Modern tropical rainforests are the most species-rich and productive of the Earth’s terrestrial biomes. They are restricted to the tropical zones of three land areas – Indo-Malay/Australasia, Afrotropics and Neotropics – which all have high rainfall and equable temperature (Richards, 1996). Following the definition of Burnham & Johnson (2004) we use the phrase modern tropical rainforest to include several key features: high diversity and abundance of angiosperm trees and lianas; high proportions of entire-margined and large leaves; high abundance of leaf drip tips; large fruit and seed size, and abundant epiphytes. However, the actual timeframe during which modern tropical rainforests began to appear remains contentious. Some fossil floras from the mid-Cretaceous have been suggested as reminiscent of tropical rainforests (Upchurch & Wolfe, 1987; Wolfe & Upchurch, 1987; Morley, 2000). Recent dated phylogenies of important components of tropical rainforests (e.g. Malpighiales and Palmae) have also bolstered support for a mid-Cretaceous origin of this biome (Davis et al., 2005; Couvreur et al., 2011a).
Terrestrial plant ecosystems were undoubtedly altered dramatically at the Cretaceous–Paleogene (K–Pg) boundary 65.5 million yr ago (Ma) (Wolfe & Upchurch, 1986; Vajda et al., 2001; McElwain & Punyasena, 2007; Nichols & Johnson, 2008; Schulte et al., 2010). The prevailing view is that modern tropical rainforests began to appear after the K–Pg boundary (e.g. Upchurch & Wolfe, 1987; Wing & Boucher, 1998; Morley, 2000). Among the lines of evidence supporting this view are the paucity of fossils of large stems (Wheeler & Baas, 1991; Wing & Boucher, 1998) and large seeds (Tiffney, 1984; Sims, 2010) of angiosperms in the Cretaceous, which some consider a requirement for germination in low light (e.g. tropical understorey). Epiphytic ferns, characteristic of tropical rainforests (Burnham & Johnson, 2004), exhibit a shift of diversification rates near the K–Pg boundary (Schuettpelz & Pryer, 2009), in agreement with the hypothesis that modern rainforests began to appear after the K–Pg boundary. However, some families apparently were not affected during this K–Pg period. For example, three relatively ancient lineages with members in tropical rainforests, that is, the liverwort family Lejeunaceae (Wilson et al., 2007) and the angiosperm families Annonaceae (Couvreur et al., 2011b) and Palmae (Couvreur et al., 2011a), have constant diversification rates over time.
The plant macrofossil evidence for angiosperm tropical rainforest in Africa comes from the late Eocene to late Oligocene of Cameroon (c. 39–26 Ma; Jacobs, 2004). The earliest record of Neotropical rainforest comes from the middle–late Paleocene of Colombia (c. 58 Ma; Jaramillo et al., 2006; Wing et al., 2009). In North America the fossil record suggests that forests similar to modern rainforest were established in the early Paleocene (64.1 Ma; Johnson & Ellis, 2002). Although floristic and vegetational changes in Southeast Asia remain poorly understood (Morley, 2000), these aforementioned fossil observations lead us to conclude that the establishment of modern tropical rainforests in different tropical areas was not synchronous.
Lianas afford important opportunities for the investigation of rainforests in that they are largely dependent on the presence of a developed rainforest biome, in which they reach their highest diversity. Lianas constitute 15–25% of the woody stem density and species diversity in modern rainforests (Gentry, 1991) and contribute up to 40% of forest leaf area and leaf productivity (Hegarty & Caballé, 1991). They are therefore an important physiognomic and structural component of modern tropical rainforests (Gentry, 1991; Schnitzer & Bongers, 2002). Additionally, lianas also play a crucial role in many aspects of rainforest dynamics, including suppressing tree regeneration, increasing tree mortality, indirectly promoting pioneer tree growth, and providing essential food and much-needed structural components of the habitat to many forest animals (Emmons & Gentry, 1983; Schnitzer & Bongers, 2002). Thus, lianas are regarded as a key indicator of modern tropical rainforests (Upchurch & Wolfe, 1987; Gentry, 1991; Richards, 1996).
In this paper we test the hypothesis that the establishment of modern tropical rainforests in different tropical areas was not synchronous by examining the historical diversification and biogeography of the angiosperm family Menispermaceae (moonseed family). Menispermaceae are a very important representative of liana families in tropical rainforests (Upchurch & Wolfe, 1987; Gentry, 1991; Richards, 1996) and therefore offer a remarkable opportunity for studying the diversification of tropical rainforests on a worldwide basis. Menispermaceae are one of the 10 most dominant liana families in tropical rainforests (Supporting Information Fig. S1; also see Fig. 2 in Nabe-Nielsen, 2001), which contribute substantially to the diversity and abundance of woody plants (Gentry, 1991; Nabe-Nielsen, 2001). Only two genera of the family, Antizoma (three species) and Menispermum (two species), are not distributed in tropical rainforests at all, whereas the remaining 70 genera are entirely or mostly distributed in tropical rainforests (Supporting Information Table S1). Stem anatomical features indicate that moonseed plants are well adapted to warm humid habitats (Carlquist, 2007). Additionally, the swollen regions at the base of the petioles are also an adaptation to tropical rainforests, with the function of turning the lamina to face the maximum light (Forman, 1986). Both the fossil record and molecular dating studies indicate that Menispermaceae are an ancient angiosperm lineage. The oldest putative fossil endocarp of the family comes from the Turonian of central Europe (91 Ma). Some fossil leaves found in North America and Asia (but unconvincingly determined as Menispermaceae) extend back to the Early Cretaceous (Doria et al., 2008). Recent molecular clock estimates suggest a stem age of 121.8 Ma for the family (115.6–125.0; Jacques et al., 2011).
Here, we first reconstruct a robust phylogenetic framework for Menispermaceae using five chloroplast DNA regions with more extensive sampling at the generic level than in any previous study. By integrating phylogenetic, biogeographic and molecular dating methods, we then investigate the temporal and spatial diversification of Menispermaceae on a global basis. Finally, we use the moonseed family as an indicator to explore the diversification of tropical rainforests worldwide. That is, we attempt to assess whether the establishment of modern tropical rainforests in different tropical areas was synchronous or asynchronous.