019A) Update 2). Most C. tenuiflora individuals had potential hosts (Figure 2). We found that C. tenuiflora can grow with one 2.4.3 | Elasticity of vital rates or more potential hosts of different species (Figure 2b). Frequent potential hosts of C. tenuiflora were P. trinervia

We calculated the sensitivities of vital rates, Srk ,following (42%), C. kaulfussii (18%), E. glabratum (12%) and the approach given by Morris and Doak (2002). To do this, P. roseus (11%) (Figure 2c), but less abundant species we summed up the derivatives of each vital rate with respect could also be potential hosts and are shown in Table S6. to aij (matrix elements) times the derivatives of aij with The micromorphology analysis of C. tenuiflora roots respect to rk (vital rates) for all the matrix elements without showed they are characterized by rectangular, well- hosts and with P. trinervia, P. roseus, E. glabratum and C. organized cells in the epidermis (Figure S1). This charac- kaulfussii. Then, we calculated the elasticities of vital rates, teristic was used to identify the presence of roots of the

En, as a proportional change in λ resulting from proportional hemiparasite entering the root tissue of its potential hosts. changes in rk (Equation (2)) (Morris & Doak, 2002) The connection between the hemiparasite and its hosts involves the thin and fragile lateral roots (secondary, ter- Xs Xs ∂λ ∂a Xs Xs ∂a tiary and quaternary), so it can be difficult to observe in S = 1 ij = S ij rk ∂a ∂r ij ∂ar field conditions. Nevertheless, it was possible to identify i =1 j =1 ij k i =1 j =1 k ð2Þ connections between the roots of C. tenuiflora and those of rk : Erk = Srk Verbesina sp. (Figure 3a,b), P. trinervia (Figure 3c) and λ1 with rhizomes of C. kaulfussii (Figure 3d).

3.2 | Effect of hosts on population 2.4.4 | Matrix comparison: LTRE dynamics of C. tenuiflora

We used a linear one-way fixed factorial design to study 3.2.1 | Life cycle the demographic consequences for C. tenuiflora growing with and without hosts, following the approach of The life cycle of C. tenuiflora with and without hosts is Caswell (2001). In the LTRE analyses, the mean annual shown in Figure 4. Almost all transitions (growth, sur- with host 2016–2018 matrix (A(h)) and the mean annual vival, retrogression and fecundity) take place with and (wh) without host 2016–2018 matrix (A ) were used to deter- without hosts (exceptions were entries of growth a41 with mine how individual matrix elements contributed to varia- hosts and a42 without hosts). Independently of the size tion in the population growth rate, λ (Caswell, 2001). We attained by each plant, the above-ground tissue of 6 GRANADOS-HERNANDEZ ET AL.

(b) (c) FIGURE 2 Individuals of Castilleja (a) With hosts With one host Piqueria trinervia tenuiflora with potential hosts. Without hosts More than one host Cheilantes kaulfussii (a) Percentage of individuals of Eupatorium glabratum Penstemon roseus C. tenuiflora with and without potential hosts. (b) Percentage of individuals of C. tenuiflora with one and with more 11% 17% than one potential host (different 12% species). (c) Percentage of individuals of 47% 53% 42% C. tenuiflora with specific potential hosts. 83% 19% n with hosts = 199, n without hosts = 51 [Color figure can be viewed at wileyonlinelibrary.com]

The highest probability is registered in permanence in (a) (b) H different size categories in both conditions, but most indi- H viduals with this behavior have nearby potential hosts. As can be observed in Figure 4, C. tenuiflora can start H P reproducing since early growth stages (21 cm), reproduc- P tive structures can be found all year round, and fecundity was always higher with hosts. Larger categories had higher fecundity values, and the highest values were attained in the presence of hosts. Growth, represented by the transition from one category to the next, tended to be (c) (d) c) P higher when hosts were present. P

3.2.2 | Estimation of stochastic population growth H H Stochastic growth rates varied between the 2 years and the two conditions, indicating short-term responses to environmental variations. λ FIGURE 3 Connection between the root of Castilleja tenuiflora Stochastic growth rates ( s) tended to be lower with- and its potential hosts. (a and b). Connection between C. tenuiflora out hosts (λs = 0.9503; CI = 0.9055, 1.0514) than with μ and Verbesina sp. scale X200 100 m, (c) connection between C. them (λs = 1.02; CI = 0.9999, 1.1), but differences were tenuiflora and Piqueria trinervia scale X100 100 μm and not significant and estimates had a high variance (d) connection between C. tenuiflora and C. kaulfussii scale X2000 (Figure 5a). When this analysis was performed consider- μ 10 m. P: root of the parasitic plant C. tenuiflora and H: root ing specific hosts (P. trinervia, C. kaulfussii, E. glabratum (or rhizome) of the host and P. roseus), no clear trend was evident. Mean values were above one, and population growth rates were equiv-

