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Performance of coronarium J. Koenig and associated local flora community in the Alto de San Miguel, Caldas, Antioquia

Estudiante Daihana Arango Vásquez

Director(es) Estela María Quintero Vallejo PhD Dino Jesús Tuberquia Muñoz

Trabajo de Grado En la modalidad de Investigación

Programa de Ecología Universidad CES Medellín Junio 2020

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10 de junio de 2020.

Se informa que el estudiante Daihana Arango Vásquez identificado con cédula: No. 1037656017 ha concluido de manera satisfactoria su trabajo de grado titulado “Performance of Hedychium coronarium J. Koenig and associated local flora community in the Alto de San Miguel, Caldas, Antioquia”.

En calidad de director(es) del proyecto en mención, y luego de haber revisado con detalle y alto rigor científico y académico el presente documento final, se aprueba este Trabajo de Grado como requisito parcial para optar al título de Ecóloga.

Estela María Quintero Vallejo Dino Jesús Tuberquia Muñoz Cédula: 43612238 Cédula: 71696411 Docente Universidad CES Docente Universidad CES

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Performance of Hedychium coronarium J. Koenig and associated local flora community in the Alto de San Miguel, Caldas, Antioquia Comportamiento de Hedychium coronarium J. Koenig y la comunidad de flora local asociada en el Alto de San Miguel, Caldas, Antioquia

Daihana Arango Vásquez

Resumen

Introducción. El efecto de la flora nativa sobre las especies de plantas invasoras está ganando una alta importancia ya que pueden reducir el riesgo de invasión en ecosistemas naturales. En este estudio examinamos el efecto de la densidad de especies, composición, cobertura, abundancia y hábito de crecimiento de las especies locales sobre el tamaño y crecimiento de Hedychium coronarium en la cuenca del rio Medellín, Colombia. Métodos. En el Alto de San Miguel, Antioquia, georreferenciamos los sitios donde se establece H. coronarium y medimos el tamaño de parches en un trayecto de 2 km de rio. Esto se realizó por medio de la aplicación Avenza maps. Realizamos un modelo lineal generalizado mixto (MGLM), donde evaluamos el efecto de las variables asociadas con lo flora local como la densidad de especies, densidad de individuos y cobertura de especies herbáceas y rastreras, índice de hábito de crecimiento y composición de especies, como variables predictivas del área de los parches; las variables respuesta fueron número y longitud de pseudotallos alcanzados por H. coronarium Resultados. Hallamos qué en este trayecto, H. coronarium ocupa alrededor de 0.2 ha, en 211 parches de tamaño variable. Encontramos un efecto negativo significativo de la densidad de especies sobre el área de los parches, es decir, parches pequeños suelen tener mayor densidad de especies que parches grandes. Adicionalmente encontramos que parches pequeños tienden a tener pseudotallos pequeños en comparación con parches grandes. Discusión y conclusiones. Los resultados de este estudio, complementado con observaciones en campo, sugieren que los sitios donde H. coronarium se ha establecido, proveen condiciones que pueden o no, favorecer su crecimiento. Por ejemplo, los sitios más perturbados en el alto de San Miguel presentan los parches de menor tamaño. Esta investigación ofrece una línea base para futuras investigaciones que conduzcan a evaluar los mecanismos responsables de la resistencia a la invasión percibida en este estudio.

Palabras clave: Hedychium coronarium, resistencia a la invasión, composición de especies, riqueza de especies, rio Medellín

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Nota sobre formato del trabajo de grado

El siguiente artículo ha sido formateado de acuerdo a las instrucciones para autores de la revista Biological invasions, las cuales se pueden consultar vía web en: https://www.springer.com/journal/10530/submission-guidelines (revisado el 10 de Junio de 2020).

