International Journal of Biology 2020; volume 11:8637

The paradox of the alien plant (but even up to 3,000 mm) and a dry season leucocephala subsp. of 3-6 months.1 As most , Leucaena Giovanna Sala, Department of Agricultural, hosts nitrogen-fixing rhizobia and it is con- Food and Forest Sciences University of glabrata (Rose) S. Zárate in sidered as a promiscuous host, being nodu- Palermo, Viale delle Scienze 13 Ed.4, Ingr. H, Sicily: another threat for the lated by both fast- and slow-growing rhizo- 90128 Palermo, Italia. native flora or a valuable bia belonging to the genera Ensifer, E-mail: [email protected] Rhizobium, and Mesorhizobium.3 The resource? Key words: , , wood, amount of nitrogen fixed by Leucaena is fast-growing , Mediterranean similar to or higher than that of crop 1 2 Emilio Badalamenti, Salvatore Pasta, legumes such as peanut and soybean, and 1 3 Contributions: EB and TLM conceived the Giovanna Sala, Valentina Catania, most of the fixed N is returned to the soil research and established methodology, all 3 1 4 Paola Quatrini, Tommaso La Mantia via leaf litter. Moreover, Leucaena benefits authors collected and analyzed data, GS ana- 1Agricultural, Food and Forest Sciences from the mycorrhizal symbiosis for lyzed the wood samples and determined ash content, EB, SP, GS, VC, PQ and TLM wrote Department, University of Palermo; increased nutrient and water uptake, reduced susceptibility to diseases, and the manuscript. 2Institute of BioSciences and increased biomass and growth. Positive BioResources (IBBR), Italian National effects of arbuscular mycorrhizal fungi Conflict of interest: The authors declare no Research Council (CNR), Unit of potential conflict of interest. 3 inoculation on its growth have been report- Palermo, Palermo; Department of ed under different conditions.5,6 Due to its Acknowledgements and Funding: Part of the Biological, Chemical and high nutritional value and protein content,2 Pharmaceutical Sciences and findings presented in this paper issues from fast-growing traits and rapid life-cycle, the field surveys carried out during the Technologies – STEBICEF - University Leucaena is a multipurpose which has Projects LIFE11+ NAT/IT/000093 “Pelagic of Palermo, Italy been successfully employed for ornamental Birds” (Linosa), Life Desert Adapt LIFE16 purposes, as livestock fodder, to obtain CCA/IT/000011 (http://www.desert- biomass and firewood, as well as to onlyadapt.it/index.php/it/) (Lampedusa) and the improve soil fertility, to control erosion, and implementation of the Programme 7,8 Abstract for the reforestation of marginal lands. BioDivMex Mistrals in collaboration with the However, Leucaena has also showed an Conseil National de la Recherche Scientifique With this contribution, an updated pic- invasive behaviour, rapidly spreading both (CNRS, Francia) - Site d’Etude en Ecologie Globale (Pantelleria). We thank Leonardo ture of the rapid expansion of Leucaena leu- in anthropogenic and ruderal habitats,use as a Scuderi (soc. Coop. Iberis) for sharing his per- cocephala subsp. glabrata in Sicily is pro- typical light-demanding pioneer plant, and vided. On the one hand, this is a quite wor- sonal unpublished data. The work was in semi-natural and forest habitats, especial- financed with Tommaso La Mantia’s fund Pj rying sign, as this woody species figures 9 ly if subject to frequent disturbance. autf 008567. among the world’s worst invasive alien Accordingly, it figures among the most dan- species. On the other hand, the species 10 gerous alien species in the world. Received for publication: 20 May 2020. shows interesting potential for production Leucaena has currently showed a marked Revision received: 28 July 2020. purposes (for wood, biomass and for feed- preference for the often fragile oceanic Accepted for publication: 28 July 2020. ing livestock), also considering its nitrogen island ecosystems,1 where it threatens fixation ability. Consequently, the two native vegetation and biodiversity, due to its This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 opposite options to cope with this species, ability to establish dense monospecific International License (CC BY-NC 4.0). i.e. cultivation and control/eradication, stands which prevent the regeneration of should accurately take into account the pos- native tree species, also altering the nitro- ©Copyright: the Author(s), 2020 sible uses as well as its invasive behaviour. 11,12 gen cycle. Furthermore, its great Licensee PAGEPress srl, Italy drought resistance, and the ability to with- International Journal of Plant Biology 2020; 11:8637 stand rather low annual rainfall (250-350 doi:10.4081/pb.2020.8637 Non-commercialmm),13 has recently allowed Leucaena to Introduction survive in Mediterranean-climate areas like prolonged flowering, and abundant (Lam.) de Wit Spain,14 where it is considered invasive. production. Like for other tree legumes, the (fam. , subfam. ) is a The high symbiotic promiscuity has invasive potential of Leucaena is exclusive- woody species native to and proba- allowed Leucaena to establish symbiosis ly linked to the characteristics of sexual bly to and Caribbean coun- with rhizobia native to different continents, reproduction. This monoecious and autoga- tries.1 Two main subspecies have been including , thus increasing its inva- described, mainly differing in the habit, i.e. sive potential. The ability to establish sym- mous species can produce fertile offspring in a very short time, being able to reach sex- the -like ‘common leucaena’ biosis with strains of Bradyrhizobium 9 Leucaena leucocephala (Lam.) de Wit canariense sv genistearum has been recent- ual maturity within the first year of life. subsp. leucocephala and the tree-like ‘giant ly reported in Portugal for the first time.15 Then, as early as two to three years of age, leucaena’ Leucaena leucocephala subsp. Sicily has been the only Italian region seed production begins to be almost contin- 1 glabrata (Rose) S. Zárate.2 Henceforth affected by the naturalization of Leucaena uous throughout the year, even reaching -2 -1 19 Leucaena leucocephala subsp. glabrata until recently.16 Just last year Leucaena has 5,500 m year . Leucaena was will be abbreviated as Leucaena. Also been observed growing wild in Sardinia, introduced to Europe almost two centuries 20 owing to its wide climatic plasticity, too.17 Moreover, Leucaena holds many of ago in the gardens of France and England, Leucaena was introduced in many tropical the biological traits most commonly found but the first signs of naturalization in and sub-tropical countries with average in invasive plant species of Mediterranean Europe date back only to the end of the last annual rainfall between 750 and 1,800 mm islands,18 such as anemochory, summer and century.13