C. tenuiflora can completely disappear, or only dry stems alent in P. trinervia and E. glabratum (λs = 1.065; may remain during the dry season (category 6). Demo- CI = 0.91, 1.12, λs = 1.05; CI = 0.91, 1.14, respectively), graphically, this means that retrogression is part of the but below one in the remaining two hosts. However, dif- life cycle, that is, the life cycle includes transitions from ferences were not significant and estimates of λs had high all categories (2–5) to category 6, and from the latter to variances (Figure 5b). smaller categories, but this type of retrogression was more important without hosts. In addition, individuals of all categories can resprout from surface or below-ground 3.2.3 | Elasticity of vital rates meristems that act as perennating buds when the growing season arrives. However, it is also common that indi- The elasticity analysis of vital rates shows that survival viduals retain leaves and reproductive structures had the most important contribution to population throughout all seasons, so reproductive structures and growth for it had the highest elasticity values both with- green leaves can be found even in the dry and hot spring. out hosts and with specific hosts (Figure 6). This was GRANADOS-HERNANDEZ ET AL. 7

FIGURE 4 Life cycle of Castilleja 23.0891 15.9154 tenuiflora with hosts (blue lines) and 10.0757 without hosts (green lines). Dotted lines 5.6952 correspond to retrogression, straight 5.4240 5.2323 0.8887 lines to growth, curves to survival 0.8442 (permanence) and above straight lines to 0.2279 fecundity. The thick lines represent the 1 2 3 450.1741 6 highest values in both matrices and the highest values of each process are shown. 1: Seeds that germinated in controlled chambers, 2: seedlings in the experimental boxes and individuals of 1–20.9 cm in height, 3: individuals of 21–35.9 cm in height, 4: individuals of 36–49.9 in height, 5: individuals >50 cm in height and 6: individuals with dry aerial tissue [Color figure can be viewed at wileyonlinelibrary.com]

0.0540 0.0550 observed in the two sampling years; however, values for TCS = 0.0603) in terms of explaining the difference in all vital parameters varied between them. In the period the growth rates of C. tenuiflora living with and without 2016–2017 (Figure 6a), the contribution of survival with- hosts(Figure7).Thismeansthatsurvivalisthemostimpor- out hosts tended to increase as size increased, and the tant vital rate for the dynamicsofthispopulationinthis contribution with hosts, especially from P. trinervia and time period. This contribution derives first from the perma- P. roseus, was more important in the first categories. The nence in category 5 (−0.0262), followed by permanence in contribution of survival with C. kaulfussii also increased category 6 (−0.0130), the transition from seedling to the first from categories 1 to 5, but then lost importance in cate- size category (category 3 = 0.0121) and finally the differ- gory 6, while the contribution with E. glabratum was con- ences in the fecundity of category 5 (−0.0122). The only posi- sistently higher in the category corresponding to the tive contribution to the difference between both growth bigger individuals. The highest elasticity values in this rates corresponds to the permanence of seedlings period were below 0.4 and corresponded to survival in (a22 = 0.0146). No trade-offs are evident from this analysis. category 6. In the period 2017–2018 (Figure 6b), the elas- Furthermore, the first-order approximation of Equa- ticity for survival was lower in the first categories, but in tion (3) is very accurate in terms of predicting growth the last one, it attained values as high as 0.8. The contri- (Equation (4)) (Caswell, 2001): bution of survival of different categories was variable but X ðÞwh ðÞh consistently reached its highest value in the last category λ = λ + Ci,j =0:9657, ð4Þ both without a host and with each of the specific hosts i,j we analyzed. In both years, growth, retrogression and P fecundity contributed very little to the population growth where Ci,j = TCF + TCS ,which is within 1% of the rate of C. tenuiflora, but elasticities were higher in the i,j actual value of λ(h). first year than in the second.

