Discussion
Sarcolaenaceae as a Model Group for Conservation in Madagascar
As mentioned above, Madagascar's biodiversity is among the most distinctive and highly endemic in the world, and the multiple threats it faces result in it being among the most threatened as well. There is thus a strong need to evaluate the effectiveness of conservation efforts, in particular the existing network of protected areas in Madagascar, with respect to their ability to ensure the survival of biodiversity, as measured not only by species richness but also in terms of phylogenetic diversity. In particular, PD is assumed to serve as a valuable tool for developing conservation policies, but to date very few studies have explored it for Madagascar (Sechrest et al. 2002; Magnuson-Ford et al. 2010; Isambert et al. 2011), only one of which
Fig. 4 (a) PD of Sarcolaenaceae in the Malagasy system of protected areas; (b) Ankeniheny Zahamena Forest Corridor; (c) Midongy du Sud; (d) Mangabe/Masoala; (e) Itremo massif; (f) Behara-Tranomaro; (g) Bongolava Forest Corridor
involving plants (Buerki et al. 2015). In that respect, we focused on Sarcolaenaceae in order to help provide a better understanding of the potential value of PD for conserving Madagascar's biodiversity.
A robust analysis of PD requires a dated phylogeny based on dense taxon sampling, as well as reliable data on the distribution of each species. For Sarcolaenaceae, our sampling comprised nearly 70 % of the total species diversity, with good representation from each of the ten genera in the family. We used the most up-to-date and reliable distributional information, based on more than 2000 occurrence points from the collections kept in the herbaria of the Paris Museum and of the Missouri Botanical Garden examined for recent taxonomic revisions and data from the ca. 40–50 new collections made each year since. The result presented in Fig. 2 provides the first insights into the distribution of species richness and PD for Madagascar's largest endemic plant family, showing that both measures of diversity are highest in areas with humid forest and lowest in dry forests and subarid thickets.
Measures of Biodiversity and Madagascar's Network of Protected Areas
Our results show a high level of congruence between the distribution of species richness (Fig. 2a) and PD (Fig. 2b). Although not a rule, congruence between species richness and PD is often observed (see for example, Arponen and Zupan, chapter “Representing Hotspots of Evolutionary History in Systematic Conservation Planning for European Mammals” and Chazot et al. chapter “Patterns of Species, Phylogenetic and Mimicry Diversity of Clearwing Butterflies in the Neotropics”). This is primarily due to the fact that they both increase as more species are included (see Nipperess, chapter “The Rarefaction of Phylogenetic Diversity: Formulation, Extension and Application”). But tree shape and the structure of geographic distributions also contribute to variation in congruence between these two statistics. The more balanced a tree is, the more similar each species' contribution will be to overall PD. Likewise, the more species from different parts of the tree co-occur, the higher the congruence between species richness and PD (Rodrigues et al. 2005).
Sarcolaenaceae present a case where both of these factors are at play. The phylogenetic tree is balanced, as shown by Colless's index, yielding little variation among species in PD values. Moreover, the areas with the highest level of species richness contain species belonging to several genera (Fig. 1b) rather than many species in a single genus, as would be expected if overall diversity were the result of radiation of a single lineage within a given eco-geographic zone. Sarcolaenaceae thus present a situation very different from that observed in Malagasy adephagan water beetles by Isambert et al. (2011) but highly similar to that observed in Fabaceae by Buerki et al. (2015), where the distributions of PD and species richness are highly congruent.
In contrast, MPD is independent of species richness, and high values of MPD indicate the presence of distantly-related species co-occurring in a particular area. The balanced nature of the phylogenetic tree partly explains the low variation in Mean Phylogenetic Diversity (MPD) across Madagascar (Fig. 2c). This measure provides additional insight into the distribution of phylogenetic diversity, being of particular interest in those areas with low species richness and low values of PD. In this case, high values of MPD could indicate areas in which ecological convergence has occurred in separate lineages of Sarcolaenaceae. We note, however, the absence of areas that concurrently exhibit low species diversity and high values of PD, although some areas do have low species diversity and low PD but high MPD.