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Performance of Hedychium coronarium J. Koenig and associated local flora community in the Alto de San Miguel, Caldas, Antioquia

Daihana Arango Vásquez - Estela Quintero-Vallejo- Dino Tuberquia

Authors information

D. Arango-Vásquez

Universidad CES, Facultad de Ciencias y Biotecnología, Programa de Ecología, Medellín, Antioquia, Colombia

Email: [email protected]

E. Quintero-Vallejo

Universidad CES, Facultad de Ciencias y Biotecnología, Grupo de investigación Biologia CES, programa de Ecología, Medellín, Antioquia, Colombia.

D. Tuberquia

Universidad CES, Facultad de Ciencias y Biotecnología, Grupo de investigación Biologia CES, programa de Biología, Medellín, Antioquia, Colombia.

Declarations

Funding: This study was funding by Secretaría de Medio Ambiente de Medellín

Conflict of interest statement: The authors declare that there is no conflict of interest or involvement in any organization or entity with any financial interest, to submit this manuscript.

Ethics approval: Comité de Ética y biodiversidad Universidad CES

Consent to participate: All the authors consent their participation in the work

Consent for publication: All the author's consent their publication of the work

Availability of data and material: The datasets generated and analyzed during the current study are not publicly available due to they are part of a dissertation that needs to be evaluated and approved before it gets into the world, but are available from the corresponding author on reasonable request.

Code availability: R 1.2.5033, Info Stat and ArcGis 10.2.2

Authors’ contribution: All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Daihana Arango-Vásquez, Estela Quintero-Vallejo and Dino Tuberquia. The first draft of the manuscript was written by Daihana Arango-Vásquez and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Abstract

Effect of local flora on invaders is gaining high importance since it could lower the risk of invasion of the natural ecosystems. We examined the link between the species density, composition, cover, abundance and growth habit of local species and patch area and growth of Hedychium coronarium in the river basin of Medellín, Colombia. The total area occupied by the patches of H. coronarium in the Alto de San Miguel was quantified. Using a Multiple General Linear Mixed-effects Models (MGLM), we evaluated the effect of the variables associated with local flora, like species density, index of habit growth, individual density, species composition and cover over the patch area reached by the invader. We found that species density such as Selaginella silvestris, Drymaria cordata, Commelinaceae sp, Justicia candelariae among others, had a significant negative effect over the patch area of H. coronarium, this means that as the density of species increases, the area decreases. We did not find a significant effect with the variables index of habit growth, individual density, species composition and cover. This research offers a baseline from which further experimental work can be conducted to determine the mechanisms responsible for invasion resistance exhibited in this study.

Key words: Hedychium coronarium, invasion resistance, species composition, richness of species, Medellin river.

Introduction

Hedychium coronarium J. Koenig is an herbaceous, rhizomatous and perennial macrophyte plant that is associated with humid environments, belonging to the family (Macedo 2009), native of the Himalayas and southern and has been widely distributed because of its attractive flowers, fragrance and other economic uses (CABI 2013). The plant has a prolific growth, forming dense and monospecific thickets that colonize new sites from fragments of its , which do not allow the establishment of native flora (CABI 2013; Aguilar-Garavito 2017; Cano-Salazar et al. 2020). Those traits are responsible for its categorization as a plant with invasive potential in Colombia (Cárdenas-López et al. 2017). In the country, it is distributed in several regions in the North, center and in the main valleys of the Andes, and towards the Amazon basin (Aguilar-Garavito et al. 2012)

Ecological interactions of Hedychium species have been explored regarding the influence of this plant in the diversity and establishment of native flora and ecological processes of the forest. For instance, in sites where Hedychium gardnerianum grows it becomes very dominant and affects native species seedlings (Minden et al. 2010). Besides, H. gardnerianum affects the succession process by decreasing the seedling of native species and leading changes in seedling composition favoring species only with big seeds (Williams et al. 2003). Hedychium species also affect ecological processes such as nutrient cycling speeding the decomposition process but decreasing nitrogen availability (Funk et al. 2008). Several studies have found that it affects the establishment of riparian species seedlings (Costa et al. 2019) and the establishment of native in general in (Chiba de Castro et al. 2016)

