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Non-native plant species in the Atlantico Department Coastal Dune Systems, Caribbean of Colombia: A new management challenge
Marine Pollution Bulletin 141 (2019) 603–610
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Baseline
Non-native plant species in the Atlantico Department Coastal Dune Systems, Caribbean of Colombia: A new management challenge
T
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Adriana Gracia C.a, Nelson Rangel-Buitragoa,b, , Julian Dario Castro-Barrosa a b
Programa de Biologia, Facultad de Ciencias Básicas, Universidad del Atlántico, Barranquilla, Atlántico, Colombia Programa de Física, Facultad de Ciencias Básicas, Universidad del Atlántico, Barranquilla, Atlántico, Colombia
A R T I C LE I N FO
A B S T R A C T
Keywords: Coastal dunes Biological pollution Conservation Invasive species Atlantico Department
Although coastal dunes exhibit typical vegetation which involves species adapted to extreme environmental conditions, the mobilization and colonization by non-native species represents a challenge in its conservation and management. In this work, eight dune systems located along the Atlantico Department, Caribbean coast of Colombia were surveyed, finding within them the presence of two plant species recognized as invasive: Calotropis procera and Cryptostegia madagascariensis. The impacts of these two invasive plant species can be significant at all ecological levels in the dune systems. The above demands the implementation of urgent management actions. Eradication seems the optimal control alternative, however preventing invasive plant species from infesting new areas is more cost-effective and efficient than trying to restore the system after it is infested. Data presented in this paper is the first step in the future development of an early detection program in the study area.
Coastal dunes are very particular areas of the planet earth. Dunes are defined as large piles of sand accumulated due the transport of fine sediments (0.06–4 mm in grain size) under a wind-dominate climate (Davis and Fitzgerald, 2004). Coastal dunes are the spatial transition between the continental environment and the sea. They are characterized by a highly specialized fauna and flora, converting them to strategic ecosystems for humankind due to their unique ecological functions (McLachlan and Brown, 2006; Rangel-Buitrago et al., 2018). Coastal dunes are located along wave-dominated environments around the world. Dunes are most commonly related to temperate and tropical climates where they can reach heights above the 150 m (Masselink and Hughes, 2003; Martinez et al., 2013). They are an incredibly dynamic environment that develops and evolves as the result of a complex interaction between sand, water, vegetation and external pressures (Short and Hesp, 1982). Their optimal position (between sea and land) makes coastal dunes a biodiversity hotspot. They are extremely important from an environmental and economic point of view due to their ability to provide multiple services, such as, raw materials, coastal protection, erosion control, water catchment and purification, maintenance of wildlife, carbon sequestration, education, and tourism - recreation (Carter et al., 1990; Pye and Tsoar, 1990; Neal et al., 2007; Rangel-Buitrago, 2019). Dune plant communities play an essential role in maintaining the integrity of dune systems. These plant assemblages are the result of the
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interaction between sand accretion, high wind velocities, salt spray, presence and tolerance of the plant species, and environmental heterogeneity (Maun, 2009). By capturing blowing sand, dune-plant communities can stabilize and shape what otherwise would be a highly unstable, shifting sand environment. Plants help in the creation and development of physical barriers of sand, bringing ecological and economic benefits for coastal communities (i.e., they have the potential to mitigate damage from massive storms and tsunamis, Feagin et al., 2010; Gracia et al., 2018a). The native vegetation located within the first kilometer of the coast is typically adapted to a dynamic environment, including among other factors: episodic conditions of salt water inundation or salt spray, mass sediment movement, and relatively rapid succession or spatial migration after disturbances (Feagin et al., 2010). This vegetation can provide a significant refuge and source of food for local and migratory faunal species. Furthermore, vegetation stands provide habitat and corridors for a wide range of invertebrates, birds, mammals, reptiles, amphibians and other wildlife (Doody, 2013). Currently, coastal dunes are threatened due to multiple vectors, one being the introduction, settlement, and colonization by non-native species (biological pollution). The introduction of non-native plants in dune systems by humans has occurred both by accident, and as also as deliberate policy. Due to of the lack of a natural control mechanism a high percentage of these plant species become invasive (Doody, 2013).
Corresponding author. E-mail address: [email protected] (N. Rangel-Buitrago).
