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Article

Removal of an Invasive Alien Mediterranean Herbaceous (Asphodelus fistulosus) in a Mexican Botanical Garden

by
Oscar Sandino Guerrero-Eloisa
1,2,
Jordan Golubov
3,*,
María C. Mandujano
4 and
Beatriz Maruri-Aguilar
5
1
Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Liga Periférico-Insurgentes Sur 4903, Parques del Pedregal, Ciudad de México 14010, Mexico
2
Doctorado en Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana, Ciudad de México 04960, Mexico
3
Departamento de El Hombre y su Ambiente, Universidad Autónoma Metropolitana–Xochimilco, Ciudad de México 04960, Mexico
4
Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Ciudad de México 04510, Mexico
5
Jardín Botánico Regional de Cadereyta “Ing. Manuel González de Cosío”, Camino Antigua Hacienda de Tovares S/N Ejido, Las Fuentes, Cadereyta de Montes 76500, Mexico
*
Author to whom correspondence should be addressed.
J. Zool. Bot. Gard. 2025, 6(4), 59; https://doi.org/10.3390/jzbg6040059
Submission received: 10 October 2025 / Revised: 17 November 2025 / Accepted: 17 November 2025 / Published: 21 November 2025
Browse Figures
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Abstract

Botanical gardens promote the conservation of native species of the sites where they are located, showing the importance of preserving native flora. It is common to find invasive alien species (IAS) established intentionally or accidentally in these sites. In a patch of native vegetation within the Cadereyta de Montes Regional Botanical Garden, the removal of the invasive alien Asphodelus fistulosus was carried out and during a subsequent 108-month period. The repopulation of the species was supervised by removing new individuals at each visit. More than 1000 individual plants of A. fistulosus were removed during the entire monitoring period, and through subsequent visits, no new individuals have been spotted. The monetary cost associated with the removal, monitoring and control of A. fistulosus was calculated over MXN 15,000.00. The removal and post-removal monitoring of species at sites of interest provide valuable information about control time and economic costs to consider in the control of IAS. Additionally, the germination experiments carried out with seeds from different years of collection showed a higher germination percentage that was not affected by the age of the seeds.

