bs_bs_banner Animal Conservation. Print ISSN 1367-9430 REVIEW Natural mixing of species: novel plant–animal communities on Caribbean Islands A. E. Lugo1, T. A. Carlo2 & J. M. Wunderle Jr1 1 International Institute of Tropical Forestry, USDA Forest Service, Río Piedras, Puerto Rico 2 The Pennsylvania State University, University Park, PA, USA Keywords Abstract novel communities; introduced species; Car- ibbean; Puerto Rico; US Virgin Islands; com- Global anthropogenic activities are responsible for the modification of landscapes, munity assembly; naturalized species; creation of novel environments and movement of species across biogeographic species invasions; tropical forests, species regions. A consequence of this activity is the mixing of native and introduced eradication. species and the formation of novel biotic communities. We review the ecological consequences of the mixing of native and introduced species in the Caribbean Correspondence Islands especially in Puerto Rico and the US Virgin Islands. Here we found Ariel E. Lugo, International Institute of Tropi- documented examples indicating that novel communities of native and natural- cal Forestry, USDA Forest Service, 1201 ized organisms are ubiquitous. The coexistence of species originating from differ- Calle Ceiba, Jardín Botánico sur, Río Piedras ent biogeographical regions raises research questions that demand attention for 00926-1115, Puerto Rico. their ecological and conservation importance. For example: Is animal abundance Email: [email protected] in novel communities a measure of habitat quality? To what degree are popula- tions in novel communities self-sustaining? What are the consequences of species Editor: Nathalie Pettorelli eradication? How does an introduced animal’s trophic position affect its effects on Associate Editor: Rob Ewers novel and native communities? We suggest that novel communities that emerge in the Caribbean after deforestation and land abandonment could be harbingers of Received 12 October 2011; accepted 16 how the biota might respond elsewhere to rapidly changing environmental con- January 2012 ditions, including global and climate change. doi:10.1111/j.1469-1795.2012.00523.x Introduction with plants and then review some of the patterns of mixing of introduced and the native animal species in various habitats. Anthropogenic activities are degrading lands, creating novel Finally, we discuss some of the implications of these patterns environments, extirpating species and accelerating the of species mixing to conservation and for future research. movement of species across historical biogeographic barri- ers, which lead to the mixing of organisms from disparate regions. Mixing of organisms occurs as species adopt open Novel plant communities niches resulting from environmental changes, now driven by We start by discussing the extraordinary historical changes anthropogenic activities but in the past by natural climate in Puerto Rico’s vegetation given that plant communities and geological change (Williams & Jackson, 2007). Biologi- provide the productive and structural base that supports cal invasions and a natural reshuffling of species take place animal communities. The 8959-km2 island was completely as species fill vacant niches that meet existing or new species- forested when the Europeans arrived, despite earlier occu- specific requirements. Thus, novel communities of organ- pation by indigenous people (Wadsworth, 1950). By the isms emerge and develop with combinations of species 1920s, however, Gleason & Cook (1926), in the first system- found nowhere else (Hobbs et al., 2006). Usually, the new atic assessment of the plant communities, wrote (p 5): combinations of species include native and introduced The dense rural population of Porto Rico, through its constant species, a situation anticipated by Elton (1958). These novel use of almost all available land for dwellings, agriculture, communities now cover about 35% of the terrestrial surface pasture, lumber and fuel, and through the secondary effect of of the world (Marris, 2009). fire, of drainage, and of irrigation, has destroyed some types of In this review, we use Puerto Rico and the US Virgin vegetation completely, and with a few exceptions, has modified Islands as an example to describe the species composition of all the rest to a greater or less degree. tropical terrestrial communities historically affected by Puerto Rico’s forest cover fell from almost 100% in 1493 anthropogenic changes. First, we summarize the situation to 6% by the late 1940s (Birdsey & Weaver, 1987) before Animal Conservation 15 (2012) 233–241 © 2012 The Authors. Animal Conservation © 2012 The Zoological Society of London 233 Novel plant–animal communities on Caribbean Islands A. E. Lugo et al. recovering