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Article

Alien and Potentially Invasive Plants in Four Lagoons on the Island of Cozumel, Mexico

by
Gonzalo Castillo-Campos
1,
José G. García-Franco
2,*,
M. Luisa Martínez
2,3,* and
J. Jesús Pale-Pale
1
1
Red de Biodiversidad y Sistemática, Instituto de Ecología A.C. (INECOL), Xalapa 91073, Mexico
2
Red de Ecología Funcional, Instituto de Ecología A.C. (INECOL), Xalapa 91073, Mexico
3
Institute of Engineering, Universidad Nacional Autónoma de México, Mexico City 97302, Mexico
*
Authors to whom correspondence should be addressed.
Plants 2023, 12(9), 1918; https://doi.org/10.3390/plants12091918
Submission received: 27 March 2023 / Revised: 25 April 2023 / Accepted: 4 May 2023 / Published: 8 May 2023
(This article belongs to the Special Issue Plant Invasion 2022)

Abstract

:
The expansion of alien invasive species is a worldwide threat that affects most ecosystems. Islands and freshwater ecosystems are among the most vulnerable to species invasion, resulting in reduced biodiversity. In this study, we aimed to explore the floristic composition of the aquatic vegetation in four lagoons in southeastern Cozumel and assess the occurrence and abundance of alien and potentially invasive plants. We found a total of 43 aquatic or underwater herbaceous species that are subject to periodic flooding. Cluster analyses grouped the lagoons into two groups according to their floristic composition. The results demonstrate that alien and potentially invasive plants were dominant in 3 of the 4 lagoons, representing from 7 to 43% of the species. Six of these species were notably abundant, especially in three lagoons. Further, 2 species are considered among the 100 worst invasive species worldwide, although their abundance in Mexico remains relatively reduced. Five alien and potentially invasive species are terrestrial and grow on the shore of the lagoons, while one is aquatic. Urgent control and management actions are necessary. These should include (a) early detection and surveillance to determine if the alien species found behave as invasives; (b) understanding the relevance of invasive species; (c) preventing and intercepting; and (d) control and management. Habitat restoration, adequate legislation, collaboration between stakeholders, and raising awareness of the dangers of releasing or cultivating invasive species in the wild are also necessary.

1. Introduction

The expansion of alien invasive plants is occurring globally and seems like an unstoppable wave, affecting many, if not all, natural ecosystems [1]. Of these, freshwater ecosystems are among the most vulnerable to alien invasive species [2]. When invaded, the body of water and the surrounding land are particularly susceptible to drastic changes in community composition, structure, and biotic interactions [3]. Furthermore, the absence of physical barriers promotes the dispersal and expansion of alien invasive species within the water bodies, especially small lakes, and standing water. Additionally, human activities promote the accidental or deliberate introduction of alien invasive plants and animals into water bodies [4].
The integrity of freshwater ecosystems is highly relevant to humans and their well-being because they provide several relevant ecosystem services, such as drinking water, fisheries, pollution dilution, and recreation, among others [5]. Nevertheless, they are increasingly threatened by human activities such as pollution, eutrophication, and the colonization and expansion of alien invasive species. Furthermore, the impact of alien invasive species is most significant on island ecosystems, which harbor almost half of the world’s endangered biodiversity [6]. Thus, the occurrence of alien invasive species within island water bodies becomes especially relevant. Nevertheless, even though alien invasive species are acknowledged as drivers of biodiversity loss, studies on the pathways, drivers, mechanisms, and effects of alien invasive species are relatively scarce for island water bodies [2].
In Mexico, the island of Cozumel has been granted several protection measures because of its high biodiversity [7,8]. Despite such conservation efforts, several alien invasive species occur on the island. For instance, Castillo-Campos et al. [9] registered the first record of the naturalization of Scaevola taccada (Gaertn.) Roxb. on the beach and coastal dunes of Cozumel. Later, the same authors explored the effects of this Asian invasive species on plant community structure and composition [10]. Similarly, García-Arroyo et al. [11] found that the Eurasian collared-dove (Streptopelia decaocto (Frivaldszky, 1838)), one of the most successive birds worldwide, was very abundant in the urban areas of the island. Additional alien invasive species reported in Cozumel include the lionfish (Pterois volitans (Linnaeus, 1957)) [12]; a tarantula (Brachypelma vagans (Ausserer, 1875)) [13]; and the boa (Boa imperator (Daudin, 1803)) [14]. The island of Cozumel contains several water bodies, but these have not been studied, so it is unknown if alien invasive species have also colonized these. Because of the relative abundance of alien invasive species on the island, and the vulnerability of water bodies to invasion, our premise was that it is very likely that water bodies would also be affected by alien invasives.
In this context, first, we aimed to study the floristic composition of four lagoons located in southeastern Cozumel and assess the occurrence, frequency, and abundance of alien and potentially invasive plants. Second, we report (a) the geographic origin of these alien species, (b) their geographic distribution, and (c) the potential mechanisms of plant invasions on the island inferred from the use of these plants by humans. With this information, we analyze future challenges and make recommendations for preventing and controlling the expansion of alien and potentially invasive species in the lagoons of Cozumel.

