Comparative analysis of the total endemic species in each area with the number of endemic species exclusive to that area.
\r\n\tThis book will be a self-contained collection of scholarly papers targeting an audience of practicing researchers, academics, PhD students and other scientists. The contents of the book will be written by multiple authors and edited by experts in the field. The area of interest and scope of the project can be described with (but are not limited to) the following keywords: Alcoholism, Depression, Addiction, Blackouts, Relapse, Binge Drinking, Genetic basis, Neurological Aspects, Treatment, Organ Damage.
\r\n\r\n\tAuthors are not limited in terms of topic, but encouraged to present a chapter proposal that best suits their current research efforts. Later, when all chapter proposals are collected, the editor will provide a more specific direction of the book.
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Venkateswarlu",coverURL:"https://cdn.intechopen.com/books/images_new/371.jpg",editedByType:"Edited by",editors:[{id:"58592",title:"Dr.",name:"Arun",surname:"Shanker",slug:"arun-shanker",fullName:"Arun Shanker"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"878",title:"Phytochemicals",subtitle:"A Global Perspective of Their Role in Nutrition and Health",isOpenForSubmission:!1,hash:"ec77671f63975ef2d16192897deb6835",slug:"phytochemicals-a-global-perspective-of-their-role-in-nutrition-and-health",bookSignature:"Venketeshwer Rao",coverURL:"https://cdn.intechopen.com/books/images_new/878.jpg",editedByType:"Edited by",editors:[{id:"82663",title:"Dr.",name:"Venketeshwer",surname:"Rao",slug:"venketeshwer-rao",fullName:"Venketeshwer Rao"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"4816",title:"Face Recognition",subtitle:null,isOpenForSubmission:!1,hash:"146063b5359146b7718ea86bad47c8eb",slug:"face_recognition",bookSignature:"Kresimir Delac and Mislav Grgic",coverURL:"https://cdn.intechopen.com/books/images_new/4816.jpg",editedByType:"Edited by",editors:[{id:"528",title:"Dr.",name:"Kresimir",surname:"Delac",slug:"kresimir-delac",fullName:"Kresimir Delac"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}}]},chapter:{item:{type:"chapter",id:"56036",title:"Biogeographical Areas of Hispaniola (Dominican Republic, Republic of Haiti)",doi:"10.5772/intechopen.69081",slug:"biogeographical-areas-of-hispaniola-dominican-republic-republic-of-haiti-",body:'\nThe geological history underlying the formation of the island of Hispaniola [1], the great differences in altitude and the wide range of substrates, have all led to the existence of 2050 endemic species distributed across a wide variability of habitats with an endemic nature that must be highlighted for the purposes of conservation. Therefore, in previous works, we started our study with a biogeographic proposal for the Spanish island [2].
\nWe therefore begin our study for a biogeographical proposal for the island of Hispaniola with the general description by Takhtajan [3] on floristic regions in the world, and the work of Rivas Martínez et al. [4] on North and Central America, which establishes the rank of sector for the island of Hispaniola, and includes it within the Neotropical‐Austro‐American kingdom, the Caribbean‐Mesoamerican region and the province of the Antilles. The studies by Borhidi [7] on the island of Cuba [5, 6] all recognise clear differences between the Greater Antilles (Cuba, Hispaniola, Jamaica and Puerto Rico) and the Lesser Antilles, based—among other considerations—fundamentally on the high biodiversity and distribution of species in the Orchidaceae family. Together with the existing local studies on the island of Hispaniola [8, 9] and our own recent fieldwork, we can establish a biogeographical typology based on the elemental biogeographical unit or tesela, defined as a variable area—either continuous or discontinuous—with a homogeneous geomorphological and ecological character giving rise to a single type of potential vegetation.
\nThe island of Hispaniola with a territorial extension of 76,486 km2 is divided between Doninican Republic and Republic of Haiti, it is an island very much studied from the floristic point of view, with very few studies of vegetation, with few studies like the one by Borhidi [7].
\nThe importance of the study is due to the high diversity of endemic species and habitats that are of interest for conservation, with species and habitats subject to high human pressure, despite being a hot spot for the Caribbean.
\nIn general, the island is dominated by areas very antropizadas, especially Haiti, where the human pressure is excessive; while in the Dominican Republic, anthropogenic action is somewhat lower, with areas dedicated to livestock and agriculture. However, there are two large well preserved landscape units: the rainforests of the mountains and the dry sub‐deciduous forests.
\nWe conduct a botanical study from a biogeographical approach; as notwithstanding the numerous botanical and floristic works of investigation by researchers such as Urban, Ekman, Cicero, Donald Dungan, Marcano Fondeur, Jürgen Hoppe, Liogier, Zanoni, Hager, May, Borhidi, Megía, Jiménez, R. García, A. Veloz and others, very few studies have been undertaken from the perspective of phytogeography and vegetation science. Recent works have taken a floristic and physiognomic rather than a phytosociological approach [4, 8–18, 20, 21]; studies using a phytosociological methodology include Refs. [22–31]. The authorship of the species is mentioned only once in the text and is taken from Ref. [36].
\nThe different types of habitats present on the island of Hispaniola are studied. For this purpose, we have performed over 300 years of phytosociological sampling as per Ref. [32]. At the same time, we do a floristic study on the distribution of 1500 endemisms. In order to explain the distribution of the different plant communities, a bibliographical and field‐based study was carried out on existing geological materials, and a bioclimatic study of ombrotipos and thermotypes is presented in refs. [4, 33–35].
\nThe island’s geological origin, the bioclimatic analysis with thermotypes ranging from the infratropical to the supratropical, with semiarid to hyperhumid ombrotypes, the origin of the flora as a result of migratory routes and the past isolation of the various sierras and mountains, all account for the large number of endemic species and habitats. The island has 1284 genera, of which 31 are endemic to Hispaniola: Zombia, Leptogonum, Arcoa, Neobuchia, Fuertesia, Sarcopilea, Salcedoa, Eupatorina, Vegaea, Coeloneurum, Theophrasta, Haitia, Stevensia, Samuelssonia, Hottea, Tortuella and Anacaona, among others. Several of the endemic genera are monotypes and have a restricted area, such as Vegaea pungens Urb., Zephyranthes ciceroana M. Mejía & R. García, Gautheria domingensis Urb., M. domingensis, Omphalea ekmanii Alain, Gonocalyx tetrapterus A. Liogier, Goetzea ekmanii, Reinhardtia paiewonskiana R.W. Read, T. Zanoni & M. Mejía, Pseudophoenix ekmanii Burret and Salcedoa mirabaliarum F. Jiménez & L. Katinas; or else local endemic species such as Pinguicula casabitoana, Fuertesia domingensis Urb., Pereskia quisqueyana, M. jimenezii Alain and Salvia montecristina.
\nThere are a total of 5800 species according to [36], a figure that was subsequently extended by [37] to 6000 vascular species distributed in 1284 genera, with an estimated 2050 endemic species. Our study characterises the various biogeographical territories based on 1582 endemic species distributed in 19 areas (A1–A19), together with their own vegetation catenas, which we in turn break down into two subprovinces: the Central subprovince and the Caribbean‐Atlantic subprovince, both clearly separate due to differences in their geological, bioclimatic, floristic and vegetation origin.
\nThe province is characterised by a large number of endemic species, of which 114 belong to the family Melastomataceae [24]. The presence of a high number of endemic species with a widespread distribution on the island causes the application of Pearson’s index to result in a low relation between areas A12 and A16 (r = 1.25), due to their different geological and floristic nature; between A16 and A13 (r = 1.17); and between A12 and A13 (r = 1.23). In this last case, the low relation between the two areas derives from the difference in the number of endemics. Although both zones have calcareous substrates, A13 has suffered greater human impact. A16 and A17 are highly separated, which is unsurprising as the Massif du Nord (A17) is a prolongation of the Central Cordillera range (A16). The frequent presence of calcareous islands and the intense human pressure in A17 is a further reason for their separation, with A17 acquiring a greater similarity with A15 (northwest Haiti).
\nThe Jaccard analysis reveals that areas A12 and A16 have a distance of 0.9, representing a coincidence of only 10% and differences of 90%; this is also the case between A16 and A17, as this analysis corroborates that A17 has greater similarity with A15. The results of Pearson’s analysis for areas A12 and A13 are similar to those obtained with the Jaccard analysis [24].
\nThe Central Cordillera is characterised by a predominance of siliceous materials and a tropical rainy and tropical pluviseasonal macrobioclimate on the summits, occasionally tropical xeric at the base. All this has led to the development of a particular endemic flora with 451 different endemic species and vegetation units [11]. This biogeographical territory (BT) contains a single area, A16, Central‐Eastern, occupying the Central Cordillera (Dominican Republic), and dominated by siliceous materials with slight inclusions of serpentines in the easternmost area, representing the transition to the Yamasense biogeographical unit. The thermotype ranges between the infra and supratropical, and the dominant ombrotype is humid‐hyperhumid. The penetration of the trade winds causes the presence of both broadleaf rainforest and cloud forest towards the mid‐mountain, with a dominance of species from the genera Prestoea, Magnolia, Didymopanax, Cyathea; while the high‐mountain areas beyond the reach of the trade winds are home to Pinus occidentalis, a forest belonging to the endemic habitat Dendropemon phycnophylli–Pinetum occidentalis Cano, Veloz & Cano‐Ortiz 2011, alternating with hemicryptophytic communities of Danthonia domingensisFigure 1.
\nVegetation catena of the Central Cordillera 1. Subhumid broadleaf forest. 2. Sierran palm forest. Community of Prestoea montana and Cyateas (palms). 3. Community of ‘palo de viento’ Didymopanax tremulus and isolated individuals of Prestoea montana. 4. Pinus occidentalis pine forest belonging to the association Dendropemon phycnophylli–Pinetum occidentalis. 5. Hemicryptophytic high‐mountain grassland of D. domingensis among the cleared pine forest of Pinus occidentalis.
In previous works, we proposed the following biogeographical territories (BT) (biogeographical sectors) for the Caribbean‐Atlantic subprovince: 2.1. Bahoruco‐Hottense (A12, A13); 2.2. Neiba‐Matheux‐North‐western (A14, A15, A17 and A19); 2.3. Azua‐ San Juán‐.Hoya Enriquillo‐Port au Prince‐Artiobonite‐Gonaivës (A9, A10, A11 and A18); 2.4. Caribbean‐Cibense (A3, A7 and A8); 2.5. Northern (A1, A2, A4, A5 and A6) [24].
\nBT‐2. 1. The Bahoruco‐Hottense district includes two areas or districts (A12 and A13). The Sierra de Bahoruco and its continuation in the Massif de la Selle and de la Hotte in Haiti have a similar geological origin and frequently suffer the impact of Caribbean hurricanes. The ombrotype in these territories ranges from subhumid to hyperhumid, leading to a predominance of broadleaf cloud forest, sierran palm forests of Prestoea montana, cloud forest of Magnolia and Didymopanax, and—in the supratropical thermotype on the summits—a pine forest of P. occidentalis, belonging to the association Coccotrino Scopari‐Pinetum occidentalis Cano, Veloz & Cano‐Ortiz 2011. The general vegetation catena characterising this biogeographical territory is therefore conditioned whether it is a dry forest, broadleaf forest, cloud forest or high‐mountain pine forest. In addition, due to its high rate of endemic species, this biogeographical territory is of interest for conservation. We are unaware of the existence of Podocarpus aristulatus Parl. and Ocotea wrightii (Meisn.) Mez in the Bahoruco‐Hottense sector; and this BT thus reveals significant differences when compared with the Neiba‐Matheux‐North‐western sector. The relation between the two areas (A12 and A13) in this BT is low, as they present a certain number of different endemic species with an r = 1.23 Figure 2.