The most important areas for conserving PD in Sarcolaenaceae are concentrated in the central-northern portion of Madagascar's Eastern region, including and adjacent to the eastern edge of the Ankeniheny Zahamena Forest Corridor (Figs. 3 and 4b). However, as this area does not include any representatives of Xerochlamys and Mediusella, and because the distributions of these two genera do not overlap, the ideal strategy for protecting all lineages of Sarcolaenaceae and to maximize conservation of PD for this family, would be to include two additional protected areas: the Bongolava Forest Corridor in the northwest (Fig. 4g) and the Itremo Massif (Fig. 4e). Taken together, these three regions contain 84.9 % of the PD of Sarcolaenaceae. It is also of critical importance to consider preserving sites with high MPD values because (1) they harbor distantly related species that do not share the same evolutionary history, (2) might be impacted by different threats, and (3) require different conservation procedures. Buerki and colleagues (2015) recently suggested that the current distribution of MPD in endemic Malagasy legumes could be explained by a range of factors, such as the role of watersheds and dispersal corridors during past climatic changes, as well as by the evolutionary history of the group's most important dispersers, viz. extant and extinct lemurs. They conclude by advocating that a sound conservation plan should incorporate, in addition to the traditional biodiversity measures (species richness, PD and MPD), a detailed investigation of the biotic and abiotic factor that play (or have played) a role in the dynamics of each ecosystem.
The trends observed in the PD of Sarcolaenaceae differ significantly from those observed in Malagasy legumes by Buerki et al. (2015), where high values of species richness and PD are found in the subhumid highlands and lower values in humid eastern forests. However, the Bongolava Forest Corridor (Fig. 4g) and Midongy du Sud (Fig. 4c) are two sites where MPD values are high for Sarcolaenaceae that were regarded by Wilmé et al. (2006) and Buerki et al. (2015) as lowand high-elevation watersheds, respectively, and considered by them to represent potential refugia during the Quaternary climatic shifts. The list of important areas for conserving Sarcolaenaceae would thus also include the Bongolava Forest Corridor, Midongy du Sud, along with Makira and Masoala in the northeast and the eco-geographically diverse Behara-Tranomaro-Andohahela-Tsotongambarika area in the southeast, which spans a sharp ecotone from humid forest in the east to subarid ticket in the west (Fig. 4).
The recent expansion of Madagascar's network of protected areas has strengthened conservation in several areas that exhibit high levels of PD for Sarcolaenaceae, such as Makira, Pointe à Larrée, the Ankeniheny Zahamena and Fandriana Marolambo Forest Corridors, Ambalabe and Alan'Agnalazaha (Fig. 4), all receiving legal protection within the last 5 years. Our results show that while Madagascar's present system of PAs was not designed to protect the phylogenetic diversity of Sarcolaenaceae, it nevertheless does a very good job of this, as indicated by the fact that 97.6 % of the total PD is included in cells that contain PAs. Furthermore, recent studies have shown that Sarcolaenaceae are part of a cohort of woody groups that are host to a diverse array of ectomycorrhizal fungi, which also includes members of two other endemic families, Asteropeiaceae and Sphaerosepalaceae, as well as the Malagasy species of the widespread tropical genus Uapaca (Phyllanthaceae), all of which are likewise endemic (Ducousso et al. 2008). Our results suggest that the overall distribution of Sarcolaenaceae (Fig. 1) might be constrained by aridity. As the presence of ectomycorrhizal fungi has been documented in the family, the spatial distribution of Sarcolaenaceae might also be limited by the dispersal ability of the associated fungi. This ecological interaction should therefore be taken into account when seeking to conserve the full diversity of this plant family. Members of these groups often co-occur and form an important component of the local vegetation, which suggests that habitat loss in areas rich in Sarcolaenaceae may also impact members of these other groups. The integration of information on the phylogenetic diversity of Sarcolaenaceae into conservation planning could thus also lead to species protection in these associated groups.
