Relationships between the geographic distribution of phytophagous insects and different types of vegetation: A case study of the flea beetle genus Chaetocnema (Coleoptera: Chrysomelidae) in the Afrotropical region

This study analyses the geographic distributions of 95 endemic and sub-endemic species of Chaetocnema (Coleoptera: Chrysomelidae) found in Sub-Saharan Africa and Madagascar, in order to compare and correlate their pattern of the geographic range (chorotype) and the distribution of terrestrial ecosystems in Africa and Madagascar. The data compiled for the species of Chaetocnema are based on records for 1639 collecting localities. Most of the species of Chaetocnema have restricted geographical ranges (67.3%), whereas relatively few species (11.6%) are very widely distributed. The latitudinal and longitudinal gradients in the numbers of species reveal that the highest levels of species richness occur in the Equatorial Belt and Southern Africa. Species of Chaetocnema in Sub-Saharan Africa have a clear preference for grassland and the wide-open environment associated with savannah. However, forest ecosystems are also important for numerous species, particularly in Madagascar. Several endemic species are associated with the Mediterranean vegetation in the southern part of West Africa. Species of Chaetocnema are generally associated with a limited number of vegetation types within the Afrotropical region. A cluster analysis based on calculating the squared Euclidean distance and using the WARD clustering method revealed a significant correlation between the chorotype and the vegetation types associated with each species. Finally, certain species of Chaetocnema that are characteristic of specific types of vegetation and/or indicators of biodiversity hotspots in Sub-Saharan Africa and Madagascar are highlighted.


INTRODUCTION
The ability to model the spatial distribution of species is of considerable importance in biogeography and conservation biology (Ferrier, 2002;Funk & Richardson, 2002;Rushton et al., 2004;Elith et al., 2006) because the analysis of species-environment relationships have always been a central issue in ecology (Lawton, 1983;McCoy & Bell, 1991;Tews et al., 2004).
The construction of databases using the Geographic Information System (GIS) for mapping and managing species distribution records and environmental data is relatively straightforward, and biological recording schemes routinely use GIS and/or relational database technologies to manage and maintain data resources. When the distribution and environmental data for species are integrated within a GIS environment, these data can be used to develop models for predicting the distribution of species (Franklin, 2009).
Distribution patterns of animals depend on several factors that may be ecological-environmental (recent or past), geographic, historical or related to an extinction-recolonisation event. Plant communities play a central role in influencing the distribution of phytophagous species.
The goal of this research is to interpret broad reliable presence-absence datasets for numerous species of Afrotropical Chaetocnema Stephens (Chrysomelidae: Galerucinae: Alticini), a genus of phytophagous flea beetles, in terms of the distribution of different types of African vegetation, primarily their divisions and formations, as identi-fied and described by Sayre et al. (2013). The leaf beetle genus Chaetocnema, includes over 400 described species, which occur in all zoogeographical regions (sensu Sclater, 1858). Approximately 120 species occur in the Palaearctic region (Löbl & Smetana, 2010), 59 in the Nearctic region (White, 1996), 106 in the Neotropical region and approximately 100 in the Oriental and Australian regions (Konstantinov et al., 2011). Over 100 described species occur in the Afrotropical region (Biondi & D'Alessandro, 2012).
Species of Chaetocnema generally inhabit moist environments and grassland, and are associated with plants belonging to several botanical families, particularly the Chenopodiaceae (currently included in the Amaranthaceae), Polygonaceae, Cyperaceae and Poaceae (Jolivet & Hawkeswood, 1995).
The geographical distribution of plants and animals may be described in terms of their "chorotypes". A chorotype is a group of species whose distribution in space overlap more than expected by chance and is deduced from a comparative analysis of the geographical ranges of species, genera and higher taxa (Vigna Taglianti et al., 1992, 1999. It represents then a statistically significant group of coincident distribution areas, constituting reference biogeographic units (Olivero et al., 2011). Our research analyses the geographic distribution of 95 endemic and sub-endemic species of Chaetocnema that occur in Sub-Saharan Africa and Madagascar (Table 1) and compares and correlates their chorotypes as defined for the Afrotropical region by Biondi Table 1. Occurrence of endemic and sub-endemic species of Chaetocnema in the different vegetation divisions of Sub-Saharan Africa and Madagascar proposed by Sayre et al. (2013) (for abbreviations of the vegetation types see the legend of Fig. 1). Chorotypes: AEQ -Afro-Equatorial; AFT -Afrotropical; AIT -Afro-Intertropical; CAT -Central Afrotropical; EAF -Eastern Afrotropical; MAL -Malagasy; NAT -Northern Afrotropical; NEA -North-Eastern Afrotropical; NWA -North-Western Afrotropical; PAF -Pan-African; SAF -Southern African; SEA -South-East African; SWA -South-West Afrotropical.