1. Introduction

The release of invasive alien species (IAS) globally is recognized as an issue of biodiversity concern, with IAS being one of the main drivers of biodiversity loss [1]. Within the pathways of movement and transport of plant IAS, horticulture has been identified as the primary global route for the introduction of invasive alien plants to new sites, facilitating their colonization, establishment in new areas, and eventual invasiveness [2,3]. Historically, botanical gardens have been recognized as sources of non-native plants that could be potentially invasive, either through escapes from collections or by supplying ornamental horticulture [4,5]; however, there has been an ongoing effort to avoid their spread and actively engage in actions (public awareness, protocols, containment and removal, active sentinel sites among others) that aim towards their management [6].
Botanical garden collections hold a large number of species and are considered responsible in identifying those species with the potential to escape from the collections and become invasive [5]. At the Royal Botanical Gardens, Kew, 206 of the 4620 species (4.5%) that were intentionally planted in the gardens have been found to grow spontaneously in adjacent natural lands. Of these escapes, 119 species (2.6% of the species planted) are now considered invasive [5]. In this context, some institutions have developed policies or guidelines for their practice that reduce the risk of additional releases of IAS by implementing strategies (e.g., identifying the area occupied by invasive plant species, avoiding range extension, implementing control actions, replacing them with native species, and promoting awareness about the impacts of invasive flora).
In Mexico, the National Strategy on Invasive Species in Mexico [7], the Mexican Strategy for Plant Conservation 2012–2030 [8], and the National Strategy on Biodiversity of Mexico, action plan 2016–2030 [9] collaborate to carry out measures for the prevention, control, and eradication of invasive alien species through their early detection, control, and eradication when possible. These strategies, together with the North American Botanic Garden Strategy for Plant Conservation 2016–2020 [10] and Botanic Gardens Conservation International (BGCI) guidelines [6] promote the increase in actions and control of invasive alien species through public awareness, control and mitigation in botanical gardens. The Mexican management plan for botanical gardens [11] follows international guidelines [6] and establishes that botanical gardens must implement eradication and control protocols for invasive alien plants, more so if located near natural protected areas or immersed in natural areas, as well as being an active stakeholder for IAS management.
Prevention is the most effective strategy to counteract the processes caused by invasive species [11]; however, this is only feasible in the early stages of the introduction–naturalization–invasion continuum [11]. In areas where IAS become established and cause damage to ecosystems, mitigation efforts such as removal become an important challenge, because this allows the impacts of these species to be evaluated and serves as a key component of environmental restoration plans [12]. The removal of IAS has been shown to favor native species richness and has allowed for the recovery of natural processes [13]. Therefore, a maximum effort in the elimination of IAS will be successful if the composition and functionality of the invaded environment is recovered [12]. These methods of removal include mechanical, physical, biological and chemical control, and the implementation of two or more of these techniques (integrated management) is often considered necessary. Physical control (using conventional tools) is a simple method that can be used when the invaded area is not too large and the aim is to eliminate the individuals (leaves, trunk, and roots) [14]. Follow up periods after control are necessary to assess success, especially with species with mechanisms that allow them to spread the risk over time (e.g., bulbs, rhizomes, seed banks) [15,16], thus having implications for the long-term management of the species [17].
Quantifying the invasion costs associated with preventing, controlling or eradicating invasions will depend on the expenditure generated in each action [18]. The first quantifications of IAS were limited to geographical areas in the USA [19,20], Europe [21], or Australia [18], focusing on certain taxonomic groups, such as insects [22], fish (Loricariidae Family) [23], and mammals such as the coypu (Myocastor coypus [Molina]) [24] or the zebra mussel (Dreissena polymorpha [Pallas]) [25]. Currently, the InvaCost database has enabled and updated monetary costs of biological invasions worldwide [26]; it estimates the cost associated with the impact of IAS globally to be USD 2.3 trillion (2017 USD) [27]. In North America, invasions cost the U.S. economy, Canada, and Mexico at least USD 1.26 trillion between 1960 and 2017 [28], and for Mexico, the invasion costs between 1992 and 2019 were estimated to be USD 5.33 billion (MXN 100.84 billion), with devilfish (Pterygoplichthys sp.) and water lily (Eichhornia crassipes [(Mart.) Solms]) having the greatest impact [29].
Asphodelus fistulosus L. (Asphodelaceae) is native perennial herb from Southern Europe, reported as invasive in the Southeastern USA, Australia, India and New Zealand [30]. A. fistulosus has prolific seed production throughout the year (>600 seeds on average) [31], can self-pollinate, and attracts a variety of native and alien floral visitors that contributes to its invasion potential [32]. The introduction of A. fitulosus has been mainly for ornamental purposes [33,34], but can easily escape from cultivation [35] and establish populations in disturbed, over-grazed habitats [36]. In Australia, it was introduced as an ornamental plant in a botanical garden in the 19th century [37] but now forms dense populations in arid and semi-arid environments and disturbed areas [37,38]. In Mexico, the first record of A. fistulosus dates back to the 1940s [39], and since then, populations have increased the geographical range and is now found in 15 out of 32 states [31].
The objective of this study was to evaluate the duration and effectiveness of manual removal of Asphodelus fistulosus in the natural area of the Cadereyta de Montes Botanical Garden. In addition, controlled seed germination experiments were conducted to assess the potential of re-invasion from the existing soil seed bank, which provides valuable information to establish an appropriate monitoring period for complete eradication at the site.