3.2.4 | Matrix comparison: LTRE 4 | DISCUSSION

The population of C. tenuiflora living with hosts, A(h) C. tenuiflora grows surrounded by potential hosts in the increased by 4% per year (λ(h) = 1.0452), whereas without PECM and can profit from them, as can be seen when its a host, A(wh), it decreased (λ(wh) = 0.9652). The total con- demographic parameters are compared with and without tribution of fecundity (Fi, TCF = 0.0192) to differences hosts. Eighty-three percent of the sampled individuals of between A(h) and A(wh) for the 2016–2018 period is three C. tenuiflora grew close to at least one potential host, usu- times smaller than that of survival (survival + growth; ally belonging to one of the most abundant species; 8 GRANADOS-HERNANDEZ ET AL.

Without hosts With hosts The high percentage of individuals of C. tenuiflora (a) 1. 4 1. 4 with potential hosts is probably associated with the colo- )

s nization process that is taking place in the heterogeneous 1. 2 1. 2 lava field. The prevailing conditions, that include low nutrients and high filtration rates (Mendoza-Hernández et al., 2013), should enhance root production and expan- 1. 0 1. 0 sion relatively near the soil surface, as has been reported by Berendse (1983) and de Kroon et al. (2012). Hosts can 0.8 0.8 be facilitators for C. tenuiflora in the ongoing succes-

Stochastic growth rate( growth Stochastic sional process, as has been reported for other hemiparasites (Press & Phoenix, 2005; Yong-Quan 0.6 0.6 et al., 2010), and can be part of the resources C. tenuiflora finds in this site.

(b) Piqueria Cheilanthes Eupatorium Penstemon The positive effect that the hosts can have on the par- trinervia kaulfussii glabratum roseus asitic plants is reflected in the vital rates of the latter. Sto- 1. 4 1. 4 1. 4 1. 4 chastic growth rates of C. tenuiflora tend to be lower without hosts than with them; however, it must be noted that both growth rates were close to one, with large confi- ) s 1. 2 1. 2 1. 2 1. 2 dence intervals, as is frequently observed in perennial species (Mandujano, Golubov, & Huenneke, 2007); thus, differences in population growth rates were not signifi- 1. 0 1. 0 1. 0 1. 0 cant, but strategies of this hemiparasitic species differed with and without host, following the pattern that we expected. Hence, our short-term analysis indicates that 0.8 0.8 0.8 0.8 Stochastic growth rate( growth Stochastic hosts tend to reduce selective pressures that affect the hemiparasite, as suggested by Matthies (1997) and Press 0.6 0.6 0.6 0.6 and Phoenix (2005), and, consequently, demographic parameters can be directly influenced by host availability,

FIGURE 5 Stochastic growth rate (λs)ofCastilleja tenuiflora as would be expected following de Kroon (2007) and de (a) without and with hosts (b) with different hosts. n with Kroon et al. (2012). As reported for other hemiparasitic hosts = 199, n without hosts = 51, with Piqueria trinervia = 83, n species (Matthies, 2017), host availability is part of the with C. kaulfussii = 37, n with Eupatorium glabratum = 25, n with environmental variability of the habitat of C. tenuiflora, P. roseus = 22 [Color figure can be viewed at and it depends on potential hosts being close and healthy wileyonlinelibrary.com] enough to be both accessible and suitable. The identity and productivity of hosts have been however, plants with more than one host were frequent, reported to have different effects on parasitic plants with the latter including also less abundant species. The (Fibich et al., 2010; Marquardt & Pennings, 2010; scanning electron microscope images showed that lateral Pennings & Callaway, 2002; Press & Phoenix, 2005). In roots of C. tenuiflora were in contact with the roots of its this study, however, stochastic growth rates calculated potential hosts, confirming the interaction between roots. with specific hosts, including the most abundant ones, Montes-Hernández et al. (2015, 2019) identified haustoria did not differ significantly among them, suggesting that of C. tenuiflora forming in lateral roots and a clear inter- the hosts were equivalent. This result further corrobo- action at the histological level with B. conferta and rates the generalist character of C. tenuiflora, since the fit- reported that C. tenuiflora obtains water, minerals, C, N ness of the population, expressed in its growth rate, is and essential oils from this host (Montes-Hernández similar with each of the hosts. et al., 2019). Haustoria are difficult to observe in this spe- The comparison of the life cycle of C. tenuiflora with cies and can be ephemeral or even nonfunctional and without hosts (Figure 4) shows that individuals of (Dobbins & Kuijt, 1973; Montes-Hernández et al., 2019), this species can survive the unfavorable season without but our results allow, through the microscopic observa- aerial structures (category 6). Elasticity values showed tion of contact between roots, the identification of poten- that survival of category 6 was the vital rate with the tial hosts and the corroboration of the interaction with highest contribution in both years. These results corrobo- several species, as expected due to the generalist charac- rate that survival of plants through underground organs ter of most hemiparasitic species (Matthies, 2017). and meristems has a crucial contribution to the GRANADOS-HERNANDEZ ET AL. 9