Study area
The research area is delimited in Fig. 1 and includes Madagascar and continental Sub-Saharan Africa, which is situated in the region that lies between 17.5°W and 52°E longitude and 20°N and 35°S latitude. Distribution maps were constructed using ESRI ArcGIS 10.0 software.

Database of vegetation types
Vegetation types considered in this study are those of Sayre et al. (2013) (Martín & Gurrea, 1999), because although present assumptions about the distribution of species of Chaetocnema in the Afrotropical region are robust, they remain far from complete (Biondi & D'Alessandro, 2006a). Vegetation maps were plotted and analyzed using ESRI ArcGIS 10.0 software.

Statistical analysis
A cluster analysis using presence-absence data of the vegetation types for each species considered was performed to find "ecologically similar" species-groups of Chaetocnema (Table 1). The analysis was conducted by calculating the Squared Euclidean Distance and using of the WARD Clustering Method (Ward, 1963;Kent, 2006). Notwithstanding that the Euclidean distance is considered to be inappropriate for analyzing the composition of communities using abundance-based data (Legendre & De Cáceres, 2013), the squared Euclidean distance is suitable for binary data because it becomes equivalent to the Hamming distance (Lourenço et al., 2004). Statistical analyses were performed and graphics produced using the NCSS version 9.0.7 package for Windows (Hintze, 2013).

Abbreviations used
Depositories
Species of Chaetocnema do not occur in desert areas and rarely occur in dry, open woodland. Fig. 5 shows the number of species (nsp) in relation to latitudinal and longitudinal gradients. Note that the diversity of species north and south of, and equidistant from the Equator is generally quite similar. Few species (6), however, are present in the Sahara desert belt (15°-20°N). Likewise, relatively few species (18) occur between 15°-20°S, which is most likely attributable to the presence there of the Namibian and Angolan desert areas (Namib and northern Kalahari) to the west and a wide belt of dry open woodland to the east; neither of these areas are suitable for species of Chaetoc nema. However, this deficit is counterbalanced by numerous species (16) in central-eastern Madagascar (Fig. 5), at the same latitude (15°-20°S). In addition, an examination of the ratio of number of species to log area (nsp/logA) reveals that the highest levels of species richness occur in southern Africa, in latitude ranges 25-30°S (nsp/logA = 6.85) and 30-35°S (nsp/logA = 5.24). The number of species is also relatively high in the Equatorial belt (5°N-5°S). The number of species recorded along the longitudinal gradients (Fig. 5) indicates that species richness levels are  highest in the longitude range 25-35°E, where the majority of the important mountainous areas in Sub-Saharan Africa are located (Fig. 5).
Within the Afrotropical region, species of Chaetocnema are generally associated with a limited number of vegetation types. Many of the species (64.2%) are associated with fewer than five vegetation divisions, and only 16.8% exist in more than 10 divisions (Fig. 6). The species occurring in the largest number of vegetation types include C. wollas toni (31 divisions), C. pulla (23), C. kibonotensis (22) and C. ljuba (21) (Fig. 7). The correlation between the number of species and the total area of each the type of vegetation considered is moderately high (r = 0.65; R 2 = 0.42) (Fig. 8).
Some of the vegetation divisions preferred by species of Chaetocnema (Fig. 9)

1.A.1. Tropical Seasonally Dry Forest
1.A.1.Fg (Albany Subtropical Thicket) (43,020 km 2 ). This vegetation division occurs in semi-arid areas in South Africa (Eastern and Western Cape Province) and is characterized by tall, dense thickets of trees and shrubs (Mucina & Rutheford, 2006). It includes numerous succulent and thorny species, as well as low thickets dominated by succulents. This type of vegetation covers 2.5% of the surface area of South Africa (nearly 31,500 km 2 ). Certain widespread endemic South African species of Chaetocnema are associated with this vegetation division, with the following chorotypes: SAF (37.5%: C. darwini, C. natalensis and C. purpurea), SWA (12.5%: C. chalcea) and SEA (12.5%: C. aluwala).