2. Results

2.1. Floristic Composition and Sampling Effort

The lagoons sampled are surrounded mainly by or immersed in a low tropical deciduous forest [15] and, to a lesser extent, mangroves (Conocarpus erectus) or flooded forests characterized by Annona glabra L., Cresentia alata Kunth, Erythroxylum confusum Britton, and Bonellia albiflora (Lundell) B. Stahl & Källersjö.
In the inventory of the plots sampled in the 4 lagoons, we registered 43 species (Table 1) of aquatic or underwater flora belonging to 24 families (27 species in lagoon 1; 15 species in lagoon 2; 22 species in lagoon 3; and 7 species in lagoon 4). These species are subject to periodic flooding and are primarily herbaceous. The occurrence of one alga (Chara haitensis) is noteworthy because of its relatively high abundance. This species was the only alga registered in our sampled plots.
Most species belonged to the herbaceous flora, characterized by Bacopa monnieri (L.) Wettst., Ceratophyllum demersum L., Echinodorus berteroi (Spreng.) Fasset, Eleocharis elegans (Kunth) Roem. & Schult., E. geniculata (L.) Roem. & Schult., Marsilea vestita Hook. & Grev., Nymphaea ampla (Salisb.) DC., Paspalidium geminatum (Forssk.) Stapf, Paspalum vaginatum Sw., and Stachytarpheta angustifolia (Mill.) Vahl. These species form dense mats that almost completely cover the humid zone surrounding the water bodies of the four lagoons. Two alien and potentially invasive plants, Paspalum vaginatum and Paspalidium geminatum, were among the most abundant and dominant species.
Notably, two of the species found are native to North America (Mexico inclusive) but are considered aggressive alien invasive plants elsewhere. For instance, Ceratophyllum demersum is distributed worldwide because of its general use in aquariums and ponds. It is a submerged aquatic plant that may form dense monospecific beds, resulting in the exclusion of other plant species [16]. This species is among the 100 worst invasive species worldwide. Bacopa monnieri is also considered native to the Americas, Asia, and Africa but is invasive in Japan, Singapore, Spain, Portugal, and the Cayman Islands. Like Ceratophyllum demersum, Bacopa monnieri grows in aquatic habitats and is an ornamental plant in aquariums and ponds. It has deleterious effects on native plants and animals, water quality, water flow, and sedimentation [17].
The rarefaction analysis based on the number of sampling units shows that species richness did not reach the expected asymptotic value, which indicates the necessity of increasing the number of sampled units. Nevertheless, the estimated cover sample values (CS 0.9642) reveal that the sampling effort was sufficient (72) (Figure 1).

2.2. Floristic Analysis

The cluster analysis distinguished two groups of plant communities (Figure 2). In these plant communities’ groups, the species richness was composed of 15 species in group 1 and 35 species in group 2. The vegetation groups can be distinguished by the species turnover between them and the presence and dominance of some species.
Group 1 contains all the samples from lagoon 2, the one furthest away from the other lagoons (12 km apart, see methods). This group was mainly characterized by five species Eleocharis elegans, Eragrotis prolifera, Bocopa monnieri, Paspalum virgatum, and Nymphoides indica (Table 1).
Group 2 contained all sampled plots from lagoons 1, 3, and 4, possibly owing to the smaller distance between them (250–290 m, see methods) (Figure 2). The lagoons shared many species, but the principal species in group 2 were Echinodorus berteroi, Eleocharis geniculata, Marsilea vestita, Paspalidium geminatum, and Paspalum vaginatum.
It is important to mention that we recorded 6 alien and potentially invasive species (Table 1), and 1–4 of these occurred in each lagoon. In lagoon 1, Cynodon dactylon, Dactyloctenium aegyptium, Paspalidium geminatum, and Paspalum vaginatum were present. In lagoon 2, only D. aegyptium was recorded. In lagoon 3, Nymphae rubra, P. geminatum, P. vaginatum, and Portulaca oleracea were observed. Finally, in lagoon 4, D. aegyptium, Paspalidium geminatum, and Paspalum vaginatum were recorded. Three grass species (Paspalum vaginatum, Paspalidium geminatum, and Dactyloctenium aegyptium) grow in all the lagoons studied. The most abundant alien and potentially invasive species was Paspalum vaginatum, while the least frequent were Cynodon dactylon, Nymphaea rubra, and Portulaca oleracea.

2.3. Relative Frequency and Abundance of Alien and Potentially Invasive Plants

The relative frequency and abundance of the alien plants, potentially invasive in Cozumel, varied between lagoons and between species (Figure 3). In all lagoons, except for lagoon 2, the relative cover of at least two species (Paspalum vaginatum and Paspalidium geminatum) was amongst the highest. In contrast, only 1 alien and potentially invasive species (Dactyloctenium aegyptium) was observed in lagoon 2, with a reduced plant cover. The results demonstrate that alien and potentially invasive plants were dominant in three of the four lagoons. For instance, these species represent 14 and 18% of the flora in lagoons 1 and 3, respectively. The extreme percentages occurred in lagoon 2, with only 1 alien and potentially invasive species representing 7% of the flora, and species-poor lagoon 4, with 3 alien and potentially invasive species representing 43% of the flora.

2.4. Geographic Distribution of the Alien and Potentially Invasive Plants

The worldwide and Mexican distributions of alien plants that are potentially invasive in Cozumel are variable (Figure 4). For instance, Cynodon dactylon, Dactyloctenium aegyptium, and Portulaca oleracea, whose centers of origin are in Africa, the Old World, and Asia, respectively, are widely distributed worldwide and in Mexico (Table 2). Cynodon dactylon is one of the 100 worst invasive species in the world. The local distribution of Paspalum geminatum and Paspalidium vaginatum (native from the USA) in Mexico is reduced. Still, Paspalum vaginatum is another invasive plant among the world’s 100 worst invasive species (Figure 4, Table 2). The least broadly spread alien and potentially invasive species was Nymphaea rubra, native to Asia, recently reported in Cozumel [9]. It is important to state that, so far, we do not have evidence to determine if these alien species can already be considered invasives in the lagoons, although some of them were already very abundant (Paspalum vaginatum and Paspalidium geminatum). Rather, they are considered potentially invasive because they have been reported as invasives in Mexico. Nevertheless, field data is necessary to determine if the species are indeed acting as invasives.