FIGURE 6 Elasticity of vitals rates (a) of Castilleja tenuiflora with different 0.40 hosts and without them (a) period 2016–2017 and (b) period 2017–2018. S: 0.35 With Piqueria trinervia survival, G: growth, R: retrogression, F: With Penstemon roseus fecundity. n with hosts = 199, n 0.30 With Eupatorium glabratum without hosts = 51, n with P. With Cheilanthes kaulfussii Without hosts trinervia = 83, n with C. 0.25 kaulfussii = 37, n with Eupatorium 0.20 glabratum = 25, n with P. roseus = 22. Note differences in scale in (a) and (b) 0.15 [Color figure can be viewed at Elasticity values wileyonlinelibrary.com] 0.10

0.05

0.00

-0.05 S S S S S S G G G G G G G G G G G G G G G R R R R R R R R R R F F F F F 1 2 3 4 5 6 21 31 41 51 61 32 42 52 62 43 53 63 54 64 65 23 24 34 25 35 45 26 36 46 56 2 3 4 5 6 (b) Vital rates 0.9

0.8 With Piqeuria trinervia With Penstemon roseus 0.7 With Eupatorium glabratum With Cheilanthes kaulfussii 0.6 Without hosts

0.5

0.4

0.3 Elasticity values

0.2

0.1

0.0

S S S S S S G G G G G G G G G G G G G G G R R R R R R R R R R F F F F F 1 2 3 4 5 6 21 31 41 51 61 32 42 52 62 43 53 63 54 64 65 23 24 34 25 35 45 26 36 46 56 2 3 4 5 6 Vital rates population growth rate, both with and without hosts. The an obligate holoparasitic species, can resprout directly role of underground meristems and buds that allow the from its haustoria. However, this strategy is more fre- transition from category 6 to previous categories is quent when there are no hosts, indicating that when extremely important in C. tenuiflora, both for individuals plants grow alone, the strategy to avoid the unfavorable growing alone or with a host. The importance of under- season is to act as geophytes, surviving through underground or surface perennation buds has been indicated ground structures and sprouting again as soon as the con- by authors like Klimešová and Klimas (2007) and Ott, ditions are favorable. Klimešová, and Hartnett (2019), who emphasize the Contrastingly, when hosts are present, most individ- potentially important role of underground and surface uals of C. tenuiflora can partially lose aerial structures, buds in disturbed and successional sites, because they are but, nevertheless, plants have leaves, flowers and fruits, determinant in the survival and above-ground population indicating an association between continuous reproduc- recovery when the growing seasons starts. Resprouting tion and the presence of hosts, which can buffer the strategies vary a lot, as exemplified by these authors and harsh environmental conditions of the extremely dry sea- by Truscott (1958), who observed that Cuscuta gronovii, son. In this sense, benefits of having a host are reflected, 10 GRANADOS-HERNANDEZ ET AL.

(a) 0 (b) 0.2 -2

-4 0.0 Fi Difference -6 P¡ Difference -0.2 -8

0.00 -0.010 F¡ Contribution P¡ Contribution -0.02 -0.015 123456 123456 Matrix element (j,:) Matrix element (j,:)