https://doi.org/10.1016/j.marpolbul.2019.03.009 Received 12 February 2019; Received in revised form 25 February 2019; Accepted 5 March 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
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and the increased popularity for adventure sports, the study area, especially the dune systems, is becoming an essential place for tourism, and are experiencing significant infrastructure development to cope with visitors. Each of the eight dune systems located along the Atlantico Department coastline was categorized in one of the existing typologies into the Bathing Area Registration and Evaluation System (BARE) proposed by Williams and Micallef (2009). This categorization allows the classification of the coastal environment into five different classes (remote, village, rural, urban and resort) taking into account their accessibility degree, environment, facilities, accommodation grade, and safety equipment. In a second step, perpendicular and longitudinal walkthroughs were developed along each of the eight dune systems to determine its plant vegetation composition. Each plant species observed over the dune was recognized in the field, and later verified and confirmed using the works of Romero-Castañeda (1971), Klackenberg (2001), Vieira et al. (2004), Hassan et al. (2015), and the electronic resources of the ISSG (http://www.iucngisd.org/gisd/) and the CABI Invasive Species Compendium (https://www.cabi.org/ISC/). Repository material of each plant species collected was stored in the Geology, Geophysics, and Marine - Coastal Process group biological collection (located at Universidad del Atlántico campus, Colombia). Four of the investigated systems belonged to the village typology, while two sites corresponded to remote areas. Two sites corresponded to resort and rural, respectively. Village dunes are located outside central urban environments. These dunes have been influenced by a small and stable population characterized by a small-scale service structure. Remote dunes have access difficulty, and are only reached mainly by foot after a walk of 300 m or more. These sites have limited to absent housing. Rural dunes are located outside urban/village environments. They have an absence of a community focal center. Housing is limited, but may be significant depending on the size of the coastal stretch. Resort dunes are related to accommodation complexes, where a substantial proportion of users are resident. A series of facilities are usually prevalent because recreation is the primary aim of these kinds of areas. Along these four dune typologies were found two species that are classified as invasive: Calotropis procera and Cryptostegia madagascariensis. Table 1 summarizes the species occurrences and sites in which they were observed. The main characteristics of these two species found are as follows: Calotropis procera also known as the ‘apple of Sodom’ was found in all eight dune systems along the Atlantico Department coastline (Fig. 3). This plant was observed as a shrub or small tree, generally up to 2 to 4 m high. Some characteristics that define the species are: presents rounded stem, usually simple, green pale, thickly covered with hoary pubescence which readily rubs off. The leaves are decussate, ovate, acuminate 10–15 cm long and 4–8 cm wide. Inflorescence a dense, flowered, umbellate cyme arising from the nodes and appearing axillary or terminal (CABI, 2018). Its Corolla is slightly campanulate, with five sepals that are 4 mm long; segments ovate, acute, slightly concave, dull purple bordered with white on the upper side, silvery on the underside (CABI, 2018). Fruits sub-globose, ellipsoid or ovoid, recurved follicle, 7.5–10.0 cm. Seed light-brown, broadly ovate, flattened, 3.2 cm with silky hairs. C. procera observed at Atlantico dunes presented flowers and fruits during survey time (March 2018). Calotropis procera is native from tropical Africa and Asia (De Oliveira et al., 2009) and was first introduced to America in the Southern United States and Brazil (Crothers and Newbound, 1998; Cárdenas López et al., 2017). For the Caribbean, specifically along the West Indies, the species was reported as “common and naturalized” in Antigua and Jamaica (Grisebach, 1864). In 1879, it was reported as “naturalized in dry localities” on the US Virgin Islands (Eggers, 1879).
Non-native species can be a real hazard to biodiversity, human health and even have the ability to severely affect economic activities (Gracia et al., 2018b). Alien species presence due to biological invasion is considered to be the second most common cause of biodiversity losing terrestrial, marine and freshwater ecosystems, and ranks first in such invasions of island territories (Winston et al., 1997; Lonsdale, 1999; Molnar et al., 2008; Goldstein et al., 2014; NOOA, 2017). Impacts due to biological invasions include the occupation and transformation of the habitat, the alteration of ecological relations and evolutionary processes, the hybridization with native species, and extinctions, among others (Williamson, 1996; Rech et al., 2016). Once non-native species are set out in a new habitat, they may outcompete the native fauna and flora, causing severe imbalances in the ecosystem, and are almost impossible to control or eradicate (Thresher and Kuris, 2004; Gracia et al., 2018a). Dune ecosystems are not excluded from hazards related to biological invasions, and the negative related impacts include the alteration of soil pH, allelopathy, and the displacement of native vegetation (Vilà et al., 2006). According to Wootton and Rowe (2009), “biological pollution” by invasive species can create problems that increase, rather than dissipate, over time. Thus, the additional threat posed by exotic and invasive species over dune ecosystems is a matter of particular concern. In Colombia, 597 species of introduced or transplanted plants in various biomes and their related ecosystems have been recorded and identified (Cárdenas López et al., 2017). Of these species, 35 are considered as exotic with a high invasion potential (Cárdenas López et al., 2017). Despite the above information, how invasive species have negatively impacted Colombian coastal dune systems or native dune species is still unknown. In a tropical and mega diverse country like this, the presence of invasive species becomes much more significant. This paper presents the new management challenge related to the presence of non-native plant species with a high invasion potential into dune systems located along the Atlantico Department coastline in the Caribbean of Colombia. Results presented in this work allow a better understanding of the susceptibility of the dune ecosystem to invasive species. Also, these results are beneficial to local or national coastal managers and planners, who need baseline information for monitoring and controlling the arrival pathways of non-native and invasive species for dune systems located in the Southern Caribbean region. The study area covers the Atlantico Department coastline, a 72 km coastal segment with a population of 1,378,950 inhabitants (4% of the total national) located in the central area of the Caribbean coast of Colombia (Fig. 1). Specifically, this work was developed on eight dune systems separated by rocky headlands and composed of medium sands (Figs. 1, 2 and Table 1). The eight coastal dune systems lie in a semi-arid tropical environment with mean temperatures of < 28 °C and maximum precipitation values of 2500 mm/yr (Rangel-Buitrago et al., 2013). Seasonal variations show two rainy periods (April–May and October–November) and two dry periods (December–March and July–September). Wind climate is characterized by mean velocity values lower than 13 m/s. Higher velocity values are associated with winds blowing from the NE during the dry period. Lower values are observed between September and November related to winds blowing from E (Anfuso et al., 2015). The average wave height is 1.5 m and peak period average is 7.5 s. From November to July, the wave system along the area is dominated by NE swells; for the remainder of the time waves from NW, WSW, and even SW occur (Gracia et al., 2018b). Tides are mixed semi-diurnal, with maximum amplitudes of 65 cm (Rangel-Buitrago et al., 2017). Longshore sand drift has a dominant south-westward component, but a minor reversal to the northeast occurs during rainy periods when southerly winds prevail in some areas and set up short, high-frequency waves able to generate significant erosion along sandy beaches (Anfuso et al., 2015). Due to its dynamic and attractive landscape, natural environments, 604
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Fig. 1. Study area with the location of dune systems and sites where non-native plants were observed.