Most of the studies have focused on the effect of the invader in the community. Nevertheless, our observations suggest that local flora could have an effect on H. coronarium stands. In fact, species richness, abundance, composition, and functional diversity of the native flora, have been reported as a mechanism from communities to resist invasions. Species richness of native flora decreases resources for the (Elton 1958; Stachowicz et al. 1999; McGlone et al. 2011); likewise, abundance has a negative effect on growth of invasive species (Michelan et al. 2013). On the other hand, invasive and phylogenetically related local species and functionally related species keep under control the invasion by decreasing invasive biomass and competing for 7

the same resources, such as graminoids and aquatic plants (Symstad 2000; Hooper and Dukes 2010; Petruzzella et al. 2020).

In places that are important for conservation of diversity and ensure ecosystem services such as national parks and reserve zones, the presence of H coronarium can be a threat to the conservation objectives of those areas. For example, H coronarium has been reported covering large areas in the Otún Quimbaya Wildlife and Fauna Sanctuary (SFFOQ) (PNN 2007) and where they founded that H. coronarium can replace native flora and modify soil properties, from alteration of the biogeochemical cycles to loss of diversity (Gonzalez Gutierrez and Mejia Diaz 2015), additionally it has been reported growing in reserve areas such as Alto de San Miguel, which provides recreation sites for the inhabitants of the city and also preserves the waters of the most important river of the city. In this area, this species has been reported growing on the banks of the Medellin River, where it forms large stands and that it could be interacting negatively with local native species (Vargas et al. 2018).

In this work, we wanted to study the relationships between H coronarium with the local flora in Alto de San Miguel, we evaluated the relationship between native species richness and composition at Alto de San Miguel, with the area of patches and length of pseudostems of H. coronarium. Our hypothesis is that H. coronarium patches would be affected by the richness, composition, and abundance, of local flora, in the form of smaller patches and pseudostems in response.

Methods

Area and study sites

The Alto de San Miguel is a Regional Protective Forest Reserve (6°02’N 75°36’W) (Fig. 1),is a cloud forest within the Altoandino ecosystem fog forest, this ecosystem maintains a high humidity. The life zone corresponds to a very humid low mountain forest (bmh-MB) (Holdridge 1967), with an average annual temperature of 14.5 °C and an annual precipitation of 2,500 and 3,600 mm (CEA and Corantioquia 2002). Alto de San Miguel is an area of high importance for the supply of ecosystem goods and services; it contains strategic ecosystems of the Cordillera Central, that divides two major basins of the Cauca and Aburrá rivers (CEA and Corantioquia 2002; Vargas et al. 2018). The study site was focused on the edge of both sides of the river basin covering about 2 km that correspond to a touristic path (Fig. 1). Along the path, we marked sites where H. coronarium was growing (hereafter called patches) using Avenza Maps®. We marked the periphery of each patch using the same app and points were joined shaping the polygon occupied by H. coronarium with the ArcGIS 10.2.2 program. Patches were separated 3 m from each other. After drawing 211 polygons, we found a high variability on areas (0.43-153m2) therefore we decided to divide the sampling effort in three categories: small, medium, and large. Small ranged in areas between 0.43- 2.9 m2, medium between 3 -10 m2, and large 11-153 m2. We decided to establish these categories to cover the whole variability of patch areas and reduce the sampling effort from 211 to 30 patches.

Length and number of pseudostems

From 211 patches, we selected 30 patches corresponding to 10 patches per category. Selection of 10 patches was made based on the median inside of each category. On every patch we measured and counted all pseudostems of H. coronarium in a 1 m2 plot. Stems less than 30 cm were discarded as we observed that inside a patch, pseudostems of this area may not be able to increase in area. Measurements and counts of pseudostems were performed in a single plot per patch in the 30 patches.