2. Materials and Methods

2.1. Study Site

The study was carried at the Cadereyta de Montes Regional Botanical Garden (hereafter CRBG) “Ing. Manuel González de Cosío” (20°41′15.8″, −99°8′17.7″; 2046 masl) (Figure 1), located in the Queretaro Semi-Desert region that is part of the Chihuahuan Desert in its extreme southern portion. The botanical garden has an area of 10 hectares, and of these 7.5 ha is natural vegetation cover (study site). The natural area contains representative native plant species characteristic of the region, including Agave difformis A.Berger., Agave salmiana Otto ex Salm-Dyck, Yucca filifera Chabaud., Mammillaria uncinata Zucc ex. Pfeiff., Opuntia tomentosa Salm-Dyck, Opuntia robusta J. C. Wendl., Neltuma laevigata (Humb. & Bonpl. ex Willd.) Britton & Rose. and Jatropha dioica Sessé. There are also other IAS such as Schinus molle L., Aloe vera L., Kalanchoe delagoensis Eckl. & Zeyh., Leonotis nepetifolia (L.) R.Br., Melinis repens (Willd.) Zizka, Reseda luteola L. and Nicotiana glauca Graham [31]. The CRBG promotes the use of native species, emphasizing knowledge as a tool for conservation and for preventing the introduction of IAS. The presence of IAS in the botanical garden is primarily due to horticultural activities in the surrounding areas. In particular, the establishment of A. fistulosus resulted from human activities as the invaded site had been used as a deposit of foreign gravel and sand that contained seeds. This site is a temporary location where materials are deposited before disinfection and use, and it shows some disturbance associated with the presence of other IAS, such as Schinus molle L. This space is also occasionally used for environmental workshops. No other populations of A. fistulosus have been found within the grounds of the botanical garden, however populations are established nearby.

2.2. Plant Removal and Monitoring

In February 2016, the first removal of Asphodelus fistulosus individuals was carried out in the natural vegetation area of the botanical garden. A 12 × 12 m (144 m2) site was documented to contain A. fistulosus individuals. Within the plot, each plant of A. fistulosus was uprooted using common gardening tools. For the initial and subsequent removals, plants were measured [plant height (cm), diameter (cm), root depth (cm), number of leaves, spikes and fruits] as well as data on the number of people involved in removal, and time invested in the process. Total seed outputs were estimated by multiplying the number of fruits by six (the number of seeds present per fruit; each fruit has six seed always). This estimation was a reference for future visits. All samples were incinerated at the Universidad Autonóma Metropolitana—Xochimilco.
Follow up visits were conducted monthly during the first six months (March–August 2016), and subsequently at 8 (October 2016), 12 (February 2017), 18 (August 2017), 20 (October 2017), 21 (November 2017), 24 (February 2018), 30 (August 2018), 36 (February 2019), 41 (July 2019), 43 (September 2019), 45 (November 2019), 47 (January 2020), 48 (February 2020), 72 (March 2022), 81 (November 2022), 84 (February 2023) 96 (February 2024) and 108 months (February 2025) after the first removal (Figure 2).
In the surveys conducted after the first removal, we searched for emerging seedlings of Asphodelus fistulosus. These seedlings can be distinguished from other herbaceous plants, mainly grasses, by their needle-like leaf shape and by the orange to reddish coloration present at the tip of the leaves.

2.3. Germination Experiment

A controlled experiment was conducted in February 2022 in which Asphodelus fistulosus seeds collected in October 2014 (eight years prior to the experiment), February 2016 (six years prior), and September 2018 (four years prior) were germinated in Petri dishes using 1.5% bacteriological agar as the culture medium, and kept with a 12:12 h photoperiod and an average temperature (24 °C) in a plant growth chamber (LAB-LINE Biotronette, Melrose Park, IL, USA). A total of 10 Petri dishes with 25 seeds (N = 250) each for every year (2014, 2016 and 2018) were used. Each seed was identified and inspected every 24 h.
We assessed the following germination parameters: the percentage of seeds germinated at the end of the germination period (germinability, GRP); the mean germination time (MGT), calculated as the weighted average time of germination; the mean germination rate (MGR), defined as the reciprocal of the mean germination time; the germination speed (GSP); and the uncertainty index (UNC), an adaptation of the Shannon index that evaluates the uncertainty associated with the relative distribution of germination frequency.
These parameters were calculated using R package GerminaR ver. 2.1.4 [40], the relationship between germination experiments and the year of which seeds were collected was analyzed using a Generalized Linear Model (GLM) with a binomial error distribution using R Studio version 4.3 [41].

2.4. Estimating Control Cost

The cost of the control was estimated by calculating the time spent on every visit and the total number of persons involved. We calculated the cost according to the Government of the State of Querétaro’s pay scale [42], using as a reference the minimum monthly salary of MXN 8134.00 (approximately one minimum wage) to a maximum of MXN 18,774.00 (equivalent to 2.3 minimum wages); a worker earning the minimum wage would receive MXN 271.33 (USD 14.66) per diem, while one earning 2.3 minimum wages would receive MXN 625.80 (USD 34.02). When adding year-end bonuses and vacation premiums, someone earning the minimum wage would earn at least MXN 304.91 (USD 16.50) per diem when prorating these two main benefits. It should be noted that this calculation is a hypothetical exercise. Ancillary costs such as transport, food, materials, and other supplies were not included.