3. Discussion

In this study, we aim to describe the floristic composition of four lagoons located on the southeastern coast of the island of Cozumel and assess the occurrence and abundance of alien and potentially invasive plant species. Our results reveal a total of 43 species of aquatic or underwater flora, which are mostly herbaceous plants, subject to periodic flooding. Six alien and potentially invasive species were notably abundant, especially in three lagoons. Further, 2 are considered among the 100 worst invasive species worldwide, although their abundance in Mexico remains relatively reduced. Five alien and potentially invasive species are terrestrial and grow on the shore of the lagoons, while one is aquatic.

3.1. Alien Potentially Invasive Species

A relatively large number of the species found in the 4 lagoons (13.9%) were alien, and considered potentially invasive, since they have been reported as invasives elsewhere in Mexico and in different types of ecosystems and environments. For example, Cynodon dactylon was considered potentially invasive in the mountain ranges along the Mexican Pacific coast [24] and in northwestern Mexico (Baja California) [25] after its introduction for grazing.
Dactyloctenium aegiptium was also observed on an island located in northwestern Mexico [26] and on coastal dunes in southeastern Mexico [27] and is considered potentially invasive. However, Zaldívar-Cruz et al. [28] did not consider this grass invasive, although it was observed growing in association with the invasive tree Casuarina equisetifolia along the coasts of Cozumel [28]. C. dactylon and D. aegiptium have also been mentioned as alien invasive plants in the riparian zones of the Sonoran Desert [29].
Other species are included in lists of alien invasive species in Mexico, but studies on them for Mexican populations are almost non-existent. For instance, Nymphaea rubra has only been recently recorded in other lagoons in Cozumel and was mentioned as possibly being invasive [10]. Paspalidium geminatum is mentioned as being invasive in Mexico by the National Commission of Biodiversity (CONABIO) [21], and the Global Invasive species database [22] acknowledges Paspalum vaginatum as invasive in Mexico. Portulaca oleracea is also referred to as invasive in Mexico by international databases [23]. However, we did not find scientific studies on these species in Mexico. The above highlights the urgent need for further in-depth studies on these potentially invasive species of Mexico.

3.2. The Routes and Possible Invasion Mechanisms and Impacts of Alien and Potentially Invasive Species in the Lagoons of the Island of Cozumel

The successful colonization and establishment of alien invasive plants depend on different factors: first, invasion pathways; second, driving factors that provide invasion opportunity windows; third, ecological mechanisms that promote a successful invasion. Finally, combining these factors determines the effects of invasive species in natural communities [2]. Next, we describe the possible invasion pathways, invasion drivers, invasion mechanisms, and invasion effects of the alien potentially invasive species found in the lagoons.
Invasion pathways—In aquatic systems, ornamental trade frequently underlies escape from captivity and deliberate release [2]. These actions occur primarily because of a general lack of knowledge regarding the potential danger of released invasive species. In our case, the only truly aquatic potentially invasive plant was Nymphae rubra which is an ornamental plant in ponds. The introduction of this plant to the island is possibly the result of its astonishingly beautiful flowers. Bird dispersal probably contributed to the expansion of this species [8].
The other alien and potentially invasive species observed in our study sites are typically associated with grasslands for cattle ranching. It is likely that they were introduced for cattle and then escaped from these disturbed sites. Some evidence for this is the observed cattle tracks (prints and droppings) in all our study sites and a few individuals of wild boar (Pecari tajacu nanus) grazing on the shores of lagoon 3.
Invasion drivers—Different environmental conditions are relevant for species invasion. Nutrient contents, floristic structure, vegetation density, climate, and hydrology oftentimes play a decisive role in the colonization, establishment, and invasion of alien species [24,25]. Because the lagoons we studied are on an island, the most likely drivers of colonization are human activities (cattle ranching) and decisions (ornamental plants).
Invasion mechanisms—In general, invasive plants show effective dispersal and spread mechanisms [30,31,32]. The seeds of the alien and potentially invasive species found in the four lagoons are tiny, and their dispersion means are associated with wind and the movement of birds because the seeds can become attached to their feathers or legs. Furthermore, because the lagoons are relatively close, dispersion between them is very likely. Additionally, clonal growth of the six species has probably promoted their expansion on the shores of the lagoons [33,34].
Invasion effects— If the observed alien and potentially invasive species expand their cover in the lagoons, it is likely that they will behave as invasives and have a relevant effect in the lagoons. Thus, even though we did not explore the long-term impact on community composition, structure, and dynamics, the high frequency of alien and potentially invasive plants is likely to significantly affect the functional integrity of these lagoons. Further studies are necessary in this regard.

3.3. Future Challenges and Recommendations

The control and management of invasive species require a program that includes a combination of actions [35]: (a) early detection and surveillance of alien and potentially invasive species to determine if they become invasive or not; (b) understanding the relevance of invasive species from a scientific and a socioeconomic point of view; (c) preventing and intercepting alien and potentially invasive species; and (d) control and management of invasive species. In Cozumel, we are only at the beginning with early detection data, and from this, we need to move forward. For instance, it is necessary to determine if these alien species become invasive (or begin to exhibit invasive behavior) as soon as possible. Then, it is necessary to implement, for example, the actions recommended by [35]. Supplementary management actions to control alien invasive plants should include habitat restoration, adequate legislation, collaboration between stakeholders, and raising awareness of the dangers of releasing or cultivating invasive species in the wild [4].