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Diversity measurements

The diversity was measured in an area correct by patch category, being equivalent to 30% of the patch area. In the case of small patches, the same pseudostems measurement plot also corresponded to the one of diversity. In the medium patches we made 2 plots and in the large ones 5-8. On each plot we counted the number of individuals of each species when possible, when it was not, we estimated the percentage of species cover on each plot. These measurements are what we will call individuals density, species density and cover. A large proportion of the identification was made on the field with the help of a botanical expert, the remaining unidentified flora was collected for identification. Additionally, we recorded the flora that grows in the adjoin of H. coronarium on each patch with the aim to characterize better the habitat where H. coronarium is growing and identify if there is any pattern in the local flora over the invader.

Data analyses

With the aim to test the relationships between patch area and pseudostems length and patch area and pseudostems number, we performed Spearman correlations. For these correlations we used information of all patch area categories, and also, we performed it inside each patch area category. With species composition data, we conducted a principal component analysis with a matrix of frequency of species in each patch, the first component explained 15.2% of the variability of data and the second component explained 8.5%. In spite of its low percentage, the first component was used in a MGLM (see below). Species density was the count of species present in each patch, individual density was the count of individual present in each patch and cover was the percentage of cover in each plot. We calculated a habit growth index for which we assigned values to the growth habit type for each individual on each patch. Growth habit type was described as 1 for trees, 2 for shrubs, 3 for vines, ferns, and epiphytes and 4 for reptants and 5 for herbaceous growth habit. Herbaceous habit had the higher designation because of the ecological similarity with H. coronarium. Ecological similarity was based on the presumption that native species more related to invasive species will have a greater overlap of niche and thus greater competition for resources (Darwin 1859). Finally, we added all recorded habit types per patch, and we divided this by the number of individuals present in the patch.

A Multiple General Linear Mixed-effects Models (MGLM) was applied to test the effect of variables associated with diversity such as species density, individuals density, cover , composition (first principal component) and index of habit growth on number of pseudostems, length of pseudostems and patch area. Model with better AIC was selected for testing significant coefficients. Correlations of Spearman were used too, to correlate the variables species composition, species density, individual’s density and index of habit growth and cover with the variables patch area, length of pseudostems and number of pseudostems. All the analyses were conducted using R 1.2.5033 and the Info Stat program. Statistical significance was defined as p < 0.05. The adjoin flora was not included in the MGML and any other statistical test since the records were no systematic. 9

Fig. 1 Map of the study area located in the Alto de San Miguel along the Medellin river

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Results

Distribution and categorization of area for patches

We recorded in total 211 patches of H. coronarium in our sampled area. The area of the patches ranged from 0.43 m2 to 153 m2 (Table 1), which added a total area of 0.23 hectares in 2 km along the river (Fig. 2). We observed that H. coronarium tends to grow in patches of small area (less than 3 m2) since 43% of the patches corresponded to this category of area, additionally, they have the smallest standard deviation. The percentage of medium and large patches were 31 and 25% respectively. The number of large patches was fewer in comparison with other area categories, but at the same time it had the highest variation in area, where 3.24% of the patches reached an area superior of 50 m2. The sampled sites had distinctive characteristics according to the de patch type, for example, 90% of the small patches were on the banks of the river with direct exposure of sunlight, 50% of the medium patches were distributed on the banks of the river and edges of the road and the other 50% in the vicinity of early forest successions with a greater proportion of arboreal species growing up around. While 90% of large patches were distributed within early and secondary successions of forest, shaded sites, and waterlogged soils, the remaining 10% was distributed in free areas but accompanied by shade of trees.

Table 1 Distribution of number of patches per category with their respective measurement range and average patch area Category Number Patch area Average patch area of patches range (m2) range ± SD (m2) Small 92 0.43-2.9 1.68 ± 0.66 Medium 67 3.0-10 5.95 ± 2.11