\nVegetation catena in the Sierra de Bahoruco. 1. Mangrove forests of Machaerio lunati‐Rhizophoretum manglis. 2. Salt marsh communities in the class Batidi‐Salicornietea. 3. Dry forest of Pilosocereus polygonus and Acacia sckleroxyla. 4. Hemicryptophytic grassland of Melocacto pedernalensis‐Leptochloopsietum virgatae. 5. Cloud forest of Magnolia hamorii and Didymopanax tremulus. 6. Sierran palm forest (forest of Prestoea montana and Cyathea arborea). 7. Pine forest of Coccotrino scopari‐Pinetum occidentalis.
BA‐A12. The Bahoruco‐La Selle district occupies calcareous mountain ranges with an occasionally supratropical thermotype. There is a broadleaf cloud forest of M. hamorii and D. tremulus, while on rainier sites and in gorges, there is a presence of formations of P. montana. This unit is home to forests of M. hamorii growing between 950 and 1500 m, as precipitation exceeds 2000 mm. These forests are characterised by M. hamorii, L. bahorucanus, Mikania venosa Alain, C. domingensis, Rondeletia ochracea Urb., P. guadalupensis, H. domingensis, Arthrostylidium sarmentosum Pilger, Weinmannia pinnata L., M. ovatum, Vriesea tuercheimii, D. tremulus, Meriania involucrata (Desr.) Naud. and Polygala fuertesii (Urb.) Blake. The same cloud forest at higher altitudes, where the pressure of the wind is greater, is enriched by D. tremulus, and on rainier sites and in moist gorges by the sierran palm forest of P. montana. A pine forest of P. occidentalis is found growing in the supratropical thermotype, with C. scoparia, A. intermixta, N. domingensis, Eupatorium sinuatum Lam. var viscigerum Urb. & Ekm., Staurogyne repens, G. ruolphiodes var haitiensis and S. barahonenis, belonging to the association Cocotrino scopari–Pinetum occidentalis Cano, Veloz & Cano‐Ortiz 2011.
\nIn basal zones such as the Procurrente de Barahona, Ceitillan and Pedernales, the ombrotype is semiarid and the thermotype is infratropical. There is a predominantly dry forest, with a floristic composition comprising Lomandra hystrix, P. polygonus, Ceratocystis moniliformis, Antillesoma antillarum, Coriandria caribaea and Melocactus pedernalensis, in whose clearings there is a hemicryptophytic and endemic community of Melocaptoa pedernalensis‐Leptochloopsietum virgatae Cano, et al. [24, 25]. In coastal areas, it is worth highlighting the presence of mangrove forests of R. mangle, L. racemosa and A. germinans, enriched towards drier areas with C. erectus. In these territories, the mangrove forest alternates with halophilous communities of S. portulacastrum. This area has a high rate of endemic species, with 693 endemic plants.
\nBA‐A13. The Hottense district is characterised by calcareous substrates whose geological origin is similar to that of La Selle and Bahoruco. It is located at the end of the southwest peninsula (Haiti), and has 171 endemic plants, but in lesser numbers than in the Bahoruco‐La Selle area. However, this biogeographical unit is home to the endemic genus Hottea, which is distributed throughout the biogeographical units A12, A13 and A14; the highest numbers of endemic species in this genus are found in A13. This biogeographical unit has a thermotype that ranges between the infra and mesotropical, and the ombrotype is dry in the basal areas to humid on the summits of La Hotte.
\nBT‐2.2. The Neiba‐Matheux‐North‐western sector has four districts (A14, A15, A17 and A19). It is floristically characterised by the presence of 90 endemic species such as Guettarda oxyphylla Urb. and Chionanthus dictyophyllus (Urb.) Stearn, with its own vegetation catenas ranging from the dry to the subhumid and cloudy, with pine forests of P. occidentalis on the summits. Two of the areas in this biogeographical territory (A14 and A15) have a relation r = 0.93, indicating major floristic differences between both biogeographical units Figure 3.
\nVegetation catena in the Sierra de Neiba. 1. Forest of Pinus occidentalis. 2. Sierran palm forest of Didymopanax tremulus and Podocarpus aristulatus; 3. Broadleaf mahogany forest of Swietenia mahagoni.
BA‐A14. The Neiba‐Matheux district covers the calcareous mountain ranges of Neiba, Matheux and Noires with an altitude of 1793 m and a dry, subhumid‐humid ombrotype and an infra, thermo and mesotropical thermotype, which is occasionally supratropical in the Massif des Montagnes Noires. It is home to a rare broadleaf forest of P. aristulatus, a cloud forest of P. montana and a forest of D. tremulus which is enriched with P. aristulatus, O. wrightii, Persea krugii Mez and Brunellia comocladifolia H. & B. In the highest sites in the Neiba range, it is still possible to find pine forests of P. ocidentalis on calcareous substrates over a limited extension. This area reveals a certain influence of the Central province due to the presence of P. aristulatus, which is also located near Valle Nuevo (Central Cordillera) and the absence of M. hamorii; the presence of the pine forest of P. occidentalis connects it with Bahoruco. There are 27 endemic species exclusive to this area.
\nBA‐A15. This district is located in the northwest of the Republic of Haiti and also has a predominance of carbonated rocks. These territories are exposed to the trade winds from the Atlantic. However, as they contain no major elevations—the maximum altitude of around 840 m—the dominant ombrotype is subhumid. West‐facing areas connecting with Gonaive and Hene Bay have a dry ombrotype, as this is an area of shade, and a thermotype ranging between infra and mesotropical. The floristic character is based on the presence of 59 endemic species.
\nBA‐A17. The Central‐Western district occupies the whole of the Massif du Nord in Haiti. This mountain is a prolongation of the Central Cordillera. In this case, there is also a dominance of siliceous materials with the inclusion of basic substrates; the thermotype is infra to mesotropical, and the ombrotype ranges from subhumid to humid. We collected fewer endemic species (60) in this biogeographical unit than in the Central‐Eastern unit (A16), as these areas are highly altered, as is generally the case in the whole of the Republic of Haiti, which has suffered widespread deforestation throughout its history.
\nBA‐A19. The Tortuga Island district is calcareous in nature and located in the north of Haiti, at a maximum altitude of 378 m so the trade winds only reach the highest areas. The vast majority of the territory has a dry ombrotype, occasionally becoming subhumid‐humid. The relation of A19 with the nearest areas—A3 and A15—is r = 1.02 and r = 0.89. In spite of its small size, the presence of the monotypical genus Tortuella abietifolia Urb. & Ekman and 15 exclusive endemic species justifies its consideration as a biogeographical unit in itself.
\nBT‐2.3. The Azua‐San Juán‐Hoya Enriquillo‐Port au Prince‐Artiobonite‐Gonaivës sector (A9, A10, A11 and A18) covers all the low‐lying areas in the south of the Dominican Republic and west of Haiti. These territories are differentiated from the Procurrente de Barahona as they have soft deposit materials, despite their similar infra and thermotropical thermotype and semiarid‐dry ombrotype. However, in this case, there is an occasional presence of the subhumid ombrotype on the heights of the Sierra Martín García, which represents a small island surrounded by dry forest, distinguishing this area from the previous one. Although most of the territory is dominated by dry forest, there is an occasional presence of broadleaf forest on the summits of Martín García. Unlike in Bahoruco and Neiba, there are no formations of P. occidentalis. The dry forest in this biogeographical unit is dominated by the species P. polygonus, L. hystrix, A. antillarum, Mimosa diplotricha C. Wright ex Sauvalle, Brya buxifolia (Murr.) Urb., N. paniculada, Thouinia domingensis Urb. & Radlk., Solanum microphyllum (Lam.) G. Don., Coccotrinax spissa Bailey, A. skleroxyla, Scolosanthus triacanthus (Spreng.) DC., C. moniliformis, M. lemairei and C. caribaea. In view of the differences in flora, vegetation, geology, ombrotype and thermotype, these areas should be treated as specific biogeographical territories. In all cases, the relations between the four areas proposed have a value of r in Pearson’s index of equal to or less than 1, as they share very few endemic species.
\nBA‐A9. The Azua‐Sán Juán‐Hoya Herniquillo district is an area that extends from Bani and Azua towards the Sán Juan river valley as far as the border with Haiti, where it becomes what is known as the Central Plain in Haiti, with higher elevations. The Cordillera Central in the Sierra de Neiba is separated through the Sán Juán valley. These semiarid‐dry territories border the Sierra de Neiba along the south, and extend along Lake Herniquillo to Jimani and Malpaso. From a geological point of view, there is a predominance of soft materials of a Quaternary nature with gypsum islands in the areas near Herniquillo Lake. There is a constant infra and thermotropical thermotype and a semiarid‐dry ombrotype. This district has 85 endemic species, some as emblematic as N. paniculada, M. lemairei, Acacia barahonesis Urb. and Zanthoxylum azuense (Urb. & Ekm.) Jiménez, which give the territory its distinctive character. This area is characterised by the presence of habitats such as the association Solano microphylli‐Leptochloopsietum virgatae Cano, et al. [24, 25] Figure 4.
\nVegetation catena of the Azua district. 1. Broadleaf forest of Acacia skleroxyla and Coccothrinax boschiana. 2. Dry forest of Neoabbottio paniculatae‐Guaiacetum officinalis. 3. Hemicryptophytic community of Solana microphylli‐Leptochloopsietum virgatae.
BA‐A10. The Central Plain district (Haiti) ascends through the area of the Sán Juán valley, past the upper stretch of the Artibonite River at altitudes of 100 m. There exists a territory with no natural vegetation that is used for agriculture (Haiti). This is the location of the Central Plain in Haiti, standing at a height of 300–400 m and separating the Massif des Montagnes Noires at 1793 m and the calcareous substrates in the siliceous Central Cordillera (Massif du Nord), with maximum altitudes of 1210 m. This district (A10) has calcareous clayey substrates, a thermotropical thermotype and a dry ombrotype, and differs from the semiarid‐dry forest in unit A9. This difference is evidenced in the values of Pearson’s index—r = 0.91—as the Central Plain in Haiti has higher rainfall, and in its eight endemic species: Bumelia picardae Urb., Carpodiptera hexaptera Urb. & Ekm, Dorstenia flagellifera Urb. & Ekman, Malpighia aquifolia L., Malpighia setosa Spreng., Phenax pauciflorus Urb., Plumeria paulinae Urb. and Thouinidium pinnatum (Turp.) Radlk.