Department coastline (Fig. 4). According to CABI (2018) it is a twining woody vine or scandent shrub, 6 to 10 m in length, with abundant milky latex. It has cylindrical stems, glabrous, reddish brown, with few lenticels. Leaves are opposite; blades 4–10 × 2–5 cm, elliptic, with an apex short-acuminate. The margins are entire; venation pinnate, with 13–16 pairs of secondary veins; upper surface dull; lower surface pale, with obscure venation; petioles glabrous, 0.5–2 cm long; stipules minute, intrapetiolar. Flowers are arranged in pedunculate cymes; bracts foliaceous, lanceolate, approximately 5 mm long. Calyx green, campanulate, the sepals lanceolate, pubescent, 0.5–1.5 cm long; corolla 3–6 cm long, violet, the tube darker inside, the lobes abaxially whitish in the overlapping portion; corona with five simple lobes, approximately 1 cm long. Two follicles, divergent, brown when mature, 5.8–13 cm long, woody. Seeds are reddish-brown, ovate-lanceolate, 3 mm long, with long, cream-colored silky hairs (Acevedo-Rodríguez and Strong, 2005; CABI, 2018). C. madagascariensis observed in Atlantico dunes presented flowers during survey time (March 2018). Cryptostegia madagascariensis is native of Madagascar (Klackenberg, 2001). It was probably introduced into tropical and subtropical countries, first as ornamentals and later planted for rubber production (CABI, 2018). Currently, C. madagascariensis has become invasive in Hawaii, Brazil, the West Indies (Puerto Rico, Virgin Islands, St Lucia, Montserrat, Anguilla), and Australia (CABI, 2018). In the catalog of plants and lichens of Colombia, this species was listed as naturalized and adventitious (Bernal et al., 2015). This plant can build dense monospecific thickets that can outcompete native dune vegetation (ISSG, 2012). For example, on some parts of the Australia coast, this species is invading coastal/dune systems threatening the native and endemic biodiversity (Australian Weeds Committee, 2012). In Puerto Rico and the Virgin Islands C.
In 1881, this species was reported as naturalized in southern Puerto Rico (Bello Espinosa, 1881). In 1898, C. procera was described as a “culta et quasi spontanea” along Cuba, Haiti, Guadeloupe and Martinique islands (Urban, 1898). In Colombia, it was reported as naturalized by Cárdenas López et al. (2017). The high invasive potential of C. procera is due to fast growth and dissemination, high seed production efficiently dispersal by the wind, a non-specialized pollination system, and high tolerance to poor soils. Some morphological and physiological adaptations can be found in C. procera due its original occurrence in desert regions where water deficits, high thermal amplitude, and nutritionally poor and sandy soils are common natural traits (Obeid and Mahmoud, 1971; Abbassi et al., 2003). These traits lead to an improved establishment capacity in arid, degraded and deficient soils, like road edges, pastures and abandoned areas (De Oliveira et al., 2009). Calotropis procera is a serious weed in pastures, and poorly managed hay fields. In dunes it successfully competes with native species and is capable of producing dense thickets that interfere with stock management, particularly mustering activities. It is reported to contain a bitter principle called calotropin which is a cardiac poison (El-Badwi and Adam, 1998). Once established, C. procera is difficult to eradicate as the deep roots survive almost any treatment. It is susceptible to regular cultivation and some herbicides. The maintenance of a dense pasture sward will assist in the invasion (Crothers and Newbound, 1998). Brandao (1995) in Brazil reported that chemical control of the weed is unknown, and that manual control presents problems because of the high costs incurred, and because the weed can re-establish itself with vigor after cutting. Cryptostegia madagascariensis also known ‘Madagascar rubbervine’ was found in one of the eight dune systems along the Atlantico 605
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Fig. 2. Dune systems surveyed. A7 Puerto Velero – Expuesto, A16 Palmarito, A18 Santa Veronica – Cajacopi, A20-A Salinas del Rey – Norte, A20-B Salinas del Rey – Sur, A21 Loma de Piedra, A22 Aguamarina, A24 Punta Astilleros.
Table 1 Location and main characteristics of the eight dune systems investigated. General information
Nonnative plant
ID
Name
A7 A16 A18 A20-a A20-b A21 A22 A24
Puerto Velero - Expuesto Palmarito Santa Veronica - Cajacopi Salinas del Rey - Norte Salinas del Rey - Sur Loma de Piedra Aguamarina Punta Astilleros
Typology
Calotropis procera
Remote Village Village Village Village Remote Resort Rural
* * * * * * * *
* indicates that species was observed on the dune. 606
Cryptostegia madagascariensis
*
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Fig. 3. Examples of Calotropis procera along the study area. A) General view, B) flowers detail, C) fruit detail.
when farmland, stubbles, and scrubs surround dune systems because these generally contain alien weeds (Jauni and Hyvonen, 2010). Calotropis procera is dispersing naturally along all dune typologies because it is a common plant found inside available lots, gardens and other green areas located near the dunes, especially in rural and village areas. In this natural dispersion process, wind is the pivotal dispersal vector and it is strongly related to plant functional traits. Calotropis procera seeds are partially or fully covered with hairs, which help in the wind dispersal due to their low terminal velocity which is the highest velocity attainable by an object as it moves through a fluid. Not much wind energy is required because these seeds can be moved several hundred meters and even kilometers under gentle breeze conditions (Francis, 2002). Along the study area, wind circulation patterns are controlled by the Intertropical Convergence Zone (ITCZ) migration. Between January–July the ITCZ is southerly located, resulting in the generation of high and constant northeast trade winds. After August, the ITCZ position is over the Northern Hemisphere; approximately over the Caribbean Sea of Colombia. During this part of the year, low magnitude
madagascariensis coastal dry forests spread by climbing over trees at the periphery of the forest and slowly spreading further into the interior forest. This non-native plant is characterized by being poisonous (Klackenberg, 2001), and its impact over Colombian coastal habitats still is unknown. Small plants can be controlled by hand pulling or digging out the plant. Fruits should be bagged and disposed of properly. Contact with milky latex should be avoided (Starr et al., 2003). Clearly, dune systems of the Atlantico Department coastline are facing an invasion process by the two non-native plant species C. procera and C. madagascariensis. The above leaves an important question to solve; the answer to which is crucial to managing the current existing risk: How do these plants arrive into these dune systems? The answer to this question is closely linked with the character of the invasion event, which seems to differ between species. The autochthonous dune plant vegetation often is threatened from the colonization and further establishment by undesired alien species that come from nearby areas due to natural dispersion processes (Wilkerson, 2013; Egawa, 2017). The above is particularly possible
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Fig. 4. Examples of Cryptostegia madagascariensis along the study area. A) General view, B) and C) flowers detail.