3. Results

3.1. Individual Removal

Asphodelus fistulosus is a prolific seed producer (600 seeds on average) during its reproductive period. At the first removal, we counted the number of mature fruits that do not have seeds inside. The estimated seed production during the first removal was 4800 seeds in this plot. For the period February 2016–November 2022 (81 months), 25 removals were carried out at different periods of time. During this time period, a total of 1330 plants of A. fistulosus were removed, and of these, 58 were reproductive plants (presence of spikes) found mostly on the first removal (40 plants) (Figure 2). Subsequent removals were carried out before plant set fruit. The average removal time of the plants in the plot for each removal was 20 min, during which two people were involved in the process of monitoring the invaded area and removing A. fistulosus plants.

3.2. Asphodelus fistulosus L. Seed Germination

Germination of A. fistulosus seeds of different ages was consistently >90% with very small, non-significant decreases over time (2014 98%, 2018 95% and 2016 94%), meaning seeds can have a seed bank of at least six years. Seeds started germinating after 24 h (except for in 2014), having the highest germination within the 24–48 h period (>80%) (Figure 3). We did not find significant differences in the germination experiments between the years of seeds collected (χ2 = 0.2443; df = 2; p = 0.885). The mean germination time for the three differents years was two days, with 2014 and 2016 having high synchrony (near 1) in comparison to 2018, and the UNC index showed lower values that are consistent with the higher germination frequency (Table 1).

3.3. Estimating the Cost of Control

The total time of monitoring and removal of Asphodelus fistulosus was 17 h in 21 working days (163 h). The removal cost during the 2016–2022 period for the plot of 12 × 12 m2 of A. fistulosus in CRBG was estimated to be MXN 15,245.5 (USD 832.08). Considering that two people carried out this process (MXN 7622.75 per person, USD 416), this estimation considered the minimum salary during the period.

4. Discussion

The introduction of IAS by human activities such as ecological restoration, the horticultural industry, and gardening provides a continuous supply of propagules that allows for the expansion and establishment of IAS populations, contributing to their spread [43,44,45].
Botanical gardens play an active and central role in the conservation of biological diversity, and they necessarily involve a wide audience and involvement in education and research [46,47], highlighting the importance of conserving plant diversity and the biodiversity associated with vegetation [47]. Botanic gardens have historically been reservoirs of IAS [48] and continuously strive to control the spread of alien plant species [49] that affect surrounding areas [50]. In CRBG, the efforts of conservation focus especially on native vegetation and representative flora of this region. The collaborative research and conservation programs of the CRBG to protect native species from external impacts such as IAS presents an invaluable conservation goal that is an integral part of ongoing efforts [49].
The introduction of exotic plants that occurs through the ornamental trade [51] is considered a major introduction pathway of naturalized and invasive alien plants [52]. The presence of A. fistulosus and other IAS in the CRBG, such as Kalanchoe (Crassulaceae) (which is well known for its ornamental value [53,54]) or Leonotis nepetifolia (L.) R. Br. (which was introduced as an ornamental plant and has become naturalized in America [55]), supports the hypothesis of the success of species brought about by horticulture [50,52]. Asphodelus fistulosus is widely used for ornamental purposes [33,34], and despite being considered invasive, it is nevertheless found in botanical gardens in Australia [43] and Mexico (this paper) with clear effects on native vegetation of semiarid environments [31,32,33,34].
The control of IAS can be challenging given the wide range of species involved and the different traits that favor invasion success. Manual removal is suggested when IAS occupy small areas or have small population sizes [56]. Di Tomaso et al. [14] described the advantages and disadvantages of implementing manual control on A. fistulosus, emphasizing the convenience of the complete removal of individuals, including leaves and roots. A key limitation of this method is the requirement for continuous monitoring and removal over extended periods (>1 year) in areas with poor accessibility [57]. In this study, conducted in a small area, the monitoring period lasted more than five years—a duration that, for larger or less accessible areas, could make this method expensive [58] or even outright impossible. The manual method must account for monitoring periods that can extend up to 108 months, as in our case, with continuous removal at specific times (e.g., before seeding), and it also requires training personnel in identifying phenophases and in applying the method for complete removal of the target species.
Prolific seed production, germination percentage and timing are an important component on A. fistulosus invasiveness, key life-history traits that play an important role in biological invasions [59,60]. These combined factors involving the early stages of development have deep implications in the long-term control and management of IAS [17]. According to [61], a short-term germination advantage or priority effects (few days/weeks) provides invasive alien species with a strong competitive advantage over native species and is a critical factor in many invasions. A. fistulosus has a high rate of germination in a short-time window [31] (this study) that provides an advantage because it minimizes the effects of interspecific competition by inhibiting the germination of neighboring species [62]. The wide distribution in Mexico of A. fistulosus is also associated with continuous flowering and fruit production [31,32], phenophases that allow the species to generate a continuous seed bank [63]. Removal efforts during critical stages, such as flowering [14], offer an opportunity to prevent the formation of a seed bank and avoid the long-term survival of populations decreasing their ability to become naturalized, and invasive [63]. Monitoring post-removal is possibly the most important part of management as it permits the evaluation of the control method and identify possible re-invasions making eradication feasible.