4. Materials and Methods

4.1. Study Site

The study took place on the island of Cozumel, located in the Mexican Caribbean area, 17 km off the eastern coast of the Yucatan Peninsula, Mexico (20°3″ N and 87°3″ W; Figure 1). The climate is warm sub-humid with a mean annual temperature of 26–27 °C and annual rainfall between 800 and 1500 mm. March and April are the driest months, with the highest rainfall in September [36]. Frequently, tropical storms or hurricanes hit the island during the summer, making landfall on the Caribbean part of the island. Human settlements and infrastructure are located on the other side of the island and are better protected from these storms.
The vegetation on the island grows on a highly permeable limestone and sandy substrate. Different ecosystems grow here: sub-deciduous tropical forests, mangrove swamps, wetlands, and coastal dune vegetation [9,10,37,38,39].

4.2. Vegetation Sampling

The vegetation was recorded in four lagoons located on the southeastern side of the island of Cozumel (Caribbean side) (Figure 5). The distances between the 3 lagoons varied between 250 and 290 m (Lagoons 1, 3, 4), and the fourth (Laguna 2) was 11 km from the first. The lagoons studied were selected on the basis of their accessibility and the presence of the water mirror at the time of the study. The lagoons had different dimensions of the body of water present during sampling and the potentially floodable area (Figure 5).
Vegetation sampling was carried out through transects oriented perpendicular to the lagoons, beginning in the water mirror where the floating leaf species grow and ending inland, where the last traces of the maximum rainy season flooding were observed. The length of the transects varied depending on the width of the margin of the water bodies, and the transects were located at different points in each lagoon.
In each transect, we established 1–3 sampling squares that were 5 m wide × 20 m long (100 m2) and separated by 25 m. The first sampled plot was always in the water 10–15 m from the shore, where the water reached a depth of 30–35 cm, and the species with floating leaves occurred. The resulting plots included plants that withstand flooding during the rainy season but are on the land when the water level drops during the dry season. In this way, we included all the species present in the different flooding conditions.
We sampled all woody species in the 100 m2 plots. Then, we recorded herbaceous species in three 2 × 2 m subplots randomly placed within the 100 m2 ones. In each plot and subplot, we listed all the species and visually estimated the percent cover of each one (0–100%). Because of this method, and because plant covers overlapped, the sum of the plant cover of all the species was greater than 100% in the most densely vegetated plots. We sampled 42 plots (100 m2) covering a total area of 4200 m2. The total number of plots sampled in each lagoon was as follows: lagoon 1 = 9 plots; lagoon 2 = 11; lagoon 3 = 20; and lagoon 4 = 2. We sampled 126 subplots (4 m2), corresponding to 504 m2. In this case, the number of subplots per lagoon was as follows: lagoon 1 = 27 subplots (109 m2); lagoon 2 = 33 (132 m2); lagoon 3 = 60 (240 m2); and lagoon 4 = 6 (24 m2). It is important to note that the number of sampled transects, plots, and subplots in each lagoon depended on the size of the water body present at the time of the study (October 2021) and the potentially floodable area at the time of the highest content of water.
Because the Island of Cozumel is a Biosphere Reserve, collecting specimens for scientific collections is not allowed, so the plant species were identified during sampling. When a species could not be determined in situ, we used high-quality photographs taken with a Canon SX270 HS 20x zoom lens for subsequent identification. We employed Family taxonomic keys and performed comparisons with herbarium specimens (XAL). The scientific names of the registered species were corroborated through the electronic databases (Tropicos.org) [40] and online herbaria data (MEXU, XAL), as well as by consulting the floristic lists published for the lagoons and wetlands of the Yucatan Peninsula [36,37,38,39,41].

4.3. Data Analyses

Occurrence and Abundance

Initially, we analyzed the sampling efficiency with a species accumulation curve using the online program iNEXT [42]. Subsequently, we explored the floristic similarity between the sample units using multivariate Hierarchical cluster analysis (UPGMA) and calculated the Jaccard similarity index with PAST 4.11 [43]. This index relates the presence or absence of the species. Using this analysis, we identified floristic affinities between the plots and lagoons. We expected that the sampled plots of each lagoon would be grouped according to their floristic affinities, that is, that four groups would be formed, one for each lagoon.
On the other hand, we obtained the relative importance value (RIV) of each species using Equation (1):
RIV = (RF + RA/2) × 100
where RF is the relative frequency, and RA is the relative coverage (as abundance value). This way, we identified the most important species in the community and each lagoon.

4.4. Distribution Worldwide and in Mexico of the Alien and Potentially Invasive Species

We used previous studies and public databases (Global Invasive Species Database) [16] and CONABIO [44] to determine the status (native or invasive) of the species found in the four lagoons. Then, we designated those species considered invasive in Mexico as potentially invasive in the lagoons of Cozumel, even though we did not collect evidence to confirm their invasiveness (see Table 2). Then, the distributions worldwide and in Mexico of the alien invasive species found in the four lagoons were mapped on the basis of the information from the Global Biodiversity Information Facility [45].

5. Conclusions

This study shows that six alien species are potentially invasive, and of these, three were notably abundant in the lagoons we studied on the island of Cozumel. Although additional studies are still necessary to determine if these alien species are indeed becoming invasives, it is also necessary to understand invasion routes, pathways, mechanisms, and impacts. Using such information, different management actions can be implemented, and these include (a) early detection and surveillance; (b) understanding the relevance of invasive species from a scientific and a socioeconomic point of view; (c) preventing and intercepting invasive species; and (d) control and management of invasive species. Additionally, habitat restoration, adequate legislation, collaboration between stakeholders, and raising awareness of the dangers of releasing or cultivating invasive species in the wild are also necessary.