successful germination rates between 90 and 95% (Starr et al., 2003; Vieira et al., 2004; Australian Weeds Committee, 2012). The impacts of invasive plant species on dunes can be significant along all ecological levels (Wootton and Rowe, 2009). These impacts can include morphological variations related to changes in the dune shape and biological alterations such as the reduction of community diversity and native species' population size. The results are changes in native plant morphology and vigor, and cascading effects on upper trophic levels. The invasion of nonnative plant species into the Atlantico Department dunes demands the implementation of urgent management actions. Eradication seems the optimal control alternative. However, eradication is often impractical if not effectively impossible, except when the alien species occurs in low numbers in a single circumscribed beachhead (this is not the case of the study area). According to Mooney (2005), the control of nonnative plants through eradication measures addresses the reality of our inability to devise fail-proof quarantine at natural geographic boundaries such as the case of dune systems. Recent efforts have recognized that preventing invasive plant species from infesting new areas is more cost-effective and efficient than trying to restore the system after it is infested (Mack et al., 2000; Davies and Sheley, 2007). Here the action chain is clear: early detection, monitoring and ultimately the implementation of an optimal management strategy. According to Brooks and Klinger (2009), the early detection and rapid response is the first line of defense against plant colonization over
winds move over the equatorial zone from the Southern Hemisphere with variable directions. Specifically, along the study area winds present mean velocity values of 5–6 m/s and mainly come from the NE (45%) and the NNE (35%). Higher velocity values ranging from 7 to 10 m/s are associated with winds blowing from the NE during the dry period (December and April). For the rest of the year, winds blow from the E and with a typically low velocity having values that fall below average (Anfuso et al., 2015; Rangel-Buitrago et al., 2018). The ornamental horticulture industry is also responsible for the introduction, propagation, and transport of thousands of nonnative plant species (Hayden and White, 2001). Most of the time, and under strict control measures, plants can stay in their intended locations or even spread without significant environmental impacts (Starr et al., 2003; Inderjit, 2009). However, some non-indigenous plant species have proved to be particularly invasive and quite deleterious environmentally (Niemiera and Holle, 2009). The above is the case of C. madagascariensis which was probably deliberately introduced along the study area as an ornament plant on resort sites (i.e., Aguamarina). Currently, this plant is forming dense, impenetrable thickets, is climbing up and covering nearby trees, and is displacing the existing native dune vegetation. The fast-growing invasive woody vine C. madagascariensis has the ability begin to reproduce after about 200 days, and can produce large numbers of seeds which have the capacity of being rapidly dispersed by wind, floodwaters, or even stuck to the fur of animals. In the same way, these seeds can remain viable up to one year, and several studies have reported 608
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any ecosystem. In that sense, early detection is the key in any invasive plant management program to be developed over dune systems because once an invading species have been established, population eradication processes become unfeasible. This early detection must be coupled with a rapid response which will allow the control of the incipient populations of invaders over the ecosystem. An efficient allocation of resources to detect plant invasions from outside the final area of colonization and establishment leaves more resources available for control efforts and other management priorities. Information presented in this paper is the first step in the future development of an early detection program that must involve compiling existing information on species and site characteristics to develop an efficient monitoring approach. Also, this information can be used to prioritize target species and specific sites that require urgent management.
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Acknowledgements This work is a contribution to research group: “Geology, Geophysics and Marine - Coastal Process,” Universidad del Atlántico (Barranquilla, Colombia). Adriana Gracia C. thanks to Colciencias-Colfuturo National Scholarship Grant N° 528. Thanks to reviewers for its comments in the manuscript improvement. Dedicated to the Colombian Ichthyologist Javier Maldonado (1977-2019). References Abbassi, K., Atay-Kadiri, Z., Ghaout, S., 2003. Biological effects of alkaloids extracted from three plants of Moroccan arid areas on the desert locust. Physiol. Entomol. 28, 232–236. Acevedo-Rodríguez, P., Strong, M.T., 2005. Catalogue of the Seed Plants of the West Indies. Smithsonian Contributions to Botany, Smithsonian Institution, Washington, USA. Anfuso, G., Rangel-Buitrago, N., Correa, I., 2015. Evolution of sandspits along the Caribbean Coast of Colombia: natural and human influences. In: Randazzo, G., Jackson, D., Cooper, J.A. (Eds.), Sand and Gravel Spits. Springer, New York, pp. 1–21. Australian Weeds Committtee, 2012. Weeds of Australia. Australian Weeds Committtee, Canberra, Australia. Bello Espinosa, D., 1881. Apuntes para la flora de Puerto Rico. Primera parte. Anales Sociedad Española de Historia Natural. 10, 231–304. Bernal, R., Gradstein, S.R., Celis, M., 2015. Catálogo de plantas y líquenes de Colombia. In: Instituto de Ciencias Naturales, Universidad Nacional de Colombia. Colombia, Bogotá. Brandao, M., 1995. Calotropis procera: a problem pasture invader in Minas Gerais. DAPHNE - Revista do Herbário – EPAMIG. 5 (1), 68–71. Brooks, M.L., Klinger, R.C., 2009. Practical considerations for early detection monitoring of plant invasions. In: Inderjit (Ed.), Management of Invasive Weeds. Springer, Dordrecht, pp. 9–33. CABI 2018. Invasive Species Compendium. https://www.cabi.org/isc/datasheet/16848 Cárdenas López, D., Baptiste, M.P., Castaño, N., 2017. Plantas exóticas con alto potencial de invasión en Colombia. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt. Bogota, Colombia. Carter, R.W.G., Hesp, P., Nordstrom, K., 1990. Erosional landforms in coastal dunes. In: Nordstrom, K., Psuty, N.P., Carter, R.W.G. (Eds.), Coastal Dunes: Forms and Process. John Wiley & Sons, New York, pp. 217–249. Crothers, M., Newbound, S., 1998. Rubber Bush (Calotropis procera). Agnote -Agdex, Northern Territory of Australia, Australia. Davies, K., Sheley, R., 2007. A conceptual framework for preventing the spatial dispersal of invasive plants. Weed Sci. 55, 178–184. Davis, R., Fitzgerald, D.M., 2004. Beaches and Coasts. Wiley-Blackwell, New York, USA. De Oliveira, S.H., Negreiros, D., Fernandes, G.W., Barbosa, N.P., Almeida-Cortez, J., 2009. Seedling growth of the invader Calotropis procera in ironstone rupestrian field and seasonally dry forest soils. Neotropical Biology and Conservation. 