Large 54 11-153 33.52 ± 28.18

Length and number of pseudostems

Regarding the length of pseudostems, we found considerable variation in length within each patch area, with large patches showing the greatest standard deviation (Table 2, Fig. 3). Small patches tended to have shorter and less variable areas of pseudostems (60-76 cm) than medium and large patches that had on average bigger pseudostems but very variable (60-130 cm). We found a significant relationship between the area of the patches and the average length of pseudostems when we considered the whole range of patch areas (r = 0.38, p = 0.04). Nevertheless, when we look per area category, we did not find significant relationship between the area of the patches and the average length of pseudostems for small (r =0.15, p = 0.68), medium (r = -0.17,p= 0.64) and large patches (r =0.30, p =0.39) (Fig. 3). The number of pseudostems does not increase as the patch increases in area, the medium area patches tend to have higher number of pseudostems but with high variability. There was no significant relationship between the area of the patch and average number of pseudostems inside each category (small r = 0.14, p = 0.70; medium r =0.11, p = 0.76; and large patches r = 0.06, p= 0.87).

Table 2 Average and standard deviation (mean ± SD) of length and density pseudostems of Hedychium coronarium according to each area category

Category Length of Density of pseudostems (cm) ± pseudostems /m2 ± SD SD

Small 70.80 ± 25.89 36.9 ± 14.1 Medium 91.25 ± 36.15 45 ± 22.9 Large 97.59 ± 45.45 40.5 ± 9.6

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Fig. 2 Distribution map of the patches of Hedychium coronarium. Small patches are represented by red stars, medium patches by white circles and large patches by blue triangles.

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Fig. 3 Boxplot (a) average area of pseudostems per m2 for each patch area category for Hedychium coronarium (b) average number of pseudostems of H. coronarium per m2 for each patch category

Diversity

Flora inside the plots and adjoin flora

We evaluated richness and composition for 23 patches. In total were found 277 individuals and 45 families (See supplementary material), the families with the highest richness correspond to Poaceae (10), Asteraceae (10), Araceae (6), Rubiaceae (5), Piperaceae (4), Lamiaceae (4) and Urticaceae (4). The 60% of the families were represented by only one species. We recorded 94 species from which 45 species could be identified until species status with other 49 species are still to be identified. The most frequent species among all the patches was Selaginella silvestris with 30 records. Regarding the growth habit, the most common habit was herbaceous, and the less common habits were epiphyte and ferns. Distribution of the growth habits differ among patches with large patches having all types of growth habits. (Fig. 4). Cover was very variable inside each patch, and it was highest in small patches (Table 3). On the other hand, individual density was not so variable and medium patch had the highest cover mean (Table 3).

Concerning the native flora growing adjoin the patches, we found that medium and large patches were accompanied by a major proportion of individuals of tree and shrubs habit compared to small patches (Fig. 4). In total we find 114 individuals distributed in 21 families. The families with the highest number of records of individuals were Euphorbiaceae (19), Melastomataceae (16), Lauraceae (14) and Solanaceae (13) (See supplementary material). The local flora heights reached on average 8 m.

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Fig. 4 Distribution of growth habits (a) individuals sampled inside the different patch areas inside the plots (b) number of individuals of the adjoin flora with their respective growth habits on the different patch areas

Table 3 Average and standard deviation (mean ± SD) of local flora variables used to model number of pseudostems, length of pseudostems and patch area. Cover was based on cover measurements and individual density was based on individuals counting (see methods section)

Category Cover ± SD Species density ± SD Individuals density ± SD Habit growth index ± SD

Small 8.97 ± 12.98 6.86 ± 4.06 2.17 ± 0.75 4.04 ± 0.96

Medium 3.50 ± 3.26 5.43 ± 2.89 2.33 ± 1.44 4.76 ± 0.57

Large 1.99 ± 1.86 3.13 ± 2.41 1.30 ± 0.59 5.51 ± 1.23

Results of MGLM show that patch area was affected by species density. Besides, there was a marginally significant effect of habit growth index on patch area, and none other variable showed a significant effect on patch area (Table 4). None of the variables tested for their effects on pseudostems height and number was significant (Table 4). As the species density decreases, the area of the patches increases; smaller patches tend to had higher number of native species per square meter, while large patches had lower number of native species in the square meter (Table 4, Fig. 5). Additionally to these results, we find that species density, index of habit growth and individuals’ density were significant in the Spearman correlation carried out with patch area of H. coronarium (Table 5). Species density and individual’s density were associated negatively with patch area, while individual’s density increases the patch area decreases. While the index of habit growth increases as the patch area increases.