\nBA‐A11. The Port au Prince‐Arbiobonite‐Gonaives district is past Jimini (Dominican Republic), approaching the border with Haiti and entering the plain of Port au Prince, where the materials continue to be soft and Quaternary in origin. The thermotype is infra and thermotropical, and the ombrotype is semiarid‐dry due to the lack of rain, as these are areas of shadow. The Sierras de Bahoruco, La Selle and Neiba act as a barrier in the south, and those of Matheux, Noires and the Central Cordillera do the same in the northeast. The altitudes range between 0 and 100 m. These are areas with scarcely any natural vegetation as they are used for agriculture; the semiarid‐dry character of the territory is prolonged the length of the northern fringe of the Massif de la Selle and de la Hotte, from Port au Prince bay to Gran Caimite, an island that is also part of this biogeographical unit. The territory extends to the southwest of the Massif de Matheux and borders these mountains before entering the Artiobonite river valley as far as the locality of Mirebalais, and northwards towards Gonaives. There are 70 endemic species in these territories, which form part of the different habitats in the dry forest in this biogeographical unit: Catesbaea sphaerocarpa Urb., C. dictyophyllus, Guettarda multinervis Urb., Stigmaphyllon haitiense Urb. & Ndz. and Psychotria haitiensis Urb.
\nBA‐A18. Gonave Island is located in the middle of Port au Prince bay, with altitudes of 702 m. It is practically devoid of natural vegetation as a result of intense human pressure. This satellite island of Hispaniola has an infra and thermotropical thermotype and a semiarid‐dry ombrotype. Due to its isolation, the floristic analysis reveals the presence of 20 endemic species, of which the following are exclusive to the island: Mouriri gonavensis Urb. & Ekman, Solanum aquartia Dunal var luxurians (O.E. Schulz) Alain, Dendropemon gonavensis Urb., Dendropemon spathulatus Urb. & Ekman, Galactia caimitensis Urb. & Ekman, Isidorea gonavensis Aiello & Borhidi and Pilea dispar Urb. = (Pilea gonavensis Urb.). It shares some endemic species with unit A11—with a Pearson’s index of r = 0.83—and the same type of vegetation (dry forest). We therefore include it in the same biogeographical sector.
\nBT‐2.4. Caribbean‐Cibense (A3, A7 and A8). This biogeographical territory comprises three geomorphological units that include the Eastern Coastal Plain, the Sierras de Yamasá and Prieta, and the Cibao Valley. The eastern coastal areas on the shores of the Caribbean have an altitude of less than 100 m, and are coralline in origin; in contrast, in the Cibao Valley, there is a dominance of alluvial materials, Miocene conglomerates, schists, Miocene loams, limestone hills, clays and calcareous loams. Both geomorphological units are separated by the Sierras of Yamasá and Prieta, in which there is an amalgam of substrates, as this is a crossroads between the Central Cordillera, Los Haitises, the Eastern Coastal Plain and the Cibao Valley. There are frequent serpentines, which can also be found in the province of Dabajón in the Cibao Valley, leading to the widespread presence of a dry spiny forest and a pine forest. The thermotype for this BT ranges from infra to thermotropical and the ombrotype is semiarid to subhumid; however, due to the type of substrate—serpentines and perforated coralline limestones—the territory behaves as dry. All this causes the predominance of a dry forest. This biogeographical unit has particular vegetation associations and catenas. The general vegetation catena is the dry and semi‐deciduous forest of M. toxiferum, S. mahagonii and C. diversifolia. It has a large number of endemic species, distributed in the three biogeographical areas. The relation between the areas in this BT is: r = 0.95 for A3–A7, r = 0.97 for A3–A8 and r = 1.01 for A7–A8 Figure 5.
\nVegetation catena of the Caribbean coastal unit. 1. Association Zamio debilis‐Metopietum toxiferi. 2. Community of Zamia debilis. 3. Association Chrysophyllo oliviformi‐Sideroxyletum salicifolii.
BA‐A3. The Cibao Valley district is characterised by a predominance of Miocene limestone, loams and conglomerates, along with the serpentines of Dabajón. The infra and thermotropical thermotype and the semiarid‐dry ombrotype have produced a dry forest flora and vegetation, and the presence of 67 endemic plants in this area. The endemic dry forest in the territory comprises a community of L. hystrix and Croton astrophorus Urb., C. caribaea, Mammillaria prolifera (Mill.) Haw., Phyllostilon brassiliensis Capan., H. nashii, P. polygonus, B. buxifolia, Opuntia antillana Britt. & Rose, C. moniliformis, Lantana camara L., Turnera difusa Willd. ex Schult, Abutilon abutiloides (Jacq.) Garcke, O. dillenii, Malpighia cnide K. Spreng., C. poitaei, S. triacanthus, Erytroxylum rotundifolium Lunam, Croton discolor Willd., A. antillarum, M. lemairei, Maytenus buxifolia (A. Rich.) Griseb., L. virgata, Phyllostilon rhamnoides (J. Poiss.) Taub, A. tortuosa, Caesalpinia coriaria (Jacq.) Willd., Caesalpinia buchii Urb. and Anthirea montecristina Urb. & Ekm. [29]. Along with this dry forest it is frequent to find habitats of Leptochloopsis virgate and Crotono astrophori‐Leptochloopsietum virgatae Cano, et al. [24, 25], and mangrove forests of Rhabdadenio biflori‐Laguncularietum racemosae Cano et al. [27].
\nIn serpenticolous territories, there is a pine forest or community of P. occidentales, Calliandra haematomma (Benth.) Benth., Tabebuia berterii (P.DC.) Britt, Chrysophyllum. oliviforme L., Psychotria dolichocalix Urb. & Ekm., Smilax habanensis Jacq., Sideroxylon cubense (Griseb.) Penn., Miconia laevigata (L.) DC. = (Miconia pyramidalis (Desr.) DC., Croton linearis Jacq., Rondeletia cristi Urb., O. ilicifolia, Leptogonum buchii Urb., Guettarda pungens Urb., Ternstroemia peduncularis A. DC., Randia aculeata L., Byrsonima crassifolia (L.) HBK. and L. camara. This is an exclusive habitat in this biogeographical unit that, along with other communities, serves to establish the differences with the other biogeographical territories: Leptogono buchi‐Pinetum occidentalis Cano, et al. [26, 19] Figure 6.
\na. Vegetation catena of the Cibao Valley. 1. Association Leptogono buchii‐Pinetum occidentalis. 2 and 3. Dry forest of Harrhisio nashii‐Prosopidetum juliflorae [29]. b. Vegetation catena of the Cibao Valley. 1. Association Crotono astrophori‐Leptochloopsietum virgatae. 2. Association Machaerio lunati‐Rhizophoretum manglis and Rhabdadenio biflori‐Laguncularietum racemosae. 3. Dry forest of Harrhisio nashii‐Prosopidetum juliflorae.
The Eastern Caribbean area occupies the whole of the coastal plain overlooking the Caribbean Sea. Its coralline origin causes the substrate to be highly porous, and although the rainfall is over 800 mm, the territory acts as dry. There is a strong floristic similarity between these territories in the Cibao Valley and the areas in the southwest, and to a lesser degree between this area and that of Yamasá. There are also differences between the flora, habitats and uses of the territory and the dry areas in the southwest, as the territories on the eastern coastal plain are essentially used for the cultivation of sugarcane and coconut. These eastern plains must therefore be treated as specific biogeographical areas. There are 60 endemic species of flora, some of which have problems of conservation, as is the case of P. quisqueyana. In terms of vegetation, it has its own characteristic plant communities depending on the substrate. The dry forest occurs when the soil is thin and porous, but if the soil is deep, these dry phytocoenoses become transformed in semi‐deciduous forests in transition between the dry and evergreen forest, comprising a forest of S. mahagonii, M. toxiferum, Krugiodendron ferreum (Vahl) Urb., C. diversifolia, Guaiacum sanctum L., Thouinia trifoliata Poit., Z. debilis, Coccotrinax barbadensis (Lodd ex Mart.) Sarg., Exostema caribaeum (Jacq.) R. & S., Sideroxylon salicifolium (L.) Lam., C. oliviforme, A. bilobata and others. On sites with more intense water runoff, there is a dry forest of Sideroxylon foetidissimum (Jacq.) Cron., P. quisqueyana, P. polygonus, L. weingartianus, B. simaruba, Clusia rosea Jacq., S. salicifolium, Celtis trinervia Lam., B. buceras, Cissus oblongo‐lanceolata (Krug & Urb.) Urb., Ficus citrifolia P. Mill., C. diversifolia, G. sanctum, A. skleroxyla, M. jimenezii, P. unguis‐cati, C. oliviforme, K. ferreum, Guapira fragrans (Dum. Cours.) Little and Capparis cynophallophora L. Forests recently diagnosed by us are Chrysophyllo oliviformi‐Sideroxyletum salicifolii Cano & Veloz 2012 and Zamio debilis‐Metopietum toxiferi Cano & Veloz 2012. The mangrove forests in the association Sthalio monospermae‐Laguncularietum racemosae Cano et al. 2012 give this eastern biogeographical area its characteristic appearance.
\nBA‐A8. The Yamasá district is a complex geomorphological unit occupying the Sierra Prieta and Yamasa ranges. It has siliceous, limestone and serpentine substrates, the last of which cause the appearance of endemic serpenticolous communities with a spiny character. This is a xerophytic high shrubland, and throughout the Quaternary era, this territory served as a route for the passage of species between the xeric areas in the Cibao Valley and the Eastern Coastal Plain and the xeric areas in the southwest. The presence of serpenticolous elements and endemic habitats in our study, such as the community of C. haematomma, Phyllanthus nummularioides Muell. Arg., Caliptrogenia biflora Alain, Eugenia crenulata (Sw.) Willd., Coccotrinax argentea (Lodd.) Sarg., L. buchii, Coccoloba nodosa Lindau, Coccoloba jimenezii Alain, Croton impressus Urb., T. peduncularis, Garcinia glaucescens Alain & M. Mejía, Scolosanthus densiflorus Urb., Rondeletia berteroana DC., Oplonia spinosa (Jacq.) Raf., Eugenia dictyophylla Urb., Pictetia spinifolia (Desv.) Urban and Z. debilis, serves as differentiating elements to establish the Yamasense area. These floristic peculiarities are related to the origin of the territory, which is why different connection forces can be established with the neighbouring territories in the various statistical studies on the rates of endemic species. Although these considerations might suggest a wide biogeographical territory, the absence of its own vegetation catenas, the fact it has a xerophytic vegetation and has served as a migratory route between the biogeographical area of the Eastern Caribbean and the Cibao Valley all lead us to propose this as a highly original biogeographical area Figure 7.
\nVegetation catena of the Sierra de Yamasá. 1. Association Coccotrino argentei‐Tabebuietum berterii. 2. Tangled scrubland of Garcinio glaucescentis‐Phyllanthetum numularioidis [28].
BT‐2.5. The areas in the north of the island include five biogeographical districts (A1, A2, A4, A5 and A6) comprising the Northern Cordillera, the Samaná Pensinsula and the Eastern Cordillera, the last of which includes Los Haitises. The dominant materials are limestones or coralline rocks, although on the Atlantic coast to the north of the Northern Cordillera, there are islands of serpentines (Puerto Plata and Gaspar Hernández). Although the value of the It/Itc is mitigated by the effects of the trade winds, the thermotype continues to be infra, thermo and mesotropical; the ombrotype in this case ranges between the subhumid in the basal areas and the hyperhumid in territories more exposed to the trade winds. The macrobioclimate is tropical Caribbean‐Mesoamerican Pluvial, and there are therefore no dry sites. The spiny forest occurs only in places with serpentines, as the territory acts as dry. The diversity of substrates, the bioclimate and the different dating of the areas accounts for the presence of 154 endemic species.