1.A.2.Fd (Guineo-Congolian
Evergreen & Semi-Evergreen Rainforest) (3,078,388 km 2 ). This vegetation division covers a wide area (10°N-10°S and 15°W-30°E) and consists of tall, dense tropical humid forest consisting of several strata. Although some of the canopy species are deciduous, the forest is primarily evergreen or semievergreen. Epiphytes, especially varieties preferring wetter conditions, are abundant. These type of vegetation occurs in Western Africa, extending from coastal regions to the Central Congo basin and also cover transitional areas of woodland formations surrounding the Congo Basin. This vegetation division is particularly significant for species of Chaetocnema occurring in the following chorotypes: NWA (14.3%: C. compressipes, C. dialloha, C. dubreka, C. mam adoua and C. nahelia), and CAT (14.3%: C. lopatini, C. maniemaensis, C. obscura, C. impressicollis and C. lufira). Guineo-Congolian Evergreen & Semi-Evergreen Rainforest is the only vegetation division in the AEQ chorotype (3.0%: C. cerylonina).

1.A.2.Fe (Malagasy Evergreen & Semi-Evergreen
Forest) (205,865 km 2 ): this vegetation division includes tropical forests ranging from sea level to an altitude of 1800 m. The Eastern Madagascar Lowland Rainforest is a humid evergreen forest located below an altitude of 800 m and found along the eastern border of Madagascar. The Eastern Madagascar Subhumid Forest is scattered across several "montane humid zone islands" located throughout the central highlands of Madagascar. It stretches from the northwestern region of Sambirano to north-western areas and includes parts of Amber Mountain in the north. Madagas-can Evergreen Littoral Forest is 5-8 m high with a closed canopy and often borders coastal lagoons and marshes. This vegetation division contains a significant number of the endemic Madagascan species of Chaetocnema (MAL 53.8%: C. consobrina,C. hygrophila,C. malgascia,C. orophila,C. pauliani,C. similis and C. vadoni).

1.B.3. Temperate Flooded & Swamp Forest
1.B.3.Fe (Fynbos Riparian Thicket) (6024 km 2 ). Dwarf shrublands divided by rivers and streams, which drain the plains and provide moist conditions suitable for the development of Riparian Thicket. The constituent species are woody shrubs and trees, and the herb layer consists of both grass and dwarf shrubs. This vegetation division occurs mainly in the Western Cape Province and hosts a number of endemic species of Chaetocnema in SAF (42.9%: C. bevinsi, C. capensis and C. darwini) and SWA (42.9%: C. capeneri, C. danielssoni and C. tablensis) chorotypes. cally 15 to 20 m tall; understory in wet miombo consists of broadleaf shrubs and a continuous carpet of grass. Dry miombo vegetation is more uniform in structure and less diverse. This broad division is particularly significant for the CAT (31.7%) chorotype, in which the following species of Chaetocnema mainly occur: C. aeneocyanea, C. genia, C. kapirensis, C. latipes, C. longipennis, C. lufira, C. maniemaensis, C. mukana, C. muya, C. nigrosericea, C. obscura, C. reprehensa and C. rotundicollis. Renosterveld, Strandveld and Cape Thicket ecosystems. The Fynbos ecosystem includes South Africa vegetation consisting of short shrubland or grassland with smallleaved shrubs and Proteaceae elements (Mucina & Rutheford, 2006). This type of vegetation only occurs in South Africa, and mainly on north-south and east-west mountain chains. It also occurs in wetter valleys in the Cape Fold Belt and the area between the mountainous coast and the Indian Ocean in the south. This division hosts a particularly rich fauna of endemic species of Chaetocnema, particularly in SAF (31.6%: C. bevinsi, C. capensis, C. darwini, C. natal ensis, C. purpurea and C. sudafricana) and SWA (31.6%: C. audisiana, C. capeneri, C. chalcea, C. convexicollis, C. danielssoni and C. tablensis) chorotypes.

3.A.2. Warm Desert & Semi-Desert
The results of the cluster analysis (squared Euclidean distance and Ward clustering method) based on presenceabsence data for species of Chaetocnema in the vegetation types examined, are presented in Fig. 11. In the dendrogram (cluster cut off = 0.7) there are five different clusters (A-E):  Cluster C: includes the largest number of species with 36 species of Chaetocnema occurring mainly in the northern and central areas of the Afrotropical region. Sixteen of the 17 species with a CAT chorotype occur in this group (44.4%). Cluster C is the only cluster that includes species with the following chorotypes: NWA (13.9%), NAT (11.1%) and AEQ (2.8%). The largest proportion of these species are associated with Tropical Grassland, Savannah & Shrubland (2A = 56.1%) and Tropical Forest (1A = 32.71%). A significant number of species with a SEA (11.1%) chorotype are also included. The latter include species mainly associated with Southern African Lowland Evergreen and Semi-Evergreen Forest (C. barkeri), and species occurring in forest and/or open environments in southern-eastern Africa with extensions into Zimbabwe, Botswana and/