FIGURE 7 Life Table Response Experiments. (a) Differences in size-specific fertility (Fi) and (b) differences in size-specific survival (Pi) between the population dynamics of Castilleja tenuiflora growing with and without hosts, (c) contribution of the difference of fertility and (d) contribution of the difference of the survival to the effect on λ. Bar color codes: dark blue: category 1, orange: category 2, light yellow: category 3, magenta category: 4, green: category 5 and light blue: category 6. Note that the graph only shows the bars that correspond to existing matrix transitions for this species. Labels on the x-axis (j = 1, 2, 3, 4, 5, 6) are followed by bars representing transitions from stage j to i = 1, 2, 3, 4, 5, 6 [Color figure can be viewed at wileyonlinelibrary.com] at a demographic level, in the high fecundity values in all iteroparous species, survival of established successful categories and in less retrogression. Our results coincide individuals is very relevant and it is frequently the most with Marvier (1998), who identified a greater production important process for the persistence of a population of of reproductive structures in T. pusilla and T. eriantla as iteroparous species (Franco & Silvertown, 2004; Sil- a benefit obtained from its hosts. Furthermore, the proba- vertown, Franco, Pisanty, & Mendoza, 1993; Zuidema & bility of transition from one category to the next, which Franco, 2001; Zuidema & Zagt, 2000). In general, survival corresponds to growth, was higher with hosts than with- was the vital rate with a higher contribution in both years out them, coinciding with Matthies (1995, 1997), who and in all conditions. The same result was found on dif- observed that two parasitic plants (R. serotinus and ferent long-lived species (Aschero, Morris, Vázquez, C. integra) grew more with than without a host. Our Alvarez, & Villagra, 2016; Enneson & Litzgus, 2008; Mor- results expand the results of these authors as they show ris & Doak, 2002; Raventós, González, Mújica, & that benefits obtained from hosts are not only evident in Bonet, 2015). In the case of C. tenuiflora, the importance individuals but are also observed at the population level. of survival of the last size category and of those individ- Elasticity values showed differences in the relative uals that lose the aerial structures and then form new contribution of each vital rate and indicated that survival ones coincides with this trend; however, fecundity is also was the vital rate with the highest contribution in both crucial, as a source of new genotypes that can success- years. On the other hand, LTRE indicated that survival fully establish in heterogenous, changing or (survival + growth) of categories 5 and 6, followed by unpredictable environments. The contribution of fecun- fecundity of category 5, are the attributes that contributed dity to the differences between the growth rates in the the most to the differences between the finite growth two conditions was three times smaller than that of sur- rates with and without potential hosts. In general, the vival but is still important in this context, considering relation between the growth rate and the variation in that the persistence of populations in which reproduction each vital parameter varies between populations (Picó and recruitment can be extended for several periods, as et al., 2003; Zuidema & Franco, 2001), but survival elas- in plants that can clone or resprout, can be favored ticities tend to increase with longevity, and for perennial, (Higgins, Pickett, & Bond, 2000). GRANADOS-HERNANDEZ ET AL. 11

The highest elasticity value in the period 2016–2017 was Thus, we propose that hosts are another kind of resource, 0.4, while in the second year, it reached 0.8, in both cases variable in time and space, and that C. tenuiflora profits corresponding to survival of category 6. The differences in from them when they are available. Our results indicate elasticity values between the two years underline the variabil- that root hemiparasitism has positive effects on the popu- ity of the environment in which C. tenuiflora lives. The lation dynamics of C. tenuiflora, and we can thus conclude 2017–2018 winter was a cold one (lowest temperature = that C. tenuiflora is not better alone. −3C; Ajusco Meteorology Station), with frosts that reduced the survival of individuals and probably also of perennating ACKNOWLEDGMENTS structures, thus slowing the recovery and growth of damaged Luisa A. Granados-Hernández received a scholarship from plants. Another important factor in this period, that was Consejo Nacional de Ciencia y Tecnología (grant number totally unexpected, was the anthropogenic disturbance that 432340) and additional financial support from Programa took place in July 2017, causing the death of 54 individuals of de Apoyo a Estudiantes de Posgrado, Universidad C. tenuiflora, both with and without hosts, and probably also Nacional Autónoma de México, as well as support from affecting the potential hosts. Disturbance introduces varia- the Department of Ecology and Natural Resources, tions in some life stages more than in others (Wisdom, Facultad de Ciencias (UNAM). We thank Mónica Millss, & Doak, 2000), with different consequences depending Queijeiro, José G. García-Franco and Fernando Vite for on how intense, prolonged or recurrent it is. their suggestions on previous versions, and Eelke No trade-offs between survival and fecundity are evi- Jongejans and two anonymous reviewers for their useful dent in our results and, in fact, both parameters go in the comments. We acknowledge Silvia Espinoza-Matias for same direction, increasing the difference between the her support with the scanning electron microscope and plants with and without hosts and probably enhancing appreciate the contributions of Pedro Mendoza-Hernández the persistence of the population. and María Esther Sánchez Coronado, as well as the aca- Environmental and ecological conditions, as well as spe- demic support of Pilar Ortega Larrocea and the technical cific life histories, affect the interaction between holo and support of Mariana Hernández-Apolinar, Israel Solano- hemiparasites and their hosts, so each case can have individ- Zavaleta and Patricia Olguín Santos. We thank Uzmar ual characteristics. However, since most root hemiparasites Gómez and José L. Trujillo for their help with fieldwork. are generalists (Marquardt & Pennings, 2011; Pennings & Callaway, 2002), our results suggest that hosts will be para- ORCID sitized and will provide some resources to the hemiparasitic Irene Pisanty https://orcid.org/0000-0002-3533-564X species which will be benefited by them, for example, María C. Mandujano https://orcid.org/0000-0001-9855- through accumulation of biomass (Matthies, 1997), increase 6645 in growth and reproduction (Marvier, 1998; Matthies, 1995; Matthies, 2017), and also in fitness. Fitness responses will REFERENCES probably depend on how easily hosts can be reached and on Adler, L. (2003). Host species affect herbivory, pollination, and the resources they offer at an individual level. If the interac- reproduction in experiments with parasitic Castilleja. 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Population Ecology