\nThis territory has a predominance of ombrophilous forest with a rainy character due to the intense influence of the trade winds. This produces a dominance of a broadleaf evergreen forest with well‐conserved formations of P. montana in Loma Diego de Ocampo, forests of M. abbottii to the northeast of the Northern Cordillera and, in somewhat less rainy areas, mahogany forests of S. mahagoni and C. diversifolia. In addition to the differences in flora and habitats with the rest of the territories, this biogeographical unit lacks the pine forests of P. occidentalis, typical of Bahoruco, Neiba and the Central province. In swampy freshwater areas, there are frequent coastal forests of Pterocarpus officinalis Jacq., and mangrove forests of L. racemosa, A. germinans and Rhyzophora mangle L., and to a lesser extent C. erectus. In all cases, the relation between the proposed biogeographical units has a Pearson’s index of equal to or less than 1, and in some situations, the value of r is very low—r = 0.73 for A2–A4 and r = 0.81 for A4–A6—indicating a high degree of similarity between the two units Figure 8.
\nVegetation catena of the Northern Cordillera. 1. Coconut cultivation. 2. Association Leptogono buchii‐Leptochloopsietum virgatae. 3. Broadleaf mahogany forest of Swietenia mahagoni. 4. Sierran palm forest of Prestoea montana.
BA‐A1. The Northern Cordillera district borders the Atlantic Coastal Plain to the north and the Cibao Valley to the south, and is the most recent mountain range on the whole island. There is a predominance of limestone, schists, and volcanic and metamorphic rocks; the thermotype ranges from infra to mesotropical and the ombrotype is subhumid to hyperhumid. From the floristic point of view, we found 39 endemic species in this unit, representing one of the lowest rates on the island: Coccotrinax boschiana M. Mejía & R. García, Eupatorium trichospermoides Alain, Gochnatia microcephala (Griseb.) Jervis & Alain var buchii (Urb.) Alain, Gonolobus domingensis Alain, Justicia spinosissima Alain, Sagraea abbottii (Urb.) Alain, Cytharexylum alainii Moldelke, Mecranium septentrionale Stean, Mikania platyloba Urb. & Ekm. and others. The dominant vegetation is the sierran palm forest of P. montana, C. racemiflora, D. tremulus, C. clusioides, Cyathea abbottii Mason, D. arboresus, T. occidentalis and O. capitatus. On somewhat less cloudy sites and therefore at lower altitudes, there are forests of M. abbottii, a species that is also found in the eastern areas of the Central Cordillera and in Sierra Prieta. This species of M. abbottii is accompanied by C. racemiflora, O. leucoxylon and S. berteriana. The epiphyte Vriesea ringens (Griseb.) Harms is widespread in these forests, while remnants of mahogany forests that have been highly altered by humans can be found in the drier areas at the foot of the mountain range. There are only small semi‐deciduous copses of S. mahagonii, C. diversifolia, Zanthoxylum martinicense (Lam.) DC., O. leucoxylon, Securidaca virgata Sw., Calophyllum calaba L., C. argenteum, C. oliviforme and G. guidonia. In this case, the vegetation catena corresponds to a semi‐deciduous mahogany forest, followed by a forest of M. abbottii and culminating in the more ombrophilous forest of P. montana.
\nBA‐A2. The Coastal‐Atlantic district is formed by small alluvial valleys of rivers with gentle gradients, with frequent marshes, isolated limestone and reef limestone. It is located to the north of the Northern Cordillera where there is a frequent presence of coconut, coffee and cocoa cultivation in addition to areas of cattle (‘potreros’ or pastures), so the natural vegetation is highly altered. However, there are 62 endemic species. The thermotype is infratropical and the ombrotype is subhumid and even humid, although the presence of serpentines in Puerto Plata and Gaspar Hernández causes soil xericity. We therefore include the spiny forest in the dry forest, characterised by the presence of specific plant communities such as Zombia antillarum (Desc. & Jacks.) Bailey and S. cubense, with a frequent presence in this type of forest of L. buchii, Ouratea ilicifolia (P.DC.) Bail., C. sidaefolius, Eugenia maleolens Pers. = (Eugenia foetida Poir.), Jacquinia umbellata DC., C. jimenezii, R. aculeata, M. buxifolia, C. biflora, Vitex heptafila A. L. Juss., M. toxiferum, L. virgata, Cordia lima (Desv.) R. & S., Tabebuia polyantha Urb. & Ekm., C. haematomma, Diospyros caribaea (A. DC.) Standl., E. crenulata, C. oliviforme, C. ferrugineum, Bromelia pinguim L., Byrsonima spicata (Cav.) HBK., Poitaea galegoides Vent., Coccoloba pubescens L., Eugenia odorata Berg and C. linearis. This is a tall serpentinicolous shrubland (copse) with 60–80% coverage, an average height of 3–4 m and abundant floristic diversity, located in Puerto Plata and Gaspar Hernández in infratropical subhumid‐humid areas. This endemic habitat in the Coastal‐Atlantic unit belongs to the association Zombio antillari‐Leptogonetum buchii [28]. In the rest of the territory, the potential forest consists of Swieteania mahagoni and C. diversifolia. An important feature in this area is the presence of the Gran Estero, developed in the last 400–500 years from deposits of materials from the Northern Cordillera. This area is subject to frequent flooding, and is home to a forest of P. officinalis belonging to the association Roystoneo hispaniolanae‐Pterocarpetum officinalis Cano, Veloz, Cano‐Ortiz & Esteban 2009. It represents the outer edge of the mangrove forests of R. mangle that are typical in the broad channels and in Samaná Bay [23].
\nBA‐A4. The Samaná Peninsula was isolated from the rest of the territory until 300–400 years ago. It constitutes a geomorphological unit dominated by karstic and limestone materials, with schists and marbles. The thermotype is infratropical and the ombrotype is subhumid‐humid. The presence of escarpments (cliffs) has led to the installation of edaphoxerophilous communities that must be considered as dry forest, owing to the predominance of P. polygonus, Z. debilis, A. antillarum, Eugenia samanensis Alain, B. simaruba, Capparis flexuosa L., Ficus velutina H. & B. ex Willd., E. maleolens, O. dilenii, Comocladia dodonaea (L.) Britt., Stigmaphyllom emarginatum (Cav.) A. L. Juss. and C. linearis. This area has over 60 species of flora Figure 9.
\nVegetation catena of the Samaná Peninsula. 1. Coconut cultivation. 3. Broadleaf forest. 2. Community of Coccothrinax gracilis and Bursera simaruba. As. Coccotrino gracili‐Burseretum simarubae [31]. 4. Cloud forest of Prestoea montana. 5. Forest of Pterocarpus officinalis. As. Roystoneo hispaniolanae‐Pterocarpetum officinalis.
BA‐A5. The Eastern Cordillera is the oldest range in this biogeographical territory, and has a frequent presence of limestone, karstic landscapes, tufas, alluvial deposits and foothills. It serves as a separation from the great eastern coastal plain, with sporadic intrusions of Palaeozoic slates and basalts. The thermotype ranges from infra to mesotropical; the macrobioclimate is rainy and the ombrotype is subhumid to hyperhumid. The subhumid forest with a semi‐deciduous character represents the transition between the dry and ombrophilous ombrotype, where there is a predominance of S. mahagoni, C. diversifolia and M. toxiferum. These formations are found primarily in the basal areas of the Eastern Cordillera, in points of contact with the Eastern Caribbean area. However, these areas are severely altered as they are used for the cultivation of cocoa, coconut and coffee, and there is a widespread presence of the cattle enclosures known as ‘potreros’. This is the reason for the low rate of endemic plants, with only eight species. Above an altitude of 600 m there is a broadleaf cloud forest with a frequent presence of D. morototoni, Inga fagifolia (L.) Willd., T. occidentalis, Cyathea arborea (L.) J. E. smith, G. guidonia, P. montana, S. virgate and B. plumeriana.
\nBA‐A6. The rainfall in Los Haitises exceeds 2000 mm, and it is home to a vegetation with a dominance of D. arboreus, G. guidonea, S. berteriana, P. montana and T. occidentalis. We propose these territories as specific biogeographical areas due to the vegetation of the ‘mogotes’ (steep sided residual hills) that are typical of this territory, the high rate of endemic species—with 49 endemic plants—and the resulting diversity of habitats. Its relation with A5 gives a value of r = 0.91 and r = 0.71 with A4 (Samaná) Figure 10.
\nVegetation catena of Los Haitises. 1. Coconut cultivation. 2. Broadleaf mahogany forest of Swietenia mahagoni. 3. Cloud forest of Prestoea montana and Didymopanax tremulus. 4. Broadleaf mahogany forest of Swietenia mahagoni. 5. Association Roystoneo hispaniolanae‐Pterocarpetum officinalis. 6. Association Machaerio lunati‐Rhizophoretum manglis.
The island of Hispaniola is characterised by its abrupt differences in altitude—from 0 to 3175 m on Pico Duarte in the Central Cordillera—[38], the wide diversity of substrates and a pluviometric gradient that ranges from 400 to 4600 mm [35]. These three parameters, in combination with the isolation to which the various territories have been subjected, are key factors in explaining the existence of the current vegetation. For the study of this vegetation, we have established several large areas based on rainfall and temperature—dry, subhumid, humid‐hyperhumid areas and high‐mountain zones—as highlighted in [22, 23]. The bioclimatic analysis reveals the presence of several macrobioclimates on Hispaniola: tropical xeric, tropical pluviseasonal and tropical pluvial; all of which are reflected in different vegetation units: dry forest, subhumid broadleaf forest, cloud forest and high‐mountain forest (pine forest) [35].
\nThe dry areas have a tropical xeric macrobioclimate with a high rate of endemic species. These zones correspond closely to the study areas A3, A9 and A12 [39]. The vegetation in all the semiarid and dry areas is physiognomically very similar; it is dominated essentially by plants from the families Agavaceae and Cactaceae among others: Lemaireocereus hystrix (Haw.) B.&R., Cylindropuntia caribae (B.&R,) Kunth, Consolea moniliformis (L.) Haw., Leptochloopsis virgata (Poir.) Griseb., Pilosocereus polygonus (Lam.) B.& R., Opuntia dillenii (Fer.‐ Gawl) Haw., Leptocereus weingartianus (Hartm.) Britt. & Rose, Acacia skleroxyla Tuss., Agave antillarum Descourt. and Pithecellobium unguis‐cati (L.) Mart. In the southwest of the island (A12), we establish two types of dry forest: first, the forest of Pedernales‐Ceitillan (Procurrente de Barahona), growing on dogtooth limestone substrates. We highlight as endemic species Melocactus pedernalensis (Ait.) M. Mejía & R. García, Galactia dictyophylla Urb., Coccoloba incrassata Urb., Caesalpinia domingensis Urb. and Guettarda stenophylla Urb. The dry forest in area A9 with an Io = 2.7 has a somewhat lower rate of endemics. The most notable endemics and those which mark the difference with the dry forest of Pedernales are Melocactus lemairei (Monv.) Miq. Neoabbottia paniculata (Lam.) Britt. & Rose and Coccotrinax spissa Bailey. In area A3, located in the northwest of the island, there is a dry forest differentiated from the previous forests by the presence of a floristic contingent of endemic species, including Salvia montecristina Urb. & Ekm., Mosiera urbaniana Borhidi, Croton poitaei Urb., Croton sidaefolius Lam., Guettarda tortuensis Urb. & Ekm. and Coccoloba buchii Urb. The most representative plant communities in the dry areas belong to the following endemic habitats: Lepotogono buchii‐Leptochloopsietum virgatae Cano et al. [24, 25], included in the serpentinicolous endemic alliance Tetramicro canaliculatae‐Leptochloopsion virgatae Cano, et al. [24, 25]; Crotono astrophori‐Leptochloopsietum virgatae Cano, et al. [24, 25], Melocacto pedenalensi‐Leptochloopsietum virgatae Cano, et al. [24, 25], Solano microphylli‐Leptochloopsietum virgatae Cano et al. [24, 25], included in the endemic alliance Crotono poitaei‐Leptochloopsion virgatae Cano et al. [24, 25]; the dry forests published in Ref. [29], and the pine forests on serpentines of Leptogono buchii‐Pinetum occidentalis Cano, Veloz & Cano‐Ortiz 2011, which we include in the endemic alliance Phyllario mummularioidi‐Leptogonion buchi Cano, Veloz, & Cano‐Ortiz 2011.