Author Contributions

Conceptualization, G.C.-C., J.G.G.-F. and M.L.M.; methodology, G.C.-C., J.G.G.-F. and J.J.P.-P.; formal analysis, J.G.G.-F. and M.L.M.; investigation, G.C.-C., J.G.G.-F. and J.J.P.-P.; writing—original draft preparation, M.L.M.; writing—review and editing, G.C.-C., J.G.G.-F. and J.J.P.-P.; funding acquisition, M.L.M. All authors have read and agreed to the published version of the manuscript.

Funding

This project was funded by Centro Mexicano de Innovación en Energía del Océano (CEMIE-Océano), CONACYT-SENER Sustentabilidad Energética FSE-2014-06-249795. MLM received funding from CONACYT for a sabbatical stay at the National Autonomous University of Mexico, Institute of Engineering.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are available upon request.

Acknowledgments

The authors are grateful for the logistic support from the Institute of Engineering (UNAM) and the Institute of Ecology, A.C. (INECOL).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Van Kleunen, M.; Bossdorf, O.; Dawson, W. The ecology and evolution of alien plants. Annu. Rev. Ecol. Evol. Syst. 2018, 49, 25–47. [Google Scholar] [CrossRef]
  2. Bolpagni, R. Towards global dominance of invasive alien plants in freshwater ecosystems: The dawn of the Exocene? Hydrobiologia 2021, 848, 2259–2279. [Google Scholar] [CrossRef]
  3. Cai, H.; Lu, H.; Tian, Y.; Liu, Z.; Huang, Y.; Jian, S. Effects of invasive plants on the health of forest ecosystems on small tropical coral islands. Ecol. Indic. 2020, 117, 106656. [Google Scholar] [CrossRef]
  4. Brundu, G. Plant invaders in European and Mediterranean inland waters: Profiles, distribution, and threats. Hydrobiologia 2015, 746, 61–79. [Google Scholar] [CrossRef]
  5. Millennium Ecosystem Assessment. Ecosystems and Human Well-Being: Synthesis; Island Press: Washington, DC, USA, 2005; pp. 141–282. [Google Scholar]
  6. Glen, A.S.; Atkinson, R.; Campbell, K.J.; Hagen, E.; Holmes, N.D.; Keitt, B.S.; Parkes, J.P.; Saunders, A.; Sawyer, J.; Torres, H. Eradicating multiple invasive species on inhabited islands: The next big step in island restoration? Biol. Invasions 2013, 15, 2589–2603. [Google Scholar] [CrossRef]
  7. SEMARNAT (Secretaría de Medio Ambiente y Recursos Naturales). Programa de Manejo-Área de Protección de Flora y Fauna Norte de la Isla de Cozumel; Gobierno de México: Mexico City, Mexico, 2016; 248p. Available online: https://simec.conanp.gob.mx/pdf_libro_pm/32_libro_pm.pdf (accessed on 10 February 2023).
  8. CONANP (Comisión Nacional de Áreas Naturales Protegidas). Área de Protección de Flora y Fauna Isla de Cozumel. La Porción Norte y la Franja Costera Oriental, Terrestres y Marinas de la Isla de Cozumel. 2021. Available online: https://simec.conanp.gob.mx/ficha.php?anp=32&reg=9 (accessed on 4 March 2023).
  9. Castillo-Campos, G.; Garcia-Franco, J.G.; Martínez, M.L. First record of naturalization of Scaevola taccada (Gaert.) Roxb. (Goodeniaceae) in southern Mexico. BioInvasions Rec. 2021, 10, 425–435. [Google Scholar] [CrossRef]
  10. Castillo-Campos, G.; Martínez, M.L.; García-Franco, J.G.; Vázquez, G.; Pérez-Maqueo, O.; Pale Pale, J. Assessing the impact of an invasive plant in a Protected Natural Area: Island of Cozumel, Mexico. Biol. Invasions 2022, 24, 1511–1526. [Google Scholar] [CrossRef]
  11. García-Arroyo, M.; Gómez-Martínez, M.A.; MacGregor-Fors, I. The queen of the island: On the density and distribution of the Eurasian Collared-Dove (Streptopelia decaocto) in Cozumel. Urban Ecosyst. 2022, 25, 285–290. [Google Scholar] [CrossRef]
  12. Bogdanoff, A.K.; Mostowy, J.; Peake, J.; Layman, C.A.; Bermudez, A.B.; Baca, C.G.; Palacios, N.H.; Gonzalez, D.T.M.; Del Rocio Bravo Xicoténcatl, M.; Morris, J.A., Jr. A brief description of invasive lionfish (Pterois sp.) diet composition in the Arrecifes de Cozumel National Park. Food Webs 2018, 17, e00104. [Google Scholar] [CrossRef]
  13. Machkour-M’Rabet, S.; Vilchis-Nestor, C.A.; Barriga-Sosa, I.D.L.A.; Legal, L.; Hénaut, Y. A molecular approach to understand the riddle of the invasive success of the tarantula, Brachypelma vagans, on Cozumel Island, Mexico. Biochem. Syst. Ecol. 2017, 70, 260–267. [Google Scholar] [CrossRef]
  14. Suárez-Atilano, M.; Cuarón, A.D.; Vázquez-Domínguez, E. Deciphering geographical affinity and reconstructing invasion scenarios of Boa imperator on the Caribbean Island of Cozumel. Copeia 2019, 107, 606–621. [Google Scholar] [CrossRef]
  15. Miranda, F.; Hernández-X, E. Los tipos de vegetación de México y su calsificación. Bol. Soc. Bot. Méx. 1963, 28, 29–179. [Google Scholar] [CrossRef]
  16. Global Invasive Species Database. Available online: http://www.iucngisd.org/gisd/ (accessed on 13 February 2023).
  17. CABI Digital Library. Available online: https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.112638 (accessed on 13 February 2023).