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Table 4 Results of general linear mixed effect model testing how three different parameters of Hedychium coronarium area, length and number of pseudostems, depended on parameters of the native community such as richness (Species density) and composition. Additionally, individual’s density and an index of growth habit were used. St: Estimate, t: t value and p: p value

Patch area Number of Length of pseudostems pseudostems Fixed effects St t p St t p St t p Species density -2.69 -3.51 0.003 0.67 0.28 0.78 -4.01 -1.59 0.13 Individual’s density 1.21 0.58 0.66 7.60 1.15 0.27 0.02 -0.03 0.99 Composition 0.03 0.05 0.85 -0.03 -0.02 0.98 0.75 0.44 0.66 Index of growth habit 3.48 2.15 0.05 3.76 0.73 0.47 7.04 1.32 0.20 Cover density 10.98 -1.54 0.14 -3.80 -0.88 0.39 8.92 2.00 0.67 AIC 138.22 184.41 185.74

Fig. 5 Effect of density of native species plant on the area of the invader Hedychium coronarium. Each dot represents an invasion site. The solid blue line is the tendency line

Table 5 Results of correlations and p-value(p) of the variables of local flora, species composition, species density, index of habit growth, individual’s density and cover with the variables of Hedychium coronarium patch area, length of pseudostems and number of pseudostems

Species p Species p Index of p Individuals p Cover p composition density habit density growth Patch area -0.13 0.54 -0.42 -0.04 0.65 0.001 -0.47 0.03 -0.23 0.30 Length of 0.24 0.27 0.16 0.47 0.20 0.36 -0.03 0.88 0.28 0.20 pseudostems Number of 0.21 0.34 0.17 0.42 -0.06 0.78 0.24 0.28 0.20 0.37 pseudostems 15

Discussion

In Colombia, H. coronarium has been particularly studied at the Otún Quimbaya Wildlife Sanctuary, where a plan for its control and eradication has been implemented (PNN 2007), that showed 69 invasion patches were recorded with a total area of 4.5 hectares invaded by H. coronarium (Aguilar-Garavito et al. 2012; Londoño et al. 2016) which contrast with the Alto de San Miguel, where we recorded 211 invasion patches occupying a much smaller area of 0.23 hectares. Besides, distribution of patches was different between Otún and San Miguel, because in San Miguel there is a higher number of patches than in Otún but occupying less area. The habitat conditions in Otún does not show a relationship between patch area and singular habitat characteristics (Gonzalez Gutierrez and Mejia Diaz 2015), since the observations by Aguilar-Garavito (2015) where H. coronarium is capable of developing under direct light or under canopy cover up to 70%. Habitat conditions in San Miguel were characterized by a distribution of small patches near the river and open areas, while medium and large patches were located in sites with greater tree cover and farther from the river. This reflects different types of invasion of H. coronarium in different landscapes and vegetation cover. Alto de San Miguel is a location with a high degree of anthropization, sand extraction from the river, multiple recreational activities and extensive livestock (Vargas et al. 2018), and these sites with a major degree of disturbance, appear to be the sites where H. coronarium tends to establish, but not the ones where reaches their maximum areas . People tend to cut H. coronarium to open roads and establish camping sites, simultaneously making small dams into the riverbed. These cutting activities could create fragments of the H. coronarium and dam creation could promote H. coronarium establishment blocking to travel through the river stream. Given that this is the main propagation mode of this species (Aguilar-Garavito 2017) which can create new focus of propagations.

We expected that large patches have a higher number of pseudostems and reach larger areas, as we anticipated big patches could be more successful. The successfulness of an invader species can be measured both in the form of larger sizes of individuals or the number of individuals (Kennedy et al. 2002). In our study site, large patches in fact reached the highest length of pseudostems but not the highest number of pseudostems and they grow flooded soils. This coincides with a removal experiment from Brazil showing that H. coronarium pseudostems were higher on average on wet soils than dry soils, but the number of new pseudostems was less (Chiba de Castro et al. 2016).