\nMost of Hispaniola has a pluviseasonal tropical macrobioclimate and a predominantly subhumid ombrotype, with rainfall ranging from 1000 to 2000 mm and an ombrothermic index of Io = 3.7–4.3 (Parque Nacional del Este); Io = 4 (El Seibo); Io = 6.2 (Miches); Io = 5.4 (Jarabacoa) and Io = 5.9 (Mayaguana) (A7). The dominant vegetation in these areas is a subhumid broadleaf forest subjected to a dry season from December to April, which is why the floristic composition includes deciduous tree species due to water stress, such as Bursera simaruba (L.) Sarg. and Swietenia mahagoni (L.) Jacq., along with other species such as Metopium toxiferum (L.) Krug & Urb., Krugidendron ferreum (Vahl) Urb., Acacia macracantha H. & B. ex Willd., Coccoloba diversifolia Jacq. and Bucida buceras L. These formations contain important endemic elements such as the climber Aristolochia bilobata L. and the tree element Melicoccus jimenezii (Alain) Acev. Rodr., in addition to scrubland plants such as Lonchocarpus neurophyllus Benth., along with the other scrubland formations that become dominant and act as dynamic substitution stages. This is the case of Zamia debilis L., which coexists with the endemic species Pereskia quisqueyana Alain and G. ekmanii O.E. Schulz.
\nWhen these subhumid forests are located on perforated reef limestone, the territory acts as dry owing to the intense water losses from the soil, and present the floristic elements P. polygonus, P. unguis‐cati, L. weingartianus and Hylocereus undatus (Haw.) Britt. & Rose. These formations connect with the dry forest in the southwest of the island. A similar phenomenon occurs in the rocky escarpments of Samaná, where there is a widespread frequent presence of B. simaruba, Coccothrinax gracilis Burret, A. antillarum, L. weingartianum and O. dilleni. These habitats tend to contain deciduous species due to water stress and correspond to the associations recently proposed by us [30]: Chrysophyllo oliviformi‐Sideroxyletum salicifolii Cano & Veloz 2012 and Zamio debilis‐Metopietum toxiferi Cano & Veloz 2012. In dry and subhumid areas, the serpenticolous vegetation is of great interest for conservation [28].
\nHumid areas have a tropical pluvial macrobioclimate, and there is therefore no dry season. Rainfall exceeds 2000 mm. These humid areas tend to be located in the mountain ranges of the Northern Cordillera, Central Cordillera, Sierra de Bahoruco, Eastern Cordillera, Los Haitises and on the Samaná Peninsula, all of which concentrate the humid rainy formations, namely broadleaf ombrophilous forests whose physiognomy varies from one place to another. In the Loma La Herradura (Eastern Cordillera), the dominant plants are Sloanea berteriana Choisy, Ormosia krugii Urb., Didymopanax morototoni (Aubl.) Dcne. & Planch. and Oreopanax capitatus (Jacq.) Dcne. & Planch. Towards the stream beds, there is a presence of the sierran palm forest of P. montana (Grah.) Nichol, whose associated flora are Guarea guidonia (L.) Sleumer, D. morototoni, Alchornea latifolia Sw. and Eugenia domingensis Berg [11].
\nIn the Central Cordillera (A16), for example, in the Ébano Verde Science Reserve, the ombrophilous forest is dominated by species from the genus Magnolia, which are endemic to the island: Magnolia pallescens Urb. & Ekm. and Magnolia domingensis Urb., along with the ‘palo de viento’ Didymopanax tremulus Krug & Urb., Ocotea leucoxylon (Sw.) Lanessan, Persea oblongifolia Kopp, Cyrilla racemiflora L., Cecropia schreberiana Miq. and Dendropanax arboreus (L.) Decne. & Planch. This forest is home to the endemic species Myrsine nubicola A. Liogier, Odontadenia polyneura (Urb.) Woods, Marcgravia rubra A. Liogier, Pinguicula casabitoana J. Jiménez and Tabebuia vinosa A. Gentry. As in the Loma La Herradura, the sierran palm forest of P. montana can be found in the most humid gorges. When these plant communities become altered and their coverage decreases, they are quickly superseded by tropical fern or herb formations of Dicranopteris pectinata (Willd.) Underw. and Gleichenia bifida (Willd.) Spreng. [9].
\nIn the Loma Humeadora, the cloud forest of ‘palo de viento’ D. tremulus grows at an altitude of 1100–1315 m, and this species is associated with Clusia clusioides (Griseb.) D’Arcy, C. racemiflora, Ocotea foeniculacea Mez, Lyonia alainii W. Judd and P. montana. Descending to 850–1100 m on slopes with a gradient of 45–60° but with abundant litterfall that effectively retains water, and in gorges, P. montana becomes dominant associated with A. latifolia, O. leucoxylon, Bombacopsis emarginata (A. Rich.) A. Robins., S. berteroana, Mora abbottii Rose & Leon., Turpinia occidentalis (Vent.) G. Don, Bactris plumeriana Mart. and Ditta maestrensis Borhidi [8].
\nIn the relevés taken both in the Central Cordillera and in Sierra Bahoruco, in addition to the existence of different substrates, the broadleaf forest shows clear floristic differences, with M. pallescens and M. domingensis in the Central Cordillera and Magnolia hamorii Howard in the Sierra de Bahoruco. The forest of M. hamorii and D. tremulus has a large number of associated endemic species such as Lasianthus bahorucanus Zanoni, Psychotria guadalupensis (DC.) Howard, H. domingensis Urb. Mecranium ovatum Cog. (local endemic), Vriesea tuercheimii (Mez.) L.B. Smith, Macrocarpaea domingensis Urb. Cestrum daphnoides Griseb. Hypolepis hispaniolica Maxon, Columnea domingensis (Urb.) Wiehler and Ilex tuerckheimii Loes. This vegetation was included in Ref. [22] in the classes Ocoteo‐Magnolietea Borhidi & Muñiz in Borhidi, Muñiz & Del Risco 1979 and in Weinmannio‐Cyrilletea Knapp 1964.
\nThe study of high‐mountain areas took place in the Central Cordillera (A16), crossing the mountain from Constanza to San José de Ocoa, and in the Sierra de Bahoruco (A12). From the physiognomic point of view, the plant formations sampled between 1203 m (Sierra Bahoruco) and 2383 m (Central Cordillera) are similar, corresponding to a pine forest of Pinus occidentalis Sw. These are territories with lower rainfall, as the sea of clouds from the trade winds originating the broadleaf forest lies beneath. The temperature may drop to 0°C in winter. The xericity and the low temperatures in the high mountains result in the presence of a pine forest of P. occidentalis, which in the Central Cordillera is accompanied by endemic species, with 8–10 endemic plants per sampling unit. This is also the case in the Sierra de Bahoruco, where the pine forest has an average of 20 endemic species per sampling. The endemic character of these two mountains is caused by their former isolation.
\nIn the Central Cordillera, these forests grow on siliceous substrates and are home to a large number of endemic species such as I. tuerckheimii, Ilex fuertesiana (Loes.) Loes. Garrya fadyenii Hooker, Mikania barahonensis Urb., Myrica picardae Krug & Urb., Rubus eggersii Rydberb., Tetrazygia urbaniana (Cogn. in Urb.) Croizat ex Moscoso and Fuchsia pringsheimii Urb.; the endemic and specific parasitic species P. occidentalis, Dendropemon pycnophyllus Krug & Urb. and Dendropemon constantiae Krug & Urb. are of particular importance. In the understorey of this forest, there is a high frequency of the grass Isachne rigidifolia (Poir.) Urb., and when the pine forest is cleared, it is substituted by a formation of single‐culm grasses dominated by D. domingensis Hack. & Pilg., which occupies large extensions above 1800 m in the Central Cordillera.
\nThe pine forest of P. occidentalis growing on limestone in the Sierra de Bahoruco has a different floristic composition, in which the endemic species Coccothrinax scoparia Becc., Agave intermixta Trel., Senecio barahonensis Urb., Cestrum brevifolium Urb., Eupatorium gabbii Urb., Lyonia truncatula Urb., Sideroxylon repens (Urb. & Ekm.) TD. Pennington, Cordia selleana Urb., Narvalina domingensis Cass. and Galactia rudolphiodes (Griseb.) Benth. & Hook. var. haitiensis Urb. are of particular interest, along with some other endemic herbs such as Pilea spathulifolia Groult, Tetramicra ekmanii Mansf., Artemisia domingensis Urb., Gnaphalium eggersii Urban and Polygala crucianelloides DC. High‐mountain pine forests that have been diagnosed by us as endemic habitats of Hispaniola [26] are Dendropemom phycnophylli‐Pinetum occidentalis Cano, Veloz & Cano‐Ortiz 2011 and Cocotrino scopari‐Pinetum occidentalis Cano, Veloz & Cano‐Ortiz 2011.
\nThe study of the 19 areas in Hispaniola shows a wide distribution of endemic species, but with three nuclei of particular interest due to their high rate of endemic plants, as highlighted by the comparative treatment between the total number of endemic species present in an area and the endemic species that are exclusive to this area. There are a total of 2094 endemic species in the 19 areas, of which 1162 are exclusive. The difference between 2094 − 1162 = 932, confirming the high number of endemic species distributed all over the island. The highest concentrations are found in areas A12, A16, A13 (Table 1), whereas the rest of the areas have a lower number of endemic species, with a slight increase in areas A4 and A9. These areas continue to be of interest as they contain endemic species that are exclusive to the territory, and even endemic genera, as occurs in A18 and A19 (Figure 11).
\nRatio of total endemic species in each area to endemic species exclusive to that area.
Plots | \nA1 | \nA2 | \nA3 | \nA4 | \nA5 | \nA6 | \nA7 | \nA8 | \nA9 | \nA10 | \nA11 | \nA12 | \nA13 | \nA14 | \nA15 | \nA16 | \nA17 | \nA18 | \nA19 | \n
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
1 | \n20 | \n15 | \n24 | \n36 | \n1 | \n12 | \n23 | \n2 | \n26 | \n1 | \n27 | \n482 | \n129 | \n11 | \n28 | \n278 | \n29 | \n8 | \n10 | \n
2 | \n40 | \n61 | \n68 | \n127 | \n9 | \n45 | \n64 | \n7 | \n87 | \n9 | \n72 | \n699 | \n173 | \n29 | \n64 | \n440 | \n65 | \n20 | \n15 | \n
Comparative analysis of the total endemic species in each area with the number of endemic species exclusive to that area.