[International Journal of Plant Biology 2020; 11:8637] [page 23] Review

and Favignana,27 and it is nearly fully estab- Conversely, some biotic and/or abiotic barriers Leucaena leucocephala in Sicily lished in Lampedusa (Table 1), where it has seem to prevent its establishment into semi- as an emblematic case for the been observed growing wild since 2012. natural and natural environments. In support of Mediterranean region Hence, Leucaena should be added to other this, we report an emblematic field observa- exotic woody species that are rapidly spread- tion from a mature Leucaena individual cul- Leucaena is probably one of the best ing in Sicily, like Acacia cyclops A.Cunn. ex tivated in the boundary of a countryside in examples of alien species which could be G.Don28 and Melia azedarach L.29 In Sicily, Palermo Province (municipality of properly used under some circumstances but Leucaena is currently able to establish exclu- Trappeto). Here, the species has shown high should not be used in others due to its invasive sively within disturbed and anthropogenic reproductive fitness, and a number of behaviour. Similar is the history of eucalypts in habitats such as roadsides and brownfields of seedlings, saplings or young trees enjoy Mediterranean habitats: suitable trees for pro- suburban areas, irrigated woody and herba- regular irrigation and tillage (Figure 1). viding high wood production in some con- ceous crops, and public or private green areas. Conversely, Leucaena appears unable to texts21 but increasingly invasive in riparian habitats.22 Hence, before choosing the most appropriate management option, it is necessary to take into account the current situation and the most likely future trends of the species in Sicily and in the whole Mediterranean area. Leucaena was introduced to Sicily, through the Botanical Garden of Palermo, in 1793.16 Although it began to produce fertile seeds very soon,23 it has not escaped from cul- tivation until recently. The first ascertained cases of naturalization concerned both the southern (Agrigento) and northern (Campofelice di Roccella and Cefalù) coasts only of the island.16 About a decade later, we pro- vide additional naturalization reports in more than 10 sites (Table 1), preferentially coastal areas, from 4 to about 120 m a.s.l., with about use 70% of sites located at less than 50 m a.s.l. Its recent spread in circum-Sicilian islands is of great concern. Leucaena has been introduced for ornamental purposes, and more rarely in reforestation, to Pantelleria24 (already cultivat- ed there in spring 1992, T. La Mantia, P. Quatrini and S. Pasta, pers. obs.), Ustica, 25 Figure 1. Massive natural regeneration of Leucaena underneath a mature individual cul- Linosa and Lampedusa. More recently, it tivated in a coastal area (Trappeto, province of Palermo) (photo by E. Badalamenti). behaves as a casual alien species in Linosa26