  18. Global Invasive Species Database. Species Profile: Cynodon dactylon. 2023. Available online: http://www.iucngisd.org/gisd/speciesname/Cynodon+dactylon (accessed on 9 March 2023).
  19. CONABIO. Malezas de México: Dactyloctenium aegyptium. Available online: http://www.conabio.gob.mx/malezasdemexico/poaceae/dactyloctenium-aegyptium/fichas/ficha.htm (accessed on 13 February 2023).
  20. Monaco Nature Encyclopedia. Discovery the Biodiversity: Nymphaea rubra. Available online: https://www.monaconatureencyclopedia.com/nymphaea-rubra/?lang=en (accessed on 10 March 2023).
  21. CONABIO. Malezas de México: Paspalidium geminatum. Available online: http://www.conabio.gob.mx/malezasdemexico/poaceae/paspalidium-geminatum/fichas/ficha.htm (accessed on 15 February 2023).
  22. Global Invasive Species Database. Species Profile: Paspalum vaginatum. 2023. Available online: http://www.iucngisd.org/gisd/speciesname/Paspalum+vaginatum (accessed on 9 March 2023).
  23. PlantUse: Portulaca oleraceae. Available online: https://uses.plantnet-project.org/en/Portulaca_oleracea_(PROTA) (accessed on 8 March 2023).
  24. Pérez-Postigo, I.; Vibrans, H.; Bendix, J.; Cuevas-Guzmán, R. Floristic composition and potential invasiveness of alien herbaceous plants in Western Mexico. Rev. Biol. Trop. 2021, 69, 1037–1054. [Google Scholar] [CrossRef]
  25. Palma-Ordaz, S.; Delgadillo-Rodríguez, J. Potential distribution to eight alien species with invasive nature in the state of Baja California, Mexico. Bot. Sci. 2014, 92, 587–597. [Google Scholar] [CrossRef]
  26. Vanderplank, S.E.; Rebman, J. Thirteen new weeds on Cedros Island, Baja California, Mexico. Acta Bot. Mex. 2021, 128, e1823. [Google Scholar] [CrossRef]
  27. Parra-Tabla, V.; Albor-Pinto, C.; Tun-Garrido, J.; Angulo-Pérez, D.; Barajas, C.; Silveira, R.; Otíz-Díaz, J.J.; Arceo-Gómez, G. Spatial patterns of species diversity in sand dune plant communities in Yucatan, Mexico: Importance of invasive species for species dominance patterns. Plant Ecol. Divers. 2018, 11, 157–172. [Google Scholar] [CrossRef]
  28. Zaldívar-Cruz, B.; Pérez-Ceballos, R.; Zaldívar-Jiménez, A.; Canales-Delgadillo, J.; Endañu-Huerta, E.; Flores, A.; Tun-Garrido, J. Structural and diversity changes in coastal dunes from the Mexican Caribbean: The case of the invasive Australian pine (Casuarina equisetifolia). Manag. Biol. Invasions 2022, 13, 131. [Google Scholar] [CrossRef]
  29. Van Devender, T.R.; Felger, R.S.; Búrquez, A. Exotic plants in the Sonoran Desert region, Arizona and Sonora. In Proceedings of the California Exotic Pest Plant Council Symposium, Concord, CA, USA, 2–4 October 1997; California Exotic Pest Plant Council: Concord, CA, USA, 1997. [Google Scholar]
  30. Hussner, A.; Heidbüchel, P.; Coetzee, J.; Gross, E.M. From introduction to nuisance growth: A review of traits of alien aquatic plants which contribute to their invasiveness. Hydrobiologia 2021, 848, 2119–2151. [Google Scholar] [CrossRef]
  31. Bernez, I.; Aguilar, F.; Violle, C.; Ferreira, T. Invasive river plants from Portuguese floodplains: What can species attributes tell us? Hydrobiologia 2006, 570, 3–9. [Google Scholar] [CrossRef]
  32. Pattison, Z.; Vallejo-Marin, M.; Willby, N. Riverbanks as battlegrounds: Why does the abundance of native and invasive plants vary? Ecosystems 2019, 22, 578–586. [Google Scholar] [CrossRef]
  33. Proctor, C.A.; Gaussoin, R.E.; Reicher, Z.J. Vegetative reproduction potential of common purslane (Portulaca oleracea). Weed Technol. 2011, 25, 694–697. [Google Scholar] [CrossRef]
  34. Chen, D.; Ali, A.; Yong, X.-H.; Lin, C.-G.; Niu, X.-H.; Cai, A.-M.; Dong, B.-C.; Zhou, Z.-X.; Wang, Y.-J. A multi-species comparison of selective placement patterns of ramets in invasive alien and native clonal plants to light, soil nutrient and water heterogeneity. Sci. Total Environ. 2019, 657, 1568–1577. [Google Scholar] [CrossRef] [PubMed]
  35. Colmenárez, Y.; Vásquez, C.; Gomes Fidelis, E.; Corniani, N. Biological control as a key tool for the management of invasive species in Latin America and the Caribbean. In Agricultural, Forestry and Bioindustry Biotechnology and Biodiscovery; Chong, P.A., Newman, D.J., Steinmacher, D.A., Eds.; Springer Nature: Cham, Switzerland, 2020; pp. 357–386. [Google Scholar]
  36. Orellana, R.; Nava, F.; Espadas, C. El clima de Cozumel y la Riviera Maya. Biodiversidad acuática de la Isla de Cozumel. In Biodiversidad Acuática de la Isla de Cozumel; Mejía-Ortiz, L.M., Ed.; Universidad de Quintana Roo, Plaza y Valdés: Mexico City, Mexico, 2007; pp. 23–32. [Google Scholar]
  37. Téllez-Valdés, O.; Cabrera, E.F.; Linares, E.; Bye, R. Las Plantas de Cozumel. Guía Botánico-Turística de la Isla de Cozumel, Quintana Roo; Instituto de Biología, Universidad Nacional Autónoma de México: Mexico City, Mexico, 1989; p. 75. [Google Scholar]