1. No. of exclusive endemic taxa by area. 2. Total number of endemic taxa by area
Hispaniola has recently been elevated by us to the rank of biogeographical province [2, 22, 24], having previously been treated with the rank of biogeographical sector [4] and included in the province of the Antilles. In previous studies, we raised it to the rank of superprovince of the Central‐Eastern Antilles and included Hispaniola in it, which along with a group of small neighbouring islands—Beata, Saona, Gonave and Tortuga—constitute the province of Hispaniola. In the current study, we propose a biogeographical typology with the rank of district for both countries (Dominican Republic and Republic of Haiti) in the biogeographical province of Hispaniola, in which we establish five biogeographical territories (sectors) and 19 areas (districts), in the Caribbean‐Mesoamerican region. This proposal is based on geological, climatic and bioclimatic aspects and on studies of the flora and vegetation.
\nThe high number of genera and endemic species in areas A12, A13 and A16 justifies their proposed designation as being of special interest for conservation.
\nSuperprovince of the Central‐Eastern Antilles. Province of Hispaniola. 1. Central subprovince. 1.1. Central BT. BA‐A16. Central‐Eastern. 2. Caribbean‐Atlantic subprovince. 2.1. Bahoruco‐Hottense BT. BA‐A12. Bahoruco‐La Selle. BA‐A13. Hottense. 2.2. Neiba‐Matheux‐North‐eastern BT. BA‐A14. Neiba‐Matheux. BA‐A15. North‐western. BA‐A17. Central‐Western. BA‐A19.Tortuga Island. 2.3. BT Azua‐ San Juán‐Hoya Enriquillo‐Port au Prince‐Artiobonite‐Gonaivës. BA‐A9. Azua‐Sán Juán‐Hoya Herniquillo. BA‐A10. Central Plain. BA‐A11. Port au Prince‐Arbiobonite‐Gonaives. BA‐A18. Gonave Island. 2.4. Caribbean‐Cibense BT. BA‐A3. Cibao Valley. BA‐A7. Eastern Caribbean. BA‐A8. Yamasense. 2.5. Northern BT. BA‐A1. Northern Cordillera. BA‐A2. Coastal Atlantic. BA‐A4. Samanense. BA‐A5. Eastern. BA‐A6.Haitiense Figure 12.
\nMap of biogeographical areas (districts) of Hispaniola. A1. Northern Cordillera. A2. Coastal‐Atlantic District. A3. Cibao Valley. A4. Samanense. A5. Eastern. A6. Haitiense. A7. Eastern‐Caribbean. A8. Yamasense. A9. Azua‐Sán Juan‐Lago Herniquillo. A10. Central Plain (Haiti). A11. Port au Prince‐Ariobonite‐Gonaivës. A12. Bahoruco‐La Selle. A13. Hottense. A14. Neiba‐Matheux. A15. Northwest Haiti. A16. Central‐Eastern. A17. Central‐western (Massif du Nord). A18. Gonave Island. A19 Tortuga Island.
Our most sincere thanks go to the architect Francisco Javier Quiros Higueras for designing the profiles and maps.
\nNanotechnology consists on the development of materials with dimensions usually between 1 and 100 nm, where the properties of matter are significantly different than their bulk counterparts, and can be tuned to the desired application. These novel chemical and physical properties are usually derived from quantum effects and from the drastically increased surface-to-volume ratio. Furthermore, since many biological structures, i.e. proteins, organelles, viruses, etc., can be found within the nanometric scale, synthetic nanostructures have easy access to biological systems.
Although Nanotechnology started purely as a physical and materials science, soon the medical properties of nanomaterials became evident, and the new era of nanomedicine and nanopharmacy started. Nanomaterials are now recognized as excellent therapeutic and diagnostic tools, and thousands of novel compounds and nanostructures are developed every year, for the most diverse applications.
As you will see in this chapter, Nanotechnology can help practitioners to overcome several hindrances of photodynamic therapy that have so far prevented this approach from reaching a broader clinical success. Over the last decade, nanostructures have been applied as drug delivery platforms for PDT, and as strategies to enhance the efficiency of photosensitizers in generating ROS upon irradiation. The nanoparticles can be organic or inorganic, can assume a multitude of shapes and sizes within the nanoscale, can act as photosensitizers themselves or as energy transducers. Even further, nanocarriers prevent the complications that arise from the poor solubility of photosensitizers in aqueous media, and increase the tumor accumulation in order to preserve healthy tissues. We are going to discuss in details the most relevant data regarding the enhancement of PDT by the use of nanomaterials.
There is a plethora of photosensitizing compounds available, but the majority of them did not present the requirements for clinical trials, i.e. good solubility, target selectivity, sufficient light absorption on the desired wavelength, and low accumulation in distant sites, especially the skin [1]. One of the biggest hindrances of photosensitizers is their hydrophobicity and consequent tendency to aggregate in aqueous environments, making the intravenous administration difficult unless some kind of delivery system is used [2, 3]. Besides, it is desirable that the photosensitizers accumulate preferentially in the target tissue rather than in healthy sites in order to avoid toxicity, therefore strategies of targeted delivery are often necessary to increase the therapeutic efficiency, and nanoparticle systems offer great advantages in this regard [1].
Besides the tendency to aggregate when photosensitizers are injected intravenously, they tend to be distributed to the whole body in a non-specific way, and to be taken up by plasma proteins or phagocytes, decreasing significantly the efficiency of PDT. To increase the specific delivery and avoid side effects, several carriers have been developed to take advantage of the enhanced permeation and retention (EPR) effect or to actively target tumors and enhance specific accumulation, such as polymer and metal nanoparticles, micelles and liposomes, and magnetic nanoparticles. The EPR effect is caused by the leaky vasculature common to tumor tissues, due to the sinusoid capillaries and the fenestrated endothelial cells, plus the inefficient lymphatic drainage from tumor sites. The active targeting, on the other hand, is actually a plethora of strategies to increase specific tumor accumulation of a drug or therapeutic compound [3].
Another obstacle for photodynamic therapy is the limited penetration of light, so it is used mostly for superficial tumors, or with the help of optic fibers introduced in the patient. Recently, researchers have been developing strategies to produce light inside of the body with the help of nanoparticle scintillators. These materials are able to convert external X-ray photons, which can reach deeper sites in the organism, into visible light photons that could excite a photosensitizer in a process called X-PDT. Another approach to excite photosensitizers with endogenous light is with Cherenkov radiation in a process referred as CR-PDT. Cherenkov radiation is generated when a particle exceeds the speed of light in a defined medium, and is common with the decay of several medical radioactive isotopes [4].
Photosensitizers that absorb in the NIR region, such as indocyanine green (absorption around 800 nm) and aluminum sulfophthalocyanine (absorption around 790 nm), although being able to be used in deeper regions due to the deeper penetration of NIR light, tend to be less efficient in generating singlet oxygen than other photosensitizers that absorb in lower wavelengths. Upconversion nanoparticles (UCNs) can overcome these limitations. The process where the absorption of multiple photons – usually two or three – from a given wavelength leads to the emission of photons from a shorter wavelength is referred as photon upconversion. This can be used as a strategy to reach deeper tissues with longer wavelengths and excite photosensitizers that absorb in shorter wavelengths and would not be reachable by light otherwise [5].
UCNs usually consist in inorganic luminescent materials, usually made with lanthanide elements that absorb NIR light and emit UV-visible light that can be used to excite more efficient photosensitizers. Other than the possibility of exciting photosensitizers in deeper regions and prevent photobleaching, enhancing PDT efficacy, they can carry a plethora of hydrophobic photosensitizers, either loaded physically or chemically [6, 7].
Nanostructured delivery systems for photosensitizers can provide some major advantages in PDT. The first one is regarding the increased quantity of dyes that can be delivered to the target cell due to the large surface-to-volume ratio, while the second one refers to the prevention of the premature release of the dyes before reaching the target, enhancing the specific accumulation in the target tissue and diminishing the side effects. The third is somehow related to the second, since the loaded dyes find few obstacles in the blood stream and acquire an amphiphilic character once conjugated with nanostructures, enhancing the tumor accumulation as well. Another advantage is the privileged accumulation of nanosized materials in tumor tissues due to the enhanced permeability and retention (EPR) effect. Finally, their surface can be functionalized with a plethora of groups, so that their biodistribution, pharmacokinetics, cell uptake and surface chemistry can be tuned according to the desired application [8]. Figure 1 summarizes the main advantages of nanotechnology combined with PDT.
The combination of nanoparticles with photosensitizers and its main advantages for tumor ablation.
Both biodegradable and non-biodegradable nanoparticles can be used to potentiate photodynamic therapy (PDT). In the case of biodegradable nanoparticles (generally polymers and lipid-based structures), the photosensitizers are trapped inside them and are released in a controlled manner, so that singlet oxygen can be generated due to the exposition to light. On the other hand, when non-biodegradable nanoparticles are used, usually the photosensitizers are adsorbed on their surface (either external or internal, in case of porous structures), and they do not need to be released completely to generate singlet oxygen [1].
Regarding biodegradable nanoparticles, many photosensitizers have been encapsulated with water-soluble polymers, such as meso-tetra(hydroxyphenyl) porphyrin, bacteriochlorophyll, verteporfin, various phthalocyanines, methylene blue, and hypericin. Their singlet oxygen efficiency depends much on the polymer. Poly lactic glycolic acid (PLGA), for instance, has demonstrated good results compared to other polymers, along with poly lactic acid (PLA) and poly ethylene glycol (PEG). The pharmacodynamics of different polymer nanoparticles may differ from one another, and so do their bioavailability, thus the PDT efficiency may be different according to the nature of the polymer [1].
Non-biodegradable nanoparticles are mostly metallic or ceramic-based (especially silica), but polyacrylamide was also reported as a photosensitizer nanocarrier. Nevertheless, solid silica nanoparticles present higher singlet oxygen yield than polyacrylamide nanoparticles, i.e. 2 to 3-fold more singlet oxygen production by silica nanoparticles loaded with methylene blue compared to their polyacrylamide counterparts [1].
Plasmonic materials, a very important class of non-biodegradable nanomaterials, have proven to act as photosensitizers in the right conditions, and if they have photosensitizers attached to their surface, they can enhance the photodynamic efficiency of the dye. It was observed that semiconductor nanoparticles that present the suitable energy gap can be used as photosensitizers and can also be conjugated with other organic dyes. In these conjugated materials, energy can be transferred from the excited nanoparticles to the photosensitizers through a FRET mechanism [5].
Gold and silver nanoparticles are more stable and present higher extinction coefficients than organic dyes, but if one desires to use them to generate singlet oxygen, O2 molecules must be adsorbed on their surface in order to provide a rapid energy transfer between the two. Furthermore, the energy transfer from the nanoparticles to the adsorbed oxygen molecules is more efficient in low-energy surface states of metal nanoparticles rather than the high-energy states. When these conditions are fulfilled, it is believed that the PDT antitumor efficiency can be up to 10 times that of chemotherapeutics like doxorubicin [5].
Gold nanorods have been developed by different authors in order to carry phthalocyanines via adsorption onto the nanoparticle surface, either chemically with a thiol group or via electrostatic interaction. The formation of a phthalocyanine layer covering the nanoparticle prevents the aggregation of the hydrophobic photosensitizer and enhances the photodynamic activity [2, 9].