4 (2), 69–76. Doody, J.P., 2013. Sand Dune Conservation, Management and Restoration. Springer, Amsterdam, Netherlands. Egawa, C., 2017. Wind dispersal of alien plant species into remnant natural vegetation from adjacent agricultural fields. Global Ecology and Conservation. 11, 33–41. Eggers, H.F.A., 1879. The Flora of St. Croix and the Virgin Islands. Washington Government Printing Office, Washington, USA. El-Badwi, S.M.A., Adam, S.E.I., 1998. Studies on laticiferous plants: toxic effects in goats on Calotropis procera latex given by different routes of administration. DTW Deutsche Tieraerztliche Wochenschrift. 105 (11), 425–427. Feagin, R.A., Mukherjee, N., Shanker, K., Baird, A.H., Cinner, J., Kerr, A.M., Koedam, N., Sridhar, A., Arthur, R., Jayatissa, L.P., Seen, D.L., Menon, M., Rodriguez, S., Shamsuddoha, Md, Dahdouh-Guebas, F., 2010. Shelter from the storm? Use and misuse of coastal vegetation bioshields for managing natural disasters. Conservation Letters. 3, 1–11.
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Georgian Court University, New Jersey Sea Grant Consortium and Cape May Plant Material Center. USA, New Jersey.
Wilkerson, M.L., 2013. Invasive plants in conservation linkages: a conceptual model that addresses an underappreciated conservation issue. Ecography 36, 1319–1330. Williams, A.T., Micallef, A., 2009. Beach Management Principles and Practice. Earthscan, London. Williamson, M.H., 1996. Biological Invasions. Chapman & Hall, London, UK. Winston, J.E., Gregory, M.R., Stevens, L.M., 1997. Encrusters, epibionts, and other biota associated with pelagic plastics: a review of biogeographical, environmental, and conservation issues. In: Alexander, D.E. (Ed.), Marine Debris: Sources, Impacts, and Solutions. Springer, Dordrecht, pp. 81–97. Wootton, L., Rowe, P., 2009. Invasive species in coastal dunes and maritime forest. In:
Web pages http://www.iucngisd.org/gisd/. https://www.cabi.org/ISC/.
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Baseline
Non-native plant species in the Atlantico Department Coastal Dune Systems, Caribbean of Colombia: A new management challenge
T
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Adriana Gracia C.a, Nelson Rangel-Buitragoa,b, , Julian Dario Castro-Barrosa a b
Programa de Biologia, Facultad de Ciencias Básicas, Universidad del Atlántico, Barranquilla, Atlántico, Colombia Programa de Física, Facultad de Ciencias Básicas, Universidad del Atlántico, Barranquilla, Atlántico, Colombia
A R T I C LE I N FO
A B S T R A C T
Keywords: Coastal dunes Biological pollution Conservation Invasive species Atlantico Department
Although coastal dunes exhibit typical vegetation which involves species adapted to extreme environmental conditions, the mobilization and colonization by non-native species represents a challenge in its conservation and management. In this work, eight dune systems located along the Atlantico Department, Caribbean coast of Colombia were surveyed, finding within them the presence of two plant species recognized as invasive: Calotropis procera and Cryptostegia madagascariensis. The impacts of these two invasive plant species can be significant at all ecological levels in the dune systems. The above demands the implementation of urgent management actions. Eradication seems the optimal control alternative, however preventing invasive plant species from infesting new areas is more cost-effective and efficient than trying to restore the system after it is infested. Data presented in this paper is the first step in the future development of an early detection program in the study area.
Coastal dunes are very particular areas of the planet earth. Dunes are defined as large piles of sand accumulated due the transport of fine sediments (0.06–4 mm in grain size) under a wind-dominate climate (Davis and Fitzgerald, 2004). Coastal dunes are the spatial transition between the continental environment and the sea. They are characterized by a highly specialized fauna and flora, converting them to strategic ecosystems for humankind due to their unique ecological functions (McLachlan and Brown, 2006; Rangel-Buitrago et al., 2018). Coastal dunes are located along wave-dominated environments around the world. Dunes are most commonly related to temperate and tropical climates where they can reach heights above the 150 m (Masselink and Hughes, 2003; Martinez et al., 2013). They are an incredibly dynamic environment that develops and evolves as the result of a complex interaction between sand, water, vegetation and external pressures (Short and Hesp, 1982). Their optimal position (between sea and land) makes coastal dunes a biodiversity hotspot. They are extremely important from an environmental and economic point of view due to their ability to provide multiple services, such as, raw materials, coastal protection, erosion control, water catchment and purification, maintenance of wildlife, carbon sequestration, education, and tourism - recreation (Carter et al., 1990; Pye and Tsoar, 1990; Neal et al., 2007; Rangel-Buitrago, 2019). Dune plant communities play an essential role in maintaining the integrity of dune systems. These plant assemblages are the result of the
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interaction between sand accretion, high wind velocities, salt spray, presence and tolerance of the plant species, and environmental heterogeneity (Maun, 2009). By capturing blowing sand, dune-plant communities can stabilize and shape what otherwise would be a highly unstable, shifting sand environment. Plants help in the creation and development of physical barriers of sand, bringing ecological and economic benefits for coastal communities (i.e., they have the potential to mitigate damage from massive storms and tsunamis, Feagin et al., 2010; Gracia et al., 2018a). The native vegetation located within the first kilometer of the coast is typically adapted to a dynamic environment, including among other factors: episodic conditions of salt water inundation or salt spray, mass sediment movement, and relatively rapid succession or spatial migration after disturbances (Feagin et al., 2010). This vegetation can provide a significant refuge and source of food for local and migratory faunal species. Furthermore, vegetation stands provide habitat and corridors for a wide range of invertebrates, birds, mammals, reptiles, amphibians and other wildlife (Doody, 2013). Currently, coastal dunes are threatened due to multiple vectors, one being the introduction, settlement, and colonization by non-native species (biological pollution). The introduction of non-native plants in dune systems by humans has occurred both by accident, and as also as deliberate policy. Due to of the lack of a natural control mechanism a high percentage of these plant species become invasive (Doody, 2013).