to 57% by 2003 because of agricultural abandon- Table 1 Approximate number of extant (still living) and extinct and/or ment (Brandeis, Helmer & Oswalt, 2007). extirpated animal species in Puerto Rico by major taxa The vegetation that emerged from abandoned agricul- Number of Percent tural lands, which in 1966 covered 68.5% of the island (Picó, Animal group species introduced 1969), was different from native plant communities present Insects (Insecta) 5373 ? before deforestation (Lugo & Helmer, 2004). These plant Oligochaetesa 29 39.3 communities differed in the diversity of introduced species, Formicidaeb 77 23.4 which have mixed with the natives to form novel plant com- Other invertebrates 4596 ? munities. For example, of the island’s 203 introduced tree Fish 983 ? species, 118 are regenerating naturally, that is are natural- Amphibians 24 25.0 ized (Francis & Liogier, 1991). Despite this new mix of Extinct amphibians 3 (3) 0 species, after several decades, these novel forests develop a Reptiles 55 7.3 physiognomy and structure similar to that of mature native Extinct reptiles 0 0 forests (Aide et al., 1996). Birdsc 354 12.7 We ask whether or not the island fauna has followed the Extinct birdsd 9 (3) 0 same path as the flora. Have animal species introductions Marine mammals 27 0 led to new assemblages of organisms? What is the nature Terrestrial mammals (bats) 16 0 and strength of the interactions among introduced plants Terrestrial mammals (quadrupeds) 13 100 and native and introduced animals? How do animal inter- Extinct terrestrial mammals 6 0 actions play out in native and novel plant communities and All mammals 62 16.1 Total animal species 11 617 habitats? In addressing these questions we shed light on the consequences of species invasions in terrestrial communities The ‘extinct species’ category is only for species that became extinct and the natural processes of plant and animal community within the last millennia, numbers in parenthesis are for species reorganization following anthropogenic disturbances. extinct since the European colonization. Question mark indicates unknown percentage introduced. The area of Puerto Rico is The contemporary big picture on 8990 km2. Unless indicated otherwise, the source is Joglar (2005). animal species diversity in Puerto aBorges 1996. bTorres and Snelling 1997. Rico and the US Virgin Islands cWege and Anadón Irizarry 2008. d Puerto Rico has about 26 410 species of organisms (plant, Raffaele 1989a. macrofungi and animals) with animals representing 43% of the species total (Joglar, 2005). The number of species in most animal taxa has increased with human introductions introduced psittacines occur in or near urban habitats and making introduced species a substantial component of the novel forests where they feed on a mixture of native and intro- biota of Puerto Rico (Table 1) and the Caribbean (Kairo duced seeds and fruits (Raffaele, 1989a). Introduced finch et al., 2003; Wege & Anadón Irizarry, 2008). Anthropogenic species differ moderately from each other and from natives in activities have also facilitated the natural spread of species patterns of resource use and behavior (Raffaele, 1989b). Some across islands. For example, natural colonization from introduced species quickly adapted to the new environments South America by Cattle Egrets (Bubulcus ibis) and Shiny by shifting to habitats different than those used in their native Cowbirds (Molothrus bonariensis) through the Lesser Anti- range. The finches Lonchura cucullata and Estrilda melpoda lles into Puerto Rico and other islands was likely facilitated have accrued significant changes to bill size (including sex by the human creation of pastures and croplands (Post & differences) since their introduction more than 100 years ago Wiley, 1977; Arendt, 1988). In the last 100 years, the creation (Raffaele, 1989b). These changes contrast with the lack of of scrublands, ecotones and pastures on adjacent islands variability and sex differences in native African populations, aided the natural colonization of similar habitats on Puerto and are thought to reflect adaptations to novel food sources in Rico by doves (Zenaida asiatica and Z. macroura) and a novel Puerto Rican plant communities, as well as intra- and flycatcher, Elaenia martinica (Raffaele, 1989a). Moreover, interspecific competition (Raffaele, 1986). human introductions have increased Puerto Rico’s finches Thus, the big picture of diversity in these islands reveals from three native seed-eaters to a remarkable 20 species, large numbers of introduced species, many of which are mostly introduced from Africa and Asia. Similarly, there are naturalized and even locally adapted to the novel plant com- now 10 introduced psittacine species (5 parakeets, 4 parrots, munities