5. Conclusions

The results of this study highlight the importance of implementing manual control methods for invasive alien species (IAS) over extended periods. Mechanical methods are often considered as a non-aggressive control alternative; however, their application is limited by the invaded area and the duration of post-removal monitoring, both of which influence budget allocation. Post-removal monitoring, combined with controlled germination experiments, enables the identification of repopulation events and provides valuable insights into the time required to eliminate the target species by depleting the seed bank. Together, these actions enhance the effectiveness and success in IAS management plans. There is an urgent need to evaluate the soil seed bank of this and other IAS and monitor the recovery of native plants at sites where IAS have been managed.

Author Contributions

Conceptualization, J.G. and B.M.-A.; Data curation, J.G.; Formal analysis, O.S.G.-E. and J.G.; Funding acquisition, M.C.M.; Investigation, J.G. and B.M.-A.; Methodology, O.S.G.-E. and J.G.; Writing—original draft, O.S.G.-E. and J.G.; Writing—review and editing, O.S.G.-E., J.G. and B.M.-A. All authors have read and agreed to the published version of the manuscript.

Funding

Financial and logistical support was provided by the Instituto de Ecología, UNAM, SEP-CONACyT 221362 and the GEF 00089333 project “Enhancing National Capacities to manage Invasive Alien Species (IAS) by implementing the National Strategy on IAS” to María C. Mandujano and Jordan Golubov.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The original data presented in the study are openly available at https://zenodo.org/records/17315727 (accessed on 10 October 2025).

Acknowledgments

The first author is a student of the PhD Program Doctorado en Ciencias Biológicas y de la Salud—Universidad Autónoma Metropolitana Xochimilco (UAM-X), and the paper is part of his dissertation in partial fulfillment of the requirements for the graduate program. Botanical Garden “Ing. Manuel González de Cosío” staff especially to Catalino Cruz “Cata” (†) and Oliverio Vera for their essential logistic and technical support during the collect of data. We thank Mariana Rojas-Arechiga for logistical support, Esteban Omar Munguía Soto and José Antonio Aranda Pineda for field assistance. We also thank the editors and three reviewers of the Journal of Zoological and Botanical Gardens for their professional suggestions for improving the manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