  38. Flores, J.S.; Espejel, I. Tipos de Vegetación de la Península de Yucatán; Fascículo 3. Etnoflora Yucatanense; Universidad Autónoma de Yucatán: Mérida, Mexico, 1994. [Google Scholar]
  39. Collantes-Chávez-Costa, A.; Alanís-Rodríguez, E.; Yam-Uicab, O.; López-Contreras, C.; Sarmiento-Muñoz, T.; Tapia-Muñoz, J.L. Composition, structure and diversity of coastal vegetation in the northeastern of Cozumel, Mexico. Bot. Sci. 2019, 97, 135–147. [Google Scholar] [CrossRef]
  40. Tropicos.org. Missouri Botanical Garden. Available online: https://tropicos.org (accessed on 4 February 2023).
  41. Subdirección de Ecología. Inventario de Flora y Fauna de la Isla de Cozumel. Ayuntamiento de Cozumel, Q. Roo., México. 16p. 2021. Available online: https://cozumel.gob.mx/wp-content/uploads/2019/05/ART93-INCISO-L.pdf (accessed on 16 February 2023).
  42. Chao, A.; Ma, K.H.; Hsieh, T.C. iNEXT Online: Software for Interpolation and Extrapolation of Species Diversity. Program and User’s Guide. Available online: http://chao.stat.nthu.edu.tw/wordpress/software_download/inext-online/ (accessed on 15 January 2023).
  43. Hammer, Ø.; Harper, D.T.; Ryan, P.D. Paleontological Statistical Software package for education and data analysis. Palaeontol. Electron. 2022, 4, 9. [Google Scholar]
  44. Comité Asesor Nacional sobre Especies Invasoras. Estrategia Nacional Sobre Especies Invasoras en México, Prevención, Control y Erradicación; Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Comisión Nacional de Áreas Protegidas, Secretaría de Medio Ambiente y Recursos Naturales: Mexico City, Mexico, 2010; p. 91.
  45. Global Biodiversity Information Facility. Available online: https://www.gbif.org (accessed on 2 February 2023).
Figure 1. Rarefaction curves for species richness (q0) calculated with incidence values of the plant species found in four lagoons on the island of Cozumel in Quintana Roo, Mexico.
Figure 1. Rarefaction curves for species richness (q0) calculated with incidence values of the plant species found in four lagoons on the island of Cozumel in Quintana Roo, Mexico.
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Figure 2. Cluster analysis based on Jaccard index shows floristic similarity between the sampled plots. Dashed red lines differentiate vegetation groups. Color labels in each group show the plots sampled in each lagoon: Black = Lake 1, Green = Lake 2, Blue = Lake 3, and Red = Lake 4.
Figure 2. Cluster analysis based on Jaccard index shows floristic similarity between the sampled plots. Dashed red lines differentiate vegetation groups. Color labels in each group show the plots sampled in each lagoon: Black = Lake 1, Green = Lake 2, Blue = Lake 3, and Red = Lake 4.
Plants 12 01918 g002
Figure 3. Relative frequency and cover of the six alien and potentially invasive species compared with the native plants observed in four lagoons on the island of Cozumel, Mexico. Red arrows and circles indicate the potentially invasive species. The acronyms are related to the species in Table 1.
Figure 3. Relative frequency and cover of the six alien and potentially invasive species compared with the native plants observed in four lagoons on the island of Cozumel, Mexico. Red arrows and circles indicate the potentially invasive species. The acronyms are related to the species in Table 1.
Plants 12 01918 g003aPlants 12 01918 g003b
Figure 4. Geographic distribution of the six alien and potentially invasive species found in four lagoons on the island of Cozumel, Mexico, based on the Global Biodiversity Information Facility (GBIF) database (https://www.gbif.org/, accessed on 13 February 2023). Inserted subfigures (af) show maps with the global distribution of each species. Each point indicates a record of the species in a locality. The orange-reddish dots represent a larger number of records at that location. Inserted photos: under creative commons license.
Figure 4. Geographic distribution of the six alien and potentially invasive species found in four lagoons on the island of Cozumel, Mexico, based on the Global Biodiversity Information Facility (GBIF) database (https://www.gbif.org/, accessed on 13 February 2023). Inserted subfigures (af) show maps with the global distribution of each species. Each point indicates a record of the species in a locality. The orange-reddish dots represent a larger number of records at that location. Inserted photos: under creative commons license.
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Figure 5. (a) Location of the island of Cozumel in the state of Quintana Roo, southeastern Mexico. The numbers indicate the lagoons studied. (b) Studied lagoons. In each lagoon, the red line shows the surface that is potentially flooded during heavy rainfalls. The flooded surface is shown in the inserted values. Images from Google Earth.