Camerin and collaborators compared the efficacy of a phthalocyanine in its free form and conjugated with gold nanoparticles in ablating B78H1 amelanotic melanoma tumors in mice. The results showed that the accumulation of photosensitizer in the tumor is enhanced when they are bound to the nanoparticles, and as a consequence, the damage was significantly more intense and the tumor growth was significantly slower than the tumors treated with the free phthalocyanines [2].
Several cases of enhancement of the photosensitizer efficiency by plasmonic nanoparticles (due to a strong energy transfer and the prevention of photobleaching) have been reported in the literature, with various photosensitizers and nanoparticle morphologies and materials [9, 10, 11, 12, 13]. One interesting example was demonstrated by [14], because the PDT efficiency of the photosensitizer conjugated with gold nanoparticles was comparable to the free photosensitizer, but the hyperthermal effect contributed to a more intense cytotoxicity against the tumor cells.
The material and the morphology of the plasmonic nanoparticles influence on the extinction coefficients and, consequently, on the energy transfer efficiency. Gold nanourchins, for instance, present an intense extinction coefficient at 940 nm, which is within the therapeutic window, and the singlet oxygen production was intense and sufficed to eliminate cancer HeLa cells while preserving normal NIH-3 T3 fibroblasts. Gold bipyramids can be efficient singlet oxygen generators if the wavelength used overlaps with the surface plasmon resonance peak, even more efficient than methylene blue. Silver and gold nanocubes are unable to generate singlet oxygen, while in the form of nanoprisms the opposite occurs [5].
This dependence on the morphology can be explained by theoretical calculations showing that O2 can be adsorbed on Au(111), Ag(111), Au(110), Ag(110), Au(100), and Ag(100) surfaces, but on Au(111), Au(100), and Ag(111) surfaces oxygen can remain in molecular form and be excited to its singlet state, whereas on the other surfaces it dissociates into its atomic form. This can only be altered when some defects are present in the crystalline structure [5].
Quantum dots are other promising materials for photodynamic therapy. Graphene quantum dots, for example, reduced tumor cell viability to 20% in a 1.8 μM concentration, compared to 35% cell viability when the same concentration of PpIX was used. Similar results were obtained for ZnO quantum dots irradiated with blue light [5].
Silica is also widely used as a nanomaterial because it is non-toxic and optically transparent, and their surface chemical functionalization is easily achieved due to the presence of several hydroxyl groups on its surface. When it comes to PDT, silica can act as a carrier of photosensitizers, protecting them from enzymatic degradation and enhancing their permeation in tumors [5]. Figure 2 shows some of the most important nanomaterials used in combination with PDT.
Some of the various morphologies and types of nanoparticles used in combination with PDT.
X-ray driven PDT makes use of scintillating materials and/or radiosensitizers (Figure 3). High-Z elements, for instance, have inner shell electrons which are very efficient in capturing X-ray photons and converting them into relaxed electrons and visible light photons. Thus, the most common scintillators are nanoparticles of high-Z elements doped with rare earth elements, and present useful properties for medical imaging and high-energy physics. The materials can be designed as films, coordination compounds, vitroceramics, metal-organic frameworks (MOFs), and hybrid organic-inorganic materials, and characteristics such as nanometric size, defects, coatings and media interaction influence on their scintillation properties [4].
Deeper penetration of X-rays and it use for X-PDT. The red circles symbolize singlet oxygen generated by the interaction of the excited photosensitizer and molecular oxygen.
Nanoscintillators can be basically divided in doped and semi-conductors scintillators. Lantanides are the most explored as doped scintillators due to their high density, high-Z, and significant intensity of luminescence, while semiconductor scintillators are mostly composed of porous Si, Si nanocrystals, ZnO, CdSe, CdS, PbS, and CuBr [4].
The efficiency of X-PDT is largely affected by the intensity of X-Ray luminescence, the singlet oxygen yield of the photosensitizer, and the way the photosensitizer is bound to the nanomaterial (either by covalent bonding, electrostatic interactions, or by pore loading). Furthermore, part of the tumor ablation might be due to the generation of UV photons during the scintillation process, apart from the photodynamic effect. The radiosensitization effect must also be considered, since high-Z materials generate ROS whenever their electrons are excited by X-rays into states above the conduction band edge, consequently producing electron hole pairs that interact with water producing hydroxyl radicals, and the electrons generate superoxide and peroxide radicals when they react with O2. Those ROS increase the cytotoxicity of the materials under X-ray irradiation [4].
Nanoscale metal-organic frameworks (nMOFs) consist of the self-assembly of metal ions or clusters and bridging ligands, usually organic polydentate. These materials are used as a means to put scintillators and photosensitizers closer to each other, enhancing the singlet oxygen generation efficiency [4].
Nanosized MOFs are usually biodegradable, offering a significant advantage over other nanomaterials, depending on the desired application. They encompass a virtually infinite possibility of structures due to the large availability amount of organic linkers and metallic parts; however, it is of utmost importance to select the components in accordance with the desired application in order to optimize the results. In the medical field, the use of MOFs is still in the prelude, since more pharmacokinetic, pharmacodynamics and biological characterization studies must be performed so that these materials reach clinical trials [15].
Regarding the use of lanthanides as scintillators, Dou et al. synthesized UCNs (NaYF4:Yb,Tm) covalently conjugated with chlorin e6 to prevent the premature release of the photosensitizer and tested them in vitro. The nanoparticles were more efficient than the free photosensitizer even at low concentrations, and the efficacy can be fine-tuned by adjusting the dose of Ce6-UCNs and the laser power [7]. On the other hand, non-lanthanide materials such as SiC/SiOx core/shell nanowires functionalized with azide groups and porphyrin derivatives were tested for X-PDT and demonstrated significant efficacy. This material showed to be non-cytotoxic in the dark, and emits fluorescence at 545 nm when irradiated with X-rays, exciting the porphyrin derivative in the process [4].
Another example of experimental X-PDT was performed by Sivasubramanian et al. using BaFBr:Eu2+ nanoparticles loaded with porphyrins. When irradiated with 3 Gy of X-rays, the nanoparticles generated luminescence that matched the excitation wavelengths of the photosensitizer, leading to photodynamic effect that damaged the DNA, the mitochondria, and generated intense oxidative stress, significantly killing prostate cancer cells in vitro [16].
One of the main concerns about X-PDT is the radiation dose that needs to be applied to the patients. In order to diminish the amount of radiation that the patient must be exposed to, some scintillators that present persistent luminescence upon irradiation, rather than fluorescence, are the option. Fluorescence is a phenomenon that lasts for a few nanoseconds, while persistent luminescence can persist for minutes to hours after the excitation, therefore the required dose of radiation for excitation can be significantly decreased. There are evidences that persistent luminescence decreases the rate of oxygen consumption during PDT and may avoid the undesired hypoxia that hinders the photodynamic efficacy [4].
Cherenkov radiation-driven PDT, symbolized in Figure 4, takes advantage of the fact that most radiopharmaceuticals accumulate in tumors in a selective manner, therefore the photodynamic ablation may occur in a more localized way. However, the generation of Cherenkov radiation occurs in low fluence rates, usually not enough to enable a good photodynamic efficiency [4].
Cherenkov radiation being generated after radionuclide decay, and its ability to excite photosensitizers in order to perform PDT. The red circles symbolize singlet oxygen.
There is a significant advantage, though, of CR-PDT over X-PDT, which is the possibility of targeting multiple metastases easier than with external X-rays. Furthermore, even if the photons generated by the radionuclides are in much lower number than external irradiation (and possibly insufficient to exert significant phototoxicity), it is likely that the damage induced directly by the radionuclides contribute synergistically for the success of tumor ablation with CR-PDT [17].
An example of experimental CR-PDT was performed by Kamkaew et al. The authors encapsulated the radionuclide 89Zr with chlorin e6 into a mesoporous silica nanoparticle. The zirconium Cherenkov radiation emission is mostly in the UV region, but there is a significant emission in the blue region around 400 nm, corresponding to one of the absorption peaks of chlorin e6. The results in vitro showed high levels of DNA damage when the photosensitizer is present compared to the radionuclide alone, while in vivo results showed complete tumor remission after 14 days, even with a sublethal radiation dose of 15 MBq. However, a significant amount of radioactive nanoparticles were found in the liver after 14 days, so strategies to avoid toxicity to health tissues must be applied [18].
Nevertheless, much progress is yet to be made before X-PDT and CR-PDT become official clinic protocols, despite all the successful results that have been obtained so far. The mechanisms of cell death by the combination of radiotherapy and PDT must be fully understood, and the materials used as scintillators must be fully characterized and optimized [4].
PDT efficacy in tumors is limited by the oxygen supply to the tumors, which tends to be reduced due to deteriorated microcirculation, especially in the tumor center. Since PDT consumes oxygen, it increases even further the local hypoxia, preventing the technique to reach its full potential. Therefore, some strategies to increase the availability of oxygen to the tumors while PDT is occurring have been developed in order to increase the tumor ablation [3]. Cheng and co-workers, for instance, loaded photosensitizers that are activated at 780 nm into perfluorocarbon nanodroplets enriched with oxygen with average size of 200 nm. The use of the nanodroplets also increases the half-life of singlet oxygen, so the PDT efficiency is enhanced both in vitro and in vivo. With intravenous administration, the tumors were significantly ablated, but with intratumor administration the tumors were eliminated completely [19].
It was observed by Kim et al. that O2 can be efficiently produced via Fenton reaction in cancer tissues due to the abundancy of H2O2 derived from the tumor metabolism, especially when mesoporous silica nanoparticles are conjugated to manganese ferrite nanoparticles, which are classical Fenton catalysts, and loaded with chlorin e6. This system enabled a continuous PDT process by providing the tissue with the necessary amount of O2 via Fenton reaction, and could act as a contrast agent for magnetic resonance imaging, acting as a theranostic material [20].
In this regard, cerium oxide nanoparticles provide a good alternative for converting hydrogen peroxide into molecular oxygen and water, even in the absence of light irradiation. They are, therefore, a smart strategy to provide the hypoxic tissues with oxygen to enhance PDT efficacy, as demonstrated by Jia et al. The authors used a mesoporous core-shell structure consisting of NaGdF4:Yb,Tm@NaGdF4 upconversion nanoparticles coated with CeOx capable of converting NIR light into UV light, which activates cerium oxide to produce ROS. Since the nanoparticles have a hollow interior, they can also be used as a drug carrier for a combined chemotherapy, besides being very efficient in tumor ablation by PDT [21].
Although most of the oxygen-generating strategies make use of the excess of hydrogen peroxide caused by the intense metabolism of tumors, which can react with iron cations generating O2 and hydroxyl radicals. There is a class of materials, however, that uses water as the source of oxygen, the so-called water-splitting materials, commonly used for solving energy and environmental problems. Since water is the major component of the organism, there is a virtually endless supply of oxygen to be used for PDT enhancement. Metal-free C3N4 decorated with carbon dots (in order to enhance the water-splitting upon irradiation with red light) was used by Zheng et al. as a water-splitting material. The nanocomposite was conjugated with the compound PpIx-PEG-RGD, consisting of the photosensitizer protoporphyrin IX with polyethylene glycol and the peptide sequence RGD (arginine, glycine, and asparagine) for active tumor targeting and photodynamic therapy. Under 630 nm irradiation, there was an increased O2 concentration and singlet oxygen production, enabling a significant cell killing without the occurrence of hypoxia [22].