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Jzbg 06 00059 g001
Figure 1. (Upper) Mexico, with the state of Querétaro shown in gray, and the light brown area indicating the extent of the Chihuahuan Desert from Arizona, New Mexico, and Texas in the USA to Querétaro and Hidalgo in Mexico. (Middle) The state of Querétaro, showing the municipality of Cadereyta de Montes in orange; the green dot marks the Cadereyta de Montes Regional Botanical Garden (CRBG) “Ing. Manuel González de Cosío”, located within the municipality. (Lower) The green line indicates the extent of the botanical garden (10 ha), and the red plot shows the study site (144 m2).
Figure 1. (Upper) Mexico, with the state of Querétaro shown in gray, and the light brown area indicating the extent of the Chihuahuan Desert from Arizona, New Mexico, and Texas in the USA to Querétaro and Hidalgo in Mexico. (Middle) The state of Querétaro, showing the municipality of Cadereyta de Montes in orange; the green dot marks the Cadereyta de Montes Regional Botanical Garden (CRBG) “Ing. Manuel González de Cosío”, located within the municipality. (Lower) The green line indicates the extent of the botanical garden (10 ha), and the red plot shows the study site (144 m2).
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Figure 2. Number of plants removed for the period February 2016–November 2022 in Cadereyta de Montes Regional Botanical Garden (CRBG) wild area. Blue bars indicate the number of plants removed in each month; gray bars indicate the number of reproductive plants; and the black line indicates the time spent on the remotion.
Figure 2. Number of plants removed for the period February 2016–November 2022 in Cadereyta de Montes Regional Botanical Garden (CRBG) wild area. Blue bars indicate the number of plants removed in each month; gray bars indicate the number of reproductive plants; and the black line indicates the time spent on the remotion.
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Figure 3. Percentage germination of Asphodelus fistulosus seeds over a 6 day period, for seeds sourced from three years (2014, 2016 and 2018), kept at a continuous temperature and 12:12 photoperiod. The experiment was carried out in 2022 such that seeds were 8, 6 and 4 years after collection.
Figure 3. Percentage germination of Asphodelus fistulosus seeds over a 6 day period, for seeds sourced from three years (2014, 2016 and 2018), kept at a continuous temperature and 12:12 photoperiod. The experiment was carried out in 2022 such that seeds were 8, 6 and 4 years after collection.
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Table 1. Seed germination indices of Asphodelus fistulosus seeds collected during three different time periods. GSN: germinated seeds, GNP: germinability, MGT: mean germination time; MGR: mean germination rate; GSP: germination speed, UNC: uncertain index, SYN: Synchronization index, VGT: germination variance, SDG: germination standard deviation, CVG: coefficient of variation.
Table 1. Seed germination indices of Asphodelus fistulosus seeds collected during three different time periods. GSN: germinated seeds, GNP: germinability, MGT: mean germination time; MGR: mean germination rate; GSP: germination speed, UNC: uncertain index, SYN: Synchronization index, VGT: germination variance, SDG: germination standard deviation, CVG: coefficient of variation.
YearSeeds (N)GSN
(N)		GNP (%)MGT DaysMGRGSP (%)UNCSYNVGTSDGCVG (%)
201425024698.42.000.49948.890.040.990.000.063.18
201625023493.62.000.49948.890.110.970.010.115.66
201825024397.21.880.53153.060.830.680.210.4624.30
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MDPI and ACS Style

Guerrero-Eloisa, O.S.; Golubov, J.; Mandujano, M.C.; Maruri-Aguilar, B. Removal of an Invasive Alien Mediterranean Herbaceous (Asphodelus fistulosus) in a Mexican Botanical Garden. J. Zool. Bot. Gard. 2025, 6, 59. https://doi.org/10.3390/jzbg6040059

AMA Style

Guerrero-Eloisa OS, Golubov J, Mandujano MC, Maruri-Aguilar B. Removal of an Invasive Alien Mediterranean Herbaceous (Asphodelus fistulosus) in a Mexican Botanical Garden. Journal of Zoological and Botanical Gardens. 2025; 6(4):59. https://doi.org/10.3390/jzbg6040059

Chicago/Turabian Style

Guerrero-Eloisa, Oscar Sandino, Jordan Golubov, María C. Mandujano, and Beatriz Maruri-Aguilar. 2025. "Removal of an Invasive Alien Mediterranean Herbaceous (Asphodelus fistulosus) in a Mexican Botanical Garden" Journal of Zoological and Botanical Gardens 6, no. 4: 59. https://doi.org/10.3390/jzbg6040059

APA Style

Guerrero-Eloisa, O. S., Golubov, J., Mandujano, M. C., & Maruri-Aguilar, B. (2025). Removal of an Invasive Alien Mediterranean Herbaceous (Asphodelus fistulosus) in a Mexican Botanical Garden. Journal of Zoological and Botanical Gardens, 6(4), 59. https://doi.org/10.3390/jzbg6040059

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