Alto de San Miguel is a biodiversity conservation and reserve area, but this does not seem to be an impediment to the establishment of H. coronarium. We wanted to understand the effect of the local flora and diversity on growth of H. coronarium. We evaluated the effect of species density, cover, individual density, and index of habit growth on H coronarium performance, finding that the only significant variable was species density. We found that the lower the species density, the larger the patch, this means that higher species density was found in small patches that were located in areas of high sun exposure. This could be interpreted as the small patches not reaching larger areas due to the presence of native flora. The effect of richness on invaders has been widely studied and has been found to have a negative effect on the invader, whether on biomass, area, coverage, roots and even its establishment (Kennedy et al. 2002; McGlone et al. 2011; Petruzzella et al. 2018, 2020). In terms of individual density although not significant in the model, but we found a significant correlation with the patch area, meaning that a higher proportion of individuals found in small patches, could be generating greater competition by occupying more space in this type of patch and reducing the susceptibility of invasion (Smith et al. 2004; Rudgers et al. 2005; Petruzzella et al. 2020).

If we consider the species composition, we observed that in small patches an extensive area of the patch was occupied by a high number of species belonging to Poaceae, Asteraceae, Piperaceae, Commelinaceae, Melastomataceae and Solanaceae. All these species have high light requirements and some of them can grow taller than H. coronarium, increasing the resistance of the riparian habitat to the invasion. Most of the species found inside the large and medium patches are conditioned to shady and semi-shady environments, mostly herbs (Urticaceae and Araceae) and trees (Lauraceae), these types of conditions are reminiscent of their 16

homeland in Asia, where H. coronarium grows in shady and semi-shady environments, waterlogged areas and soils rich in hummus (Joly and Brandle 1995), in San Miguel this type of condition could be favoring the growth of H. coronarium more than the high sun exposure and less humid areas Our results on the growth habit index also showed that high proportion of herbaceous species were found in small patches, which was expected since herbaceous plants found in small patches will be competing with H. coronarium based on the idea that species functionally similar to the invasive will have a negative effect (Symstad 2000; Hooper and Dukes 2010). Regarding to the flora growing around the patches, we recorded a greater number of species of shrubs and trees, which provide more shade in medium and large patches. On the other hand, one of the most representative species surrounding patches was Cavendishia pubescens (Ericaceae), which is a frequent species in the riparian vegetation of the Medellín River. This species can surround the patches, taking up space and extending long branches over H. coronarium.

In conclusion, we can say that the conditions present in Alto de San Miguel, unlike Otún, reflect a much smaller patch area than those found there but San Miguel exhibits a major number of patches. The species density had an effect on the area of the patches, with the highest species density in small patches. The habit index growth, individual density, composition, and cover were not significant in the MGML model, but despite these results the variables describe patterns associated with the establishment and areas reached by H. coronarium. Albeit our findings of species density on the area of H. coronarium patches, we cannot rule out environmental factors that can influence patch area. We recommend further studies that control variables such as environmental factors and controlled mesocosms experiments that would allow us to disentangle the role of species density over patch area (Naeem et al. 2000; Petruzzella et al. 2018). Based on the negative effect that adjoin flora has on area and survival of the invaders (Pacala and Silander Jr 1987; Kennedy et al. 2002), we propose the use of the species found here to be used in planting experiments and the evaluation of perturbation since it appears to be important in the growing of H. coronarium, all of these will allow to improve the understanding of the interaction between local flora and H. coronarium.

References

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Acknowledgements

Secretaria de Medio Ambiente de Medellín for financing this project, Junta Acción Comunal La Clara, Germán Arango, Alejandra Carvajal, Francisco Javier Roldán, Mario Quijano, Fernando Giraldo, Jonatan Castro, Wilson Rodríguez, Juliana Cardona, Estela Quintero, Dino Tuberquia.