Luisa A. Granados-Hernández1, Irene Pisanty 1*, JoséRaventós 2, Judith Márquez-Guzmán 3 and Mar´ıaC. Mandujano 4

1Departamento de Ecolog´ıay Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónomade México,Av Universidad 3000, Cd. Universitaria, Coyoacán,04510 Ciudad de M´xico; 2Departamento de Ecolog´ıa, Universidad de Alicante, Carretera S. Vicente del Raspeig s/n, 03080, San Vicente del Raspeig, Alicante, Spain; 3Departamento de Biolog´ıaComparada, Facultad de Ciencias, Universidad Nacional Autónomade México,Av Universidad 3000, Cd. Universitaria, Coyoacán,04510 Ciudad de México; 4Departamento de Ecolog´ıade la Biodiversidad, Instituto de Ecolog´ıa, Universidad Autónomade México,Av Universidad 3000, Cd. Universitaria, Coyoacán,04510 Ciudad de México.

*For correspondence: [email protected]

Supplementary information

1 Table S.1: Plant community in a disturbed lava ﬁeld in the Ecological Park of Mexico City (PECM).

Relative species Relative species Family Species abundance (Pi) frequency (Fi) Asparagaceae Agave salmeana 0.002 0.006 Asteraceae Bidens sp. 0.042 0.035 Asteraceae Bidens linulata 0.002 0.006 Asteraceae Dhalia coccinea 0.002 0.009 Asteraceae Eupatorium glabratum 0.028 0.063 Asteraceae Eupatorium pazcuarensis 0.007 0.009 Asteraceae Gnaphalium sp. 0.005 0.014 Asteraceae Stevia sp. 0.001 0.003 Asteraceae Piqueria trinervia 0.201 0.115 Asteraceae Verbesina sp. 0.012 0.029 Begoniaceae Begonia sp. 0.001 0.003 Boraginaceae Wigandia urens 0.020 0.026 Cactaceae Opuntia robusta 0.015 0.026 Cactaceae Opuntia rzendowzki 0.001 0.003 Commelinaceae Commelina sp. 0.033 0.046 Crassulaceae Sedum sp. 0.002 0.003 Crassulaceae Sedum oxipetalum 0.014 0.029 Cyperaceae Cyperus sp. 0.038 0.026 Geraniaeae Geranio sp. 0.036 0.009 Lamiaceae Manrrubio sp 0.102 0.029 Orchidaceae unidentified orchid 0.002 0.009 Orobanchaceae Castilleja tenuiflora 0.113 0.098 Orobanchaceae Lamoruxia dasyantha 0.001 0.003 Oxalidaceae Oxalis sp. 0.013 0.015 Plantaginaceae Penstemon roseus 0.084 0.095 Poaceae Mullenbergia sp. 0.001 0.003 Poaceae Pennisetum clandestinum 0.001 0.003 Polemoniaceae Loeselia mexicana 0.027 0.029 Polypodiaceae Polypodium thyssanolepis 0.010 0.011 Portulacaceae Portulaca sp. 0.006 0.012 Pteridaceae Cheilanthes bonariensis 0.058 0.078 Pteridaceae Cheilanthes kaulfussii 0.083 0.103 Pteridaceae Pellaea ternifolia 0.022 0.020 Rubiaceae Bouvardia terniflora 0.002 0.006 Sapindaceae Dodonea viscosa 0.001 0.003 Scrophulariaceae Buddleja cordata 0.012 0.029

2 Table S.2: Survival and fecundity of Castilleja tenuiﬂora with and without hosts in a disturbed lava ﬁeld in the Ecological Park of Mexico City (PECM)