Table 1. Historical and new records of naturalization events by Leucaena leucocephala subsp. glabrata in Sicily. Year Location Altitude Habitat Reference (Municipality, Province) (m a.s.l.) or observer/s 2007 Agrigento (AG) n.s. Abandoned lands, roadside along the highway SS 118 R & D Campofelice di Roccella (PA) n.s. Citrus orchard, near the rail station Cefalù (PA) Non-commercial n.s. Roadside 2007 Ribera (AG), at the crossroads for “Piana Grande” 90 Roadside (together with Asclepias fruticosa L.) LS 2009 Trappeto (PA) 65 Irrigated fields EB 2011-2015 Palermo (PA) 35-94 Urban and suburban environments (gardens, irrigated pots, road borders and trees, the Botanical Garden, citrus groves) EB 2011 Service area of the Highway SS 115 (Ribera, AG) 25 Small escarpment on abandoned land EB & TLM 2011 Isola delle Femmine (PA) 33 Roadsides EB 2012-2020 Lampedusa (Porto Vecchio) (AG) 4-10 Palm grove in harbour area and sandy soils, and small escarpment EB & TLM 2012 Ribera (Secca Grande) (AG) 23 Roadside EB 2013 Villagrazia di Palermo (PA) 118 Irrigated fields EB 2014 Cefalù (PA) 47 Urban areas EB 2014 Balestrate (PA) 5 Afforestation and roadside EB 2014 Favignana (TP) 10 Base of a sidewalk LM 2015 Linosa (AG) 13 Private garden P & al 2019 Pantelleria (TP) 15 Abandoned lands EB & TLM EB = E. Badalamenti, TLM = T. La Mantia, LM=L. Maggioni27, P&al = Pasta et al28, R&D = Raimondo & Domina16, LS = L. Scuderi; n.s.: not specified.