Figure 5. (a) Location of the island of Cozumel in the state of Quintana Roo, southeastern Mexico. The numbers indicate the lagoons studied. (b) Studied lagoons. In each lagoon, the red line shows the surface that is potentially flooded during heavy rainfalls. The flooded surface is shown in the inserted values. Images from Google Earth.
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Table 1. Aquatic and subaquatic species observed in four lagoons located in southeastern Cozumel, Mexico. Acronyms of each species are shown. Asterisks indicate the alien and potentially invasive plants found. The relative importance values are shown for each species and for each lagoon; bold letters indicate the largest values in each lagoon.
Table 1. Aquatic and subaquatic species observed in four lagoons located in southeastern Cozumel, Mexico. Acronyms of each species are shown. Asterisks indicate the alien and potentially invasive plants found. The relative importance values are shown for each species and for each lagoon; bold letters indicate the largest values in each lagoon.
FamilySpeciesAcronymsL1L2L3L4
Alismataceae Echinodorus berteroi (Spreng.) FassetEch ber16.6014.421.3
Amaranthaceae Blutaparon vermiculare (L.) MearsBlu ver2.9000
Apocynaceae Asclepias curassavica L.Asc cur000.10
AsteraceaeMelanthera aspera (Jacq.) Steud. ex SmallMel asp0.7000
CeratophyllaceaeCeratophyllum demersum L.Cer dem11.70.57.70
CharaceaeChara haitensis D. E. BertholdCha hai002.00
CombretaceaeConocarpus erectus L.Con ere0.5000
Convolvulaceae Evolvulus alsinoides (L.) L.Evo als000.80
Cordiaceae Cordia curassavica (Jacq.) Roem. & Schult.Cor cur0.3000
CyperaceaeCyperus elegans L.Cyp ele0.5000
Cyperus ligularis L.Cyp lig1.400.50
Eleocharis elegans (Kunth) Roem. & Schult.Ele ele025.300
Eleocharis geniculata (L.) Roem. & Schult.Ele gen4.510.05.42.1
Eleocharis mutata (L.) Roem. & Schult.Ele mut01.100
Rhynchospora holoschoenoides (Rich.) HerterRhy hol00.400
Rhynchospora plumosa ElliottRhy plu000.10
Erythroxylaceae Erythroxylum confusum BrittonEry conf00.400
Fabaceae Centrosema virginianum (L.) Benth.Cen vir0.300.40
Pithecellobium keyense BrittonPit key0.5000
Lythraceae Ammannia coccinea Rottb.Amm coc1.100.50
MarsileaceaeMarsilea vestita Hook.& Grev.Mar ves4.9018.423.5
Menyanthaceae Nymphoides indica (L.) KuntzeNym ind05.400
Nymphaeaceae Nymphaea ampla (Salisb.) DC.Nym amp6.73.08.20
Nymphaea capensis Thunb.Nym cap000.30
Nymphaea rubra Roxb. ex Salisb. *Nym rub000.50
PlantaginaceaeAngelonia angustifolia Benth.Ang ang0.3000
Bacopa monnieri (L.) Wettst.Bac mon0.514.50.70
Poaceae Cynodon dactylon (L.) Pers. *Cyn dac0.6000
Dactyloctenium aegyptium (L.) Willd. *Dac aeg0.41.602.0
Eragrostis prolifera (Sw.) Steud.Era pro0.54.300
Panicum amarum ElliottPan ama1.67.400
Paspalidium geminatum (Forssk.) Stapf *Pas gem5.708.84
Paspalum vaginatum Sw. *Pas vag13.709.520.2
Paspalum virgatum L.Pas vir012.200
Sporobolus virginicus (L.) KunthSpo vir002.60
PortulacaceaePortulaca oleracea L. *Por ole000.10
Portulaca pilosa L. Por pil0.700.80
Primulaceae Bonellia albiflora (Lundell) B. Ståhl & KällersjöBon alb0.7000
Rubiaceae Borreria densiflora DC.Bor den01.400
Sapotaceae Sideroxylon americanum (Mill.) T.D. Penn.Sid ame0.4000
Verbenaceae Lippia nodiflora (L.) Michx.Lip nod18.518.5416.226.9
Stachytarpheta angustifolia (Mill.) VahlSta ang3.51.41.90
VitaceaeCissus trifoliata (L.) L.Cis tri0.4000
Table 2. Attributes of the six alien and potentially invasive plants found in four lagoons on the island of Cozumel. The acronyms of each species are explained in Table 1.
Table 2. Attributes of the six alien and potentially invasive plants found in four lagoons on the island of Cozumel. The acronyms of each species are explained in Table 1.
SpeciesHabitatGrowth FormUseStatus in MexicoOriginUICN StatusReference
Cyn dacTerrestrialHerbCattleInvasiveAfrica100 worst [18]
Dac aegTerrestrialHerbCattleInvasiveOld World [19]
Nym rubFreshwaterHerbOrnamentalInvasiveAsia [20]
Pas gemTerrestrialHerbUnknownIntroducedUSA [21]
Pas vagTerrestrial/FreshwaterHerbCattleInvasiveUSA100 worst [22]
Por oleTerrestrialHerbFoodOld exotic (invasive)Asia [23]
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Castillo-Campos, G.; García-Franco, J.G.; Martínez, M.L.; Pale-Pale, J.J. Alien and Potentially Invasive Plants in Four Lagoons on the Island of Cozumel, Mexico. Plants 2023, 12, 1918. https://doi.org/10.3390/plants12091918

AMA Style

Castillo-Campos G, García-Franco JG, Martínez ML, Pale-Pale JJ. Alien and Potentially Invasive Plants in Four Lagoons on the Island of Cozumel, Mexico. Plants. 2023; 12(9):1918. https://doi.org/10.3390/plants12091918

Chicago/Turabian Style

Castillo-Campos, Gonzalo, José G. García-Franco, M. Luisa Martínez, and J. Jesús Pale-Pale. 2023. "Alien and Potentially Invasive Plants in Four Lagoons on the Island of Cozumel, Mexico" Plants 12, no. 9: 1918. https://doi.org/10.3390/plants12091918

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