Symbol Without Without With host With host Demographic in sym- host mean host mean mean value mean value rate bolic value value 2016-2017 2017-2018 matrix 2016-2017 2017-2018 Survival of class S 0.2250 0.2250 0.2250 0.2250 1 1 Survival of class S 0.9136 0.8833 0.7417 0.9833 2 2 Survival of class S 1.0000 0.9219 1.0000 0.7720 3 3 Survival of class S 1.0000 0.9123 1.0000 0.7659 4 4 Survival of class S 1.0000 0.9758 0.9881 0.6266 5 5 Survival of class S 0.9790 0.9597 0.9591 0.9360 6 6 Fecundity class F 0.0000 0.0000 0.0000 0.0000 2 2 Fecundity class F 6.7630 4.5255 5.7762 6.0347 3 3 Fecundity class F 12.4789 8.5969 7.1271 5.7735 4 4 Fecundity class F 24.9114 21.8317 18.3225 20.8616 5 5 Fecundity class F 0.0000 0.0000 0.0000 0.0000 6 6

3 Table S.3: Growth and retrogression of Castilleja tenuiﬂora with and without hosts in a disturbed lava ﬁeld in the Ecological Park of Mexico City (PECM)

Symbol Without Without With host With host Demographic in sym- host mean host mean mean value mean value rate bolic value value 2016-2017 2017-2018 matrix 2016-2017 2017-2018 Growth from G 0.0808 0.1028 0.0829 0.0880 class 1 to 2 21 Growth from G 0.0000 0.0027 0.0000 0.0071 class 1 to 3 31 Growth from G 0.0000 0.0000 0.0000 0.0048 class 1 to 4 41 Growth form G 0.0000 0.0000 0.0000 0.0000 class 1 to 5 51 Growth from G 0.0000 0.0000 0.0000 0.0000 class 1 to 6 61 Growth from G 0.2218 0.2203 0.1454 0.2136 class 2 to 3 32 Growth from G 0.0195 0.0130 0.0000 0.0000 class 2 to 4 42 Growth from G 0.0255 0.0000 0.0064 0.0000 class 2 to 5 52 Growth from G 0.1632 0.1629 0.1356 0.0962 class 2 to 6 62 Retrogression R 0.1251 0.1152 0.0815 0.0516 from class 3 to 2 23 Growth from G 0.1487 0.1960 0.1422 0.2030 class 3 to 4 43 Growth from G 0.0129 0.0304 0.0515 0.0258 class 3 to 5 53 Growth from G 0.0900 0.1029 0.1089 0.1667 class 3 to 6 63 Retrogression R 0.0353 0.0222 0.0180 0.0167 from class 4 to 2 24 Retrogression R 0.1137 0.1000 0.0765 0.0432 from class 4 to 3 34 Growth from G 0.1837 0.2930 0.1482 0.2461 class 4 to 5 54 Growth from G 0.0513 0.1299 0.1001 0.0500 class 4 to 6 64 Retrogression R 0.0414 0.0358 0.0745 0.0208 from class 5 to 2 25 Retrogression R 0.0231 0.0375 0.0185 0.0278 from class 5 to 3 35 Retrogression R 0.0788 0.0494 0.0625 0.0521 from class 5 to 4 45 Growth from G 0.0534 0.1066 0.0745 0.1736 class 5 to 6 65 Retrogression R 0.0387 0.0721 0.0333 0.0829 from class 6 to 2 26 Retrogression R 0.0242 0.0120 0.0283 0.0159 from class 6 to 3 36 Retrogression R 0.0081 0.0046 0.0132 0.0242 from class 6 to 4 46 Retrogression R 0.0127 0.0079 0.0076 0.0250 from class 6 to 5 56

4 Table S.4: Survival and fecundity of Castilleja tenuiflora with different hosts in a disturbed lava field in the Ecological Park of Mexico City (PECM)

5 Table S.5: Growth and retrogression of Castilleja tenuiflora with differents hosts in a disturbed lava field in the Ecological Park of Mexico City (PECM)