Red blood cells (RBCs) can be used as photosensitizer and oxygen carriers at the same time in order to increase the efficacy of PDT in hypoxic situations. Wang et al., for example, coupled the photosensitizer Rose Bengal and a hypoxic probe on the surface of RBCs. Upon low levels of oxygen, the hypoxic probe can switch to an active state and undergo an orthogonal near-infrared upconversion, resulting in the release of O2 from the oxygenated hemoglobin when 980 nm light is applied. The photodynamic process is, thus, kept for longer and results in a better tumor ablation [3].
Oh the opposite side of the previous strategies, a protocol has been developed in order not to avoid the hypoxia in the tumors, but to use it to potentiate chemotherapy after PDT has been performed. This is possible with the use of hypoxia-activated prodrugs such as triapazamine or apaziquone. He and collaborators used nanoscale metal-organic frameworks (NMOFs) as porous nanocarriers of photosensitizers and hypoxia-activated chemotherapeutics. Both in vitro and in vivo results indicate an on-demand release behavior of the nanoparticles and an intense tumor ablation, therefore it consists on a promising antitumor strategy [23].
One of the most common strategies of actively targeting specific organs or tissues is by the use of antibodies. Stuchinskaya and collaborators combined the versatility of gold nanoparticles with a hydrophobic photosensitizer (zinc phthalocyanine derivative), preventing its aggregation before reaching the target, and decorated the nanoparticle with tumor-specific antibodies (anti-HER2 for breast cancer) by covalent bonds formed with the coating layer of polyethylene glycol. There was a high efficiency in singlet oxygen generation in cancer cells after a selective targeting [24].
Active targeting can also make use of membrane proteins that are overexpressed in tumor cells, i.e. some integrins and neuropilin-1. By coupling ligands like RGD (a tripeptide composed of arginine, glycine, and aspartate), biotin, and folic acid to nanocarriers, the tumor accumulation is significantly enhanced [3]. Organelle targeting is also an option, especially when it comes to mitochondria. Several lines of evidence show that targeting the mitochondria for PDT avoids drug-resistance by tumor cells via a decreased level of intracellular ATP (the drug resistance phenotype in tumor cells is often associated with overexpressed ATP-driven transmembrane efflux pumps), besides the fact that damage to the mitochondria often leads to cell death [25]. Targeting the lysosomes can be additionally useful because the leakage of protons and hydrolases into the cytoplasm can damage inner structures and lead to cell death [3].
Another reason that makes organelle-targeting important is the short action range of singlet oxygen (no more than 20 nm), so a localized photosensitizer excitation is required. Hou et al. developed a Fe3O4@Dex-TPP nanoparticles that enhance the oxygen concentration in tumor cells via Fenton reaction, target the mitochondria (via the triphenylphosphine group, TPP), and are able to be imaged by magnetic resonance imaging due to the magnetic behavior of Fe3O4. This system was loaded with the photosensitizer protoporphyrin IX and grafted with a reduced glutathione-responsive moiety. Upon internalization, Fe2+ and Fe3+ ions are liberated from the Fe3O4 core and diffuse into the cytoplasm, then oxygen is produced by Fenton reaction (Fe2+ reacting with the excess of H2O2 producing O2 and hydroxyl radical (•OH). This allows the PDT process to keep occurring, enhancing the therapeutic efficacy [25].
One of the strategies for specific delivery is the development of pH-sensitive materials that make use of the mild acidity environment found in tumors (around 6.5 to 7.2). Ai and co-workers developed upconversion nanoparticles with a low-pH insertion peptide that in acidic environments allow the insertion of the nanoparticles into the plasma membrane. They observed a large accumulation in the tumor tissue compared to healthy tissues [26].
Calcium phosphate is a biocompatible and biodegradable material, as it is the main component of hard tissues such as bones and teeth. It is sensitive to pH, maintaining its stable structure in physiological pH and dissolves in acidic environments, therefore it can be useful for controlled delivery to tumors. Another advantage relies on the fact that, once inside the cells, calcium phosphate nanoparticles dissolve and liberate calcium ions across lysosomal membranes, impairing the osmotic pressure of the cell and leading it to necrosis [27].
Liu et al. fabricated calcium phosphate-encapsulated core-shell structured nanoparticles (UCNPs-Ce6@SiO2@Calcium phosphate-Doxorubicin), characteristic for being biodegradable, biocompatible, pH-sensitive (which enables the liberation of the chemotherapeutic in the tissue), and provides therapeutic efficiency by PDT upon irradiation with 808 nm due to the presence of Chlorin e6 in its structure. Finally, due to the presence of rare earth elements, it can be used as an imaging tool for diagnostic purposes [27].
Another strategy is the development of nanomaterials that can be degraded by enzymes that are overexpressed in tumors, such as matrix metalloproteinases (MMPs) and hyaluronidase. One good example is the nanomaterial developed by Li et al. [28], which consisted of hyaluronic acid nanoparticles conjugated with chlorin e6 that disassemble in the presence of hyalurinodase and liberate the photosensitizer. This way, they can act as theranostic materials, meaning they can use as diagnostic tools and therapeutic agents. Another example was the MMP2-responsive chimeric peptide nanoparticles coupled with protoporphyrin-IX, which turn from a sphere into large fibers when MMP-2 is present, and this sphere-to-fiber transition contributes to the augmented tumor retention of the nanoparticles [29].
Dai et al. developed a peptide nanoparticle coupled with protoporphyrin-IX (PpIX-Ahx-K8(DMA)-PLGVR-PEG8) responsive to both pH and enzyme. This nanoparticle assumes a spherical shape while in circulation and avoids nonspecific uptake, and when in tumor environments they undergo a charge reversal and cleavage of the PLGVR sequence by MMP-2. Simultaneously, the DMA group is detached because of the low pH. This logic worked to enhance even more the specific uptake by tumor tissues [23].
A very intricate nanosystem combining tumor-targeted PDT with antiangiogenesis therapy and reduced glutathione (GSH) was developed by Min et al.. It consisted on a porphyrinic zirconium-metal-organic framework nanoparticle that can act simultaneously as a photosensitizer and a carrier of the vascular endothelial growth factor receptor 2 (VEGFR2) inhibitor apatinib. MnO2 covers the nanoparticle core in order to consume the intratumoral GSH, and the whole system is decorated with a camouflage made of a tumor cell membrane. The tumor specificity was much enhanced, and so was the ablative efficiency of the combined treatment provided by this nanomaterial [30].
In addition to the previous strategies, some researchers have developed nanoparticles that are activated by near-infrared light for selective photodynamic therapy, protecting healthy tissues like the skin. The mechanism of action of these systems is based on the blockage of photodynamic action from the photosensitizer by a co-loaded NIR dye via a fluorescence resonance energy transfer (FRET) effect. The photosensitizer action is recovered once the NIR dye is photobleached by NIR light irradiation in the specific site. Dong et al. developed CaCO3-PDA-PEG hollow and porous nanoparticles loaded with chlorin e6 for this purpose, and observed that they are degraded in acidic environments such as tumors, liberating the photosensitizer in a selective manner. The generation of singlet oxygen was enhanced in the acidic environment, and the photosensitizer was taken up more efficiently when administered within the nanoparticles, compared to the free photosensitizer and other formulations. It is worthy to mention that when chlorin e6 is injected in a liposomal formulation, the mice present significant weight loss, probably due to an intrinsic toxicity, and this does not happen in the CaCO3-PDA-PEG formulation [31].
Jeong et al. tested human serum albumin nanoparticles loaded with chlorin e6 in order to develop a more biocompatible system for enhanced PDT efficacy. The nanoparticles, with circa 88 nm in diameter, proved to be non-cytotoxic in the dark, but produced significant amounts of singlet oxygen upon irradiation with the appropriate wavelength. Remarkably, when injected in mice they provided a very specific tumor delivery compared with the free photosensitizer, and simultaneously provided a good imaging property die to the fluorescence of chlorin e6 [32].
PDT can be not only an adjuvant for chemotherapy, but also for immunotherapy, and nanotechnology can potentiate the results and enable the combination of the two therapies in one single approach. That is what was demonstrated by Xu et al. when they developed mesoporous silica nanoparticles made of amorphous silicon dioxide. The nanoparticles were relatively small (around 80 nm in diameter) in order to enhance the cell internalization and avoid side effects, and the pores were large (around 5–10 nm) in order to optimize the drug loading capacity. The nanoparticles were loaded with CpG oligodeoxynucleotide, which is a Toll-like receptor-9 agonist for immunotherapy, and chlorin e6. The authors observed an effective accumulation in tumors in vivo after intravenous injection, and the treatment induced cell damage and the recruitment of dendritic cells. With the immune response elicited, there was a strong cancer vaccination effect, therefore tumors in distant sites can also be affected by the treatment [21].
Finally, a novel phenomenon has been calling the attention of researchers, namely aggregation-induced emission (AIE) of photosensitizers. Some fluorophores are poor light emitters when they are in a single molecule state, but they become strong emitters when aggregated, enabling bioimaging with significant biocompatibility and photostability. Besides, they can generate singlet oxygen in the aggregated state, so they can act as efficient PDT agents. Liu and coworkers synthesized AIEsomes, which are lipid structures conjugated with compounds with AIE property, and tested their efficacy in vivo. Their compounds were biocompatible, provided efficient bioimaging and loading efficiency, ultimately leading to a significant photodynamic effect [33].
Photodynamic therapy has long proven to be an efficient way to eliminate tumors and control infections in a non-invasive way. PDT consists on the use of light-absorbent compounds named photosensitizers, which are able to excite O2 from its ground triplet state to its excited singlet state, or to generate reactive oxygen species whenever they are irradiated with an appropriate wavelength. Much success has been achieved so far, and some PDT protocols are already available for the treatment of tumors, skin infections and for dentistry applications.
Nevertheless, the full clinic potential of PDT is yet to be achieved, mainly due to some limitations of the technique, i.e. the lack solubility of photosensitizers and limited stability in aqueous media such as the blood and the biological tissues (which makes the administration to patients somewhat difficult), the limited penetration of light, especially in the visible spectrum (limiting most of the applications to superficial sites), and the hypoxia that is usually present in tumor tissues, especially the center, and is increased during photodynamic action (since PDT is intrinsically dependent on oxygen, hypoxia hinders the full therapeutic potential of PDT).
Nanotechnology offers potential solutions to these limitations due to the intrinsic properties of nanomaterials, derived mainly from quantum effects that appear in matter in the nanometric scale, and from the surface chemistry that is often optimized in nanomaterials. Nanoparticles can act as photosensitizers given the necessary conditions, or can potentiate the photodynamic properties of attached photosensitizers. Additionally, nanocarriers can be loaded with hydrophobic photosensitizers, avoiding their aggregation and enhancing their specific accumulation in the target site. Finally, upconversion, scintillating and/or radiosensitizing nanomaterials enable the application of PDT in deep-seated tumors because they absorb wavelengths that reach deeper into the organism and emit visible light that can excite photosensitizers in the vicinity.
Nevertheless, some more studies must be performed in order to develop nanoplatforms that join the advantages of both Nanotechnology and Photodynamic Therapy, with good biocompatibility and with optimized clinical results. The potential, though, is strong for Nano-PDT to become various protocols for the most diverse medical applications.
The author would like to thank Fundação de Amparo à Pesquisa do Estado de São Paulo – FAPESP for all the financial support. Fapesp grant number 2018/15598-2.
The authors declare no conflict of interest.
IntechOpen publishes different types of publications
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