[page 24] [International Journal of Plant Biology 2020; 11:8637] Review overcome the competition of the native importance to carry out regular monitoring found to promote the growth and establish- species of the adjacent perennial grassland of known nuclei, especially those close to ment of Leucaena individuals (P. Quatrini dominated by Hyparrhenia hirta (L.) Stapf, protected areas, natural and semi-natural pers. obs.). The subsequent naturalization of even if this plant community is very dis- environments and island ecosystems, which the species has proved its plasticity and turbed, as indicated by local abundance of are particularly vulnerable to the prolifera- ability to find in Mediterranean soils the Dittrichia viscosa (L.) Greuter, and with no tion of invasive alien species. In this sense, necessary symbiont microorganisms. Other doubt is easily reachable by Leucaena it is of great concern the recent spread of field experiments proved that Leucaena is seeds. Leucaena in Pantelleria National Park, a able to produce a high amount of wood even Such evidence, together with the cur- Mediterranean island with a high biodiver- under stressful climatic conditions such as 7 rent distribution, suggests a low competitive sity heritage. As a precautionary measure, limited water availability. A preliminary ability against native flora. However, it is Leucaena should be excluded from test of the productive potential of the worth highlighting its early achievement of afforestation interventions in similar sites, species was carried out, and the first exper- sexual maturity and its ability to rapidly in order to prevent fast spreading like that imental data are below reported. In a small 32 spread even at medium to long distances, a recently performed by Acacia spp. area with homogeneous soil conditions and key factor for invasive .30 Although Contrariwise, several experiments have uniform plant growth, seven woody disks the majority of naturalized Leucaena indi- been recently carried out to verify the from seven trunks of Leucaena plants, cut at viduals were observed growing near the potential of Leucaena for productive pur- the base, were sampled. The age of the sam- mother plants, some of them have been poses. Particularly, Rhizobium spp. strains pled plants ranged from 2 to 7 years. The detected more than 500 meters far from isolated from Acacia saligna (Labill.) H.L. mean annual diameter increment was 1.20 -1 them. Furthermore, the Sicilian nuclei Wendl. and Prosopis spp. root nodules were cm year , with the younger trees (2-4 promptly resprout after fire passage and/or mechanical damages caused by periodic road maintenance interventions. A remark- able plasticity in terms of light requirements was also observed, although Leucaena is a only typical pioneer and light-demanding species. In the Campus of the SAAF Department of the University of Palermo, numerous seedlings and saplings were use found under the canopy of large exotic fig trees such as Ficus microcarpa L. and Ficus macrophylla f. columnaris (C. Moore) D.J. Dixon (Figure 2). Both species are widely known for the high shading, one of the rea- sons why Ficus microcarpa is considered an excellent species for urban streets. This is further confirmed by the occurrence under their canopies of Hedera helix L., a shade-tolerant species (Figure 2). The adap- tation to a wide range of soil conditions has been also pointed out. In the port of Figure 2. Leucaena saplings growing under the shady canopy of Ficus macrophylla f. Lampedusa Island, Leucaena was found columnaris at the Campus of SAAF Department (University of Palermo). Please remark the lack of other plant species except for Hedera helix (photo by E. Badalamenti). invading a date Palm (Phoenix dactylifera L.) grove just a few steps from the sea, on purely sandy and brackish soil (Figure 3). The species has been observedNon-commercial in similar environments in Israel.16

Future perspectives: to use or not to use Leucaena? One constraining factor for the future spread of Leucaena in Sicily is its use, cur- rently limited to public and private green areas. On the other hand, the growing num- ber of reports and the characteristics of Leucaena would suggest to be cautious when assessing its invasive potential in Mediterranean-climate habitats.13 The expected climatic trends could favour the success of the species and the speed of its Figure 3. Naturalized young Leucaena individual growing at the Port of Lampedusa. future invasion.31 It is therefore of great

[International Journal of Plant Biology 2020; 11:8637] [page 25] Review years) showing the highest increment rate ing vegetation and biodiversity, and areas on the native plant community in the (1.77 cm year-1). Regarding fuel properties where Leucaena should be cleared at all to Ogasawara (Bonin) Islands. Weed of Leucaena biomass, Feria et al. (2011)33 prevent its invasion. As a precautionary Technol 2004;18:1371-75. reported calorific values equal to 18.95 MJ measure, the introduction of Leucaena 12. Guézou A, Pozo P, Buddenhagen C. kg-1, i.e. higher than those obtained from within protected areas (e.g. those belonging Preventing establishment: an inventory the residues of food plants and agricultural to Natura2000 network) should be strictly of introduced plants in Puerto Villamil, crops. In our wood samples, the ash content forbidden. Isabela Island, Galapagos. PLoS ONE varied from 1.41 to 3.73% of dry weight in 2007;2:e1042. plants with diameter from 2.2 to 4.3 cm. 13. Dana E, Randall RP, Sanz-Elorza M, The young plants showed the highest con- References Sobrino E. First evidence of the inva- sive behaviour of Leucaena leucocepha- tent. The values of ash content reported in 1. Binggeli P, Hall JB, Healey JR. An our work are similar to those obtained in la in Europe. Oryx 2003;37:14. 33 Overview of Invasive Woody Plants in other countries. According to the ruling the Tropics. School of Agricultural and 14. Sanz-Elorza M, Dana ED, Sobrino E. ISO 17225-1:2014, defining fuel quality Forest Science Publication No.13. Atlas de las Plantas Alóctonas Invasoras classes and specifications for solid biofuels, University of Wales, Bangor, 1998. en España. Madrid: Dirección General the analyzed wood samples of Leucaena 2. Bageel A, Honda MDH, Carrillo JT, para la Biodiversidad; 2004. would be classified as A1.5 (≤1.5%). These Borthakur D. Giant leucaena (Leucaena 15. 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Non-commercial

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