With With With With With With With Eu- With Eu- Symbol Penste- Penste- Cheilan- Cheilan- Piqueria Piqueria patorium patorium in mon mon thes thes Demographic trinervia trinervia glabratum glabratum sym- roseus roseus kaulfussii kaulfussii rate mean mean mean mean bolic mean mean mean mean value value value value matrix value value value value 2016-2017 2017-2018 2016-2017 2017-2018 2016-2017 2017-2018 2016-2017 2017-2018 Growth from G 0.0829 0.0880 0.0829 0.0880 0.0829 0.0880 0.0829 0.0880 class 1 to 2 21 Growth from G 0.0000 0.0071 0.0000 0.0071 0.0000 0.0071 0.0000 0.0071 class 1 to 3 31 Growth from G 0.0000 0.0048 0.0000 0.0048 0.0000 0.0048 0.0000 0.0048 class 1 to 4 41 Growth form G 0.0000 0.0000 0.0000 0.0000 0.0000 0.0000 0.0000 0.0000 class 1 to 5 51 Growth from G 0.0000 0.0000 0.0000 0.0000 0.0000 0.0000 0.0000 0.0000 class 1 to 6 61 Growth from G 0.2832 0.2043 0.1349 0.2146 0.0972 0.2569 0.2013 0.2153 class 2 to 3 32 Growth from G 0.0040 0.0191 0.0000 0.0000 0.0000 0.0139 0.0382 0.0000 class 2 to 4 42 Growth from G 0.0248 0.0000 0.0833 0.0000 0.0652 0.0000 0.0278 0.0000 class 2 to 5 52 Growth from G 0.1219 0.1402 0.1369 0.1771 0.2431 0.1528 0.1968 0.0910 class 2 to 6 62 Retrogression from class 3 R23 0.1334 0.0921 0.0000 0.0417 0.1187 0.0764 0.1107 0.0417 to 2 Growth from G 0.1510 0.2267 0.2264 0.1667 0.1288 0.2500 0.1585 0.2486 class 3 to 4 43 Growth from G 0.0159 0.0110 0.0833 0.0000 0.0076 0.0208 0.0049 0.0556 class 3 to 5 53 Growth from G 0.0896 0.0813 0.1389 0.0000 0.0625 0.0833 0.0866 0.1375 class 3 to 6 63 Retrogression from class 4 R24 0.0512 0.0000 0.0301 0.0833 0.0444 0.0000 0.0689 0.0167 to 2 Retrogression from class 4 R34 0.1212 0.1318 0.1319 0.0000 0.0417 0.0833 0.0694 0.0167 to 3 Growth from G 0.1361 0.1934 0.1134 0.1181 0.1544 0.1278 0.2080 0.0861 class 4 to 5 54 Growth from G 0.0495 0.1207 0.0417 0.0556 0.1056 0.2694 0.0520 0.2083 class 4 to 6 64 Retrogression from class 5 R25 0.0564 0.0625 0.0083 0.0536 0.0840 0.0278 0.0342 0.0000 to 2 Retrogression from class 5 R35 0.0152 0.0875 0.0104 0.0833 0.0000 0.0000 0.0487 0.0000 to 3 Retrogression from class 5 R45 0.0975 0.0490 0.0465 0.0444 0.0522 0.1111 0.1523 0.0667 to 4 Growth from G 0.0155 0.0875 0.8651 0.0643 0.0850 0.0208 0.0327 0.1167 class 5 to 6 65 Retrogression from class 6 R26 0.0458 0.0786 0.0258 0.0749 0.0374 0.0392 0.0277 0.0522 to 2 Retrogression from class 6 R36 0.0343 0.0086 0.0000 0.0000 0.0215 0.0069 0.0278 0.0213 to 3 Retrogression from class 6 R46 0.0128 0.0028 0.0000 0.0139 0.0242 0.0139 0.0056 0.0052 to 4 Retrogression from class 6 R56 0.0650 0.0090 0.0258 0.0139 0.0715 0.0000 0.0187 0.0056 to 5 6 Table S.6: Potential hosts of Castilleja tenuiﬂora and their relative abundance in a disturbed lava ﬁeld in the Ecological Park of Mexico City (PECM)

Relative species Family Potential hosts (species) abundance (Pi) Asteraceae Piqueria trinervia 0.201 Asteraceae Eupatorium glabratum 0.028 Asteraceae Eupatorium pazcuarensis 0.007 Asteraceae Verbesina spp. 0.012 Pteridaceae Cheilanthes kaulfussii 0.083 Pteridaceae Cheilanthes bonariensis 0.058 Pteridaceae Pellaea ternifolia 0.022 Orobanchaceae Castilleja tenuiﬂora 0.113 Orobanchaceae Lamoruxia dasyantha 0.001 Plantaginaceae Penstemon roseus 0.084 Poaceae Mulhenbergia spp. 0.001 Boraginaceae Wigandia urens 0.020 Cactaceae Opuntia robusta 0.015 Polemoniaceae Loeselia mexicana 0.027 Commelinaceae Commelina spp. 0.033 Asparagaceae Agave salmeana 0.002 Crassulaceae Sedum oxypetalum 0.014 Crassulaceae Sedum spp. 0.002

7 a

Figure S.1: Scanning electron microscope image of a) root Castilleja tenuiﬂora b) lateral root