Corresponding author. E-mail address: [email protected] (N. Rangel-Buitrago).
https://doi.org/10.1016/j.marpolbul.2019.03.009 Received 12 February 2019; Received in revised form 25 February 2019; Accepted 5 March 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
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and the increased popularity for adventure sports, the study area, especially the dune systems, is becoming an essential place for tourism, and are experiencing significant infrastructure development to cope with visitors. Each of the eight dune systems located along the Atlantico Department coastline was categorized in one of the existing typologies into the Bathing Area Registration and Evaluation System (BARE) proposed by Williams and Micallef (2009). This categorization allows the classification of the coastal environment into five different classes (remote, village, rural, urban and resort) taking into account their accessibility degree, environment, facilities, accommodation grade, and safety equipment. In a second step, perpendicular and longitudinal walkthroughs were developed along each of the eight dune systems to determine its plant vegetation composition. Each plant species observed over the dune was recognized in the field, and later verified and confirmed using the works of Romero-Castañeda (1971), Klackenberg (2001), Vieira et al. (2004), Hassan et al. (2015), and the electronic resources of the ISSG (http://www.iucngisd.org/gisd/) and the CABI Invasive Species Compendium (https://www.cabi.org/ISC/). Repository material of each plant species collected was stored in the Geology, Geophysics, and Marine - Coastal Process group biological collection (located at Universidad del Atlántico campus, Colombia). Four of the investigated systems belonged to the village typology, while two sites corresponded to remote areas. Two sites corresponded to resort and rural, respectively. Village dunes are located outside central urban environments. These dunes have been influenced by a small and stable population characterized by a small-scale service structure. Remote dunes have access difficulty, and are only reached mainly by foot after a walk of 300 m or more. These sites have limited to absent housing. Rural dunes are located outside urban/village environments. They have an absence of a community focal center. Housing is limited, but may be significant depending on the size of the coastal stretch. Resort dunes are related to accommodation complexes, where a substantial proportion of users are resident. A series of facilities are usually prevalent because recreation is the primary aim of these kinds of areas. Along these four dune typologies were found two species that are classified as invasive: Calotropis procera and Cryptostegia madagascariensis. Table 1 summarizes the species occurrences and sites in which they were observed. The main characteristics of these two species found are as follows: Calotropis procera also known as the ‘apple of Sodom’ was found in all eight dune systems along the Atlantico Department coastline (Fig. 3). This plant was observed as a shrub or small tree, generally up to 2 to 4 m high. Some characteristics that define the species are: presents rounded stem, usually simple, green pale, thickly covered with hoary pubescence which readily rubs off. The leaves are decussate, ovate, acuminate 10–15 cm long and 4–8 cm wide. Inflorescence a dense, flowered, umbellate cyme arising from the nodes and appearing axillary or terminal (CABI, 2018). Its Corolla is slightly campanulate, with five sepals that are 4 mm long; segments ovate, acute, slightly concave, dull purple bordered with white on the upper side, silvery on the underside (CABI, 2018). Fruits sub-globose, ellipsoid or ovoid, recurved follicle, 7.5–10.0 cm. Seed light-brown, broadly ovate, flattened, 3.2 cm with silky hairs. C. procera observed at Atlantico dunes presented flowers and fruits during survey time (March 2018). Calotropis procera is native from tropical Africa and Asia (De Oliveira et al., 2009) and was first introduced to America in the Southern United States and Brazil (Crothers and Newbound, 1998; Cárdenas López et al., 2017). For the Caribbean, specifically along the West Indies, the species was reported as “common and naturalized” in Antigua and Jamaica (Grisebach, 1864). In 1879, it was reported as “naturalized in dry localities” on the US Virgin Islands (Eggers, 1879).
Non-native species can be a real hazard to biodiversity, human health and even have the ability to severely affect economic activities (Gracia et al., 2018b). Alien species presence due to biological invasion is considered to be the second most common cause of biodiversity losing terrestrial, marine and freshwater ecosystems, and ranks first in such invasions of island territories (Winston et al., 1997; Lonsdale, 1999; Molnar et al., 2008; Goldstein et al., 2014; NOOA, 2017). Impacts due to biological invasions include the occupation and transformation of the habitat, the alteration of ecological relations and evolutionary processes, the hybridization with native species, and extinctions, among others (Williamson, 1996; Rech et al., 2016). Once non-native species are set out in a new habitat, they may outcompete the native fauna and flora, causing severe imbalances in the ecosystem, and are almost impossible to control or eradicate (Thresher and Kuris, 2004; Gracia et al., 2018a). Dune ecosystems are not excluded from hazards related to biological invasions, and the negative related impacts include the alteration of soil pH, allelopathy, and the displacement of native vegetation (Vilà et al., 2006). According to Wootton and Rowe (2009), “biological pollution” by invasive species can create problems that increase, rather than dissipate, over time. Thus, the additional threat posed by exotic and invasive species over dune ecosystems is a matter of particular concern. In Colombia, 597 species of introduced or transplanted plants in various biomes and their related ecosystems have been recorded and identified (Cárdenas López et al., 2017). Of these species, 35 are considered as exotic with a high invasion potential (Cárdenas López et al., 2017). Despite the above information, how invasive species have negatively impacted Colombian coastal dune systems or native dune species is still unknown. In a tropical and mega diverse country like this, the presence of invasive species becomes much more significant. This paper presents the new management challenge related to the presence of non-native plant species with a high invasion potential into dune systems located along the Atlantico Department coastline in the Caribbean of Colombia. Results presented in this work allow a better understanding of the susceptibility of the dune ecosystem to invasive species. Also, these results are beneficial to local or national coastal managers and planners, who need baseline information for monitoring and controlling the arrival pathways of non-native and invasive species for dune systems located in the Southern Caribbean region. The study area covers the Atlantico Department coastline, a 72 km coastal segment with a population of 1,378,950 inhabitants (4% of the total national) located in the central area of the Caribbean coast of Colombia (Fig. 1). Specifically, this work was developed on eight dune systems separated by rocky headlands and composed of medium sands (Figs. 1, 2 and Table 1). The eight coastal dune systems lie in a semi-arid tropical environment with mean temperatures of < 28 °C and maximum precipitation values of 2500 mm/yr (Rangel-Buitrago et al., 2013). Seasonal variations show two rainy periods (April–May and October–November) and two dry periods (December–March and July–September). Wind climate is characterized by mean velocity values lower than 13 m/s. Higher velocity values are associated with winds blowing from the NE during the dry period. Lower values are observed between September and November related to winds blowing from E (Anfuso et al., 2015). The average wave height is 1.5 m and peak period average is 7.5 s. From November to July, the wave system along the area is dominated by NE swells; for the remainder of the time waves from NW, WSW, and even SW occur (Gracia et al., 2018b). Tides are mixed semi-diurnal, with maximum amplitudes of 65 cm (Rangel-Buitrago et al., 2017). Longshore sand drift has a dominant south-westward component, but a minor reversal to the northeast occurs during rainy periods when southerly winds prevail in some areas and set up short, high-frequency waves able to generate significant erosion along sandy beaches (Anfuso et al., 2015). Due to its dynamic and attractive landscape, natural environments, 604
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Fig. 1. Study area with the location of dune systems and sites where non-native plants were observed.
Department coastline (Fig. 4). According to CABI (2018) it is a twining woody vine or scandent shrub, 6 to 10 m in length, with abundant milky latex. It has cylindrical stems, glabrous, reddish brown, with few lenticels. Leaves are opposite; blades 4–10 × 2–5 cm, elliptic, with an apex short-acuminate. The margins are entire; venation pinnate, with 13–16 pairs of secondary veins; upper surface dull; lower surface pale, with obscure venation; petioles glabrous, 0.5–2 cm long; stipules minute, intrapetiolar. Flowers are arranged in pedunculate cymes; bracts foliaceous, lanceolate, approximately 5 mm long. Calyx green, campanulate, the sepals lanceolate, pubescent, 0.5–1.5 cm long; corolla 3–6 cm long, violet, the tube darker inside, the lobes abaxially whitish in the overlapping portion; corona with five simple lobes, approximately 1 cm long. Two follicles, divergent, brown when mature, 5.8–13 cm long, woody. Seeds are reddish-brown, ovate-lanceolate, 3 mm long, with long, cream-colored silky hairs (Acevedo-Rodríguez and Strong, 2005; CABI, 2018). C. madagascariensis observed in Atlantico dunes presented flowers during survey time (March 2018). Cryptostegia madagascariensis is native of Madagascar (Klackenberg, 2001). It was probably introduced into tropical and subtropical countries, first as ornamentals and later planted for rubber production (CABI, 2018). Currently, C. madagascariensis has become invasive in Hawaii, Brazil, the West Indies (Puerto Rico, Virgin Islands, St Lucia, Montserrat, Anguilla), and Australia (CABI, 2018). In the catalog of plants and lichens of Colombia, this species was listed as naturalized and adventitious (Bernal et al., 2015). This plant can build dense monospecific thickets that can outcompete native dune vegetation (ISSG, 2012). For example, on some parts of the Australia coast, this species is invading coastal/dune systems threatening the native and endemic biodiversity (Australian Weeds Committee, 2012). In Puerto Rico and the Virgin Islands C.
In 1881, this species was reported as naturalized in southern Puerto Rico (Bello Espinosa, 1881). In 1898, C. procera was described as a “culta et quasi spontanea” along Cuba, Haiti, Guadeloupe and Martinique islands (Urban, 1898). In Colombia, it was reported as naturalized by Cárdenas López et al. (2017). The high invasive potential of C. procera is due to fast growth and dissemination, high seed production efficiently dispersal by the wind, a non-specialized pollination system, and high tolerance to poor soils. Some morphological and physiological adaptations can be found in C. procera due its original occurrence in desert regions where water deficits, high thermal amplitude, and nutritionally poor and sandy soils are common natural traits (Obeid and Mahmoud, 1971; Abbassi et al., 2003). These traits lead to an improved establishment capacity in arid, degraded and deficient soils, like road edges, pastures and abandoned areas (De Oliveira et al., 2009). Calotropis procera is a serious weed in pastures, and poorly managed hay fields. In dunes it successfully competes with native species and is capable of producing dense thickets that interfere with stock management, particularly mustering activities. It is reported to contain a bitter principle called calotropin which is a cardiac poison (El-Badwi and Adam, 1998). Once established, C. procera is difficult to eradicate as the deep roots survive almost any treatment. It is susceptible to regular cultivation and some herbicides. The maintenance of a dense pasture sward will assist in the invasion (Crothers and Newbound, 1998). Brandao (1995) in Brazil reported that chemical control of the weed is unknown, and that manual control presents problems because of the high costs incurred, and because the weed can re-establish itself with vigor after cutting. Cryptostegia madagascariensis also known ‘Madagascar rubbervine’ was found in one of the eight dune systems along the Atlantico 605
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Fig. 2. Dune systems surveyed. A7 Puerto Velero – Expuesto, A16 Palmarito, A18 Santa Veronica – Cajacopi, A20-A Salinas del Rey – Norte, A20-B Salinas del Rey – Sur, A21 Loma de Piedra, A22 Aguamarina, A24 Punta Astilleros.
Table 1 Location and main characteristics of the eight dune systems investigated. General information
Nonnative plant
ID
Name
A7 A16 A18 A20-a A20-b A21 A22 A24
Puerto Velero - Expuesto Palmarito Santa Veronica - Cajacopi Salinas del Rey - Norte Salinas del Rey - Sur Loma de Piedra Aguamarina Punta Astilleros
Typology
Calotropis procera
Remote Village Village Village Village Remote Resort Rural
* * * * * * * *
* indicates that species was observed on the dune. 606
Cryptostegia madagascariensis
*
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Fig. 3. Examples of Calotropis procera along the study area. A) General view, B) flowers detail, C) fruit detail.
when farmland, stubbles, and scrubs surround dune systems because these generally contain alien weeds (Jauni and Hyvonen, 2010). Calotropis procera is dispersing naturally along all dune typologies because it is a common plant found inside available lots, gardens and other green areas located near the dunes, especially in rural and village areas. In this natural dispersion process, wind is the pivotal dispersal vector and it is strongly related to plant functional traits. Calotropis procera seeds are partially or fully covered with hairs, which help in the wind dispersal due to their low terminal velocity which is the highest velocity attainable by an object as it moves through a fluid. Not much wind energy is required because these seeds can be moved several hundred meters and even kilometers under gentle breeze conditions (Francis, 2002). Along the study area, wind circulation patterns are controlled by the Intertropical Convergence Zone (ITCZ) migration. Between January–July the ITCZ is southerly located, resulting in the generation of high and constant northeast trade winds. After August, the ITCZ position is over the Northern Hemisphere; approximately over the Caribbean Sea of Colombia. During this part of the year, low magnitude
madagascariensis coastal dry forests spread by climbing over trees at the periphery of the forest and slowly spreading further into the interior forest. This non-native plant is characterized by being poisonous (Klackenberg, 2001), and its impact over Colombian coastal habitats still is unknown. Small plants can be controlled by hand pulling or digging out the plant. Fruits should be bagged and disposed of properly. Contact with milky latex should be avoided (Starr et al., 2003). Clearly, dune systems of the Atlantico Department coastline are facing an invasion process by the two non-native plant species C. procera and C. madagascariensis. The above leaves an important question to solve; the answer to which is crucial to managing the current existing risk: How do these plants arrive into these dune systems? The answer to this question is closely linked with the character of the invasion event, which seems to differ between species. The autochthonous dune plant vegetation often is threatened from the colonization and further establishment by undesired alien species that come from nearby areas due to natural dispersion processes (Wilkerson, 2013; Egawa, 2017). The above is particularly possible
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Fig. 4. Examples of Cryptostegia madagascariensis along the study area. A) General view, B) and C) flowers detail.
successful germination rates between 90 and 95% (Starr et al., 2003; Vieira et al., 2004; Australian Weeds Committee, 2012). The impacts of invasive plant species on dunes can be significant along all ecological levels (Wootton and Rowe, 2009). These impacts can include morphological variations related to changes in the dune shape and biological alterations such as the reduction of community diversity and native species' population size. The results are changes in native plant morphology and vigor, and cascading effects on upper trophic levels. The invasion of nonnative plant species into the Atlantico Department dunes demands the implementation of urgent management actions. Eradication seems the optimal control alternative. However, eradication is often impractical if not effectively impossible, except when the alien species occurs in low numbers in a single circumscribed beachhead (this is not the case of the study area). According to Mooney (2005), the control of nonnative plants through eradication measures addresses the reality of our inability to devise fail-proof quarantine at natural geographic boundaries such as the case of dune systems. Recent efforts have recognized that preventing invasive plant species from infesting new areas is more cost-effective and efficient than trying to restore the system after it is infested (Mack et al., 2000; Davies and Sheley, 2007). Here the action chain is clear: early detection, monitoring and ultimately the implementation of an optimal management strategy. According to Brooks and Klinger (2009), the early detection and rapid response is the first line of defense against plant colonization over
winds move over the equatorial zone from the Southern Hemisphere with variable directions. Specifically, along the study area winds present mean velocity values of 5–6 m/s and mainly come from the NE (45%) and the NNE (35%). Higher velocity values ranging from 7 to 10 m/s are associated with winds blowing from the NE during the dry period (December and April). For the rest of the year, winds blow from the E and with a typically low velocity having values that fall below average (Anfuso et al., 2015; Rangel-Buitrago et al., 2018). The ornamental horticulture industry is also responsible for the introduction, propagation, and transport of thousands of nonnative plant species (Hayden and White, 2001). Most of the time, and under strict control measures, plants can stay in their intended locations or even spread without significant environmental impacts (Starr et al., 2003; Inderjit, 2009). However, some non-indigenous plant species have proved to be particularly invasive and quite deleterious environmentally (Niemiera and Holle, 2009). The above is the case of C. madagascariensis which was probably deliberately introduced along the study area as an ornament plant on resort sites (i.e., Aguamarina). Currently, this plant is forming dense, impenetrable thickets, is climbing up and covering nearby trees, and is displacing the existing native dune vegetation. The fast-growing invasive woody vine C. madagascariensis has the ability begin to reproduce after about 200 days, and can produce large numbers of seeds which have the capacity of being rapidly dispersed by wind, floodwaters, or even stuck to the fur of animals. In the same way, these seeds can remain viable up to one year, and several studies have reported 608
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any ecosystem. In that sense, early detection is the key in any invasive plant management program to be developed over dune systems because once an invading species have been established, population eradication processes become unfeasible. This early detection must be coupled with a rapid response which will allow the control of the incipient populations of invaders over the ecosystem. An efficient allocation of resources to detect plant invasions from outside the final area of colonization and establishment leaves more resources available for control efforts and other management priorities. Information presented in this paper is the first step in the future development of an early detection program that must involve compiling existing information on species and site characteristics to develop an efficient monitoring approach. Also, this information can be used to prioritize target species and specific sites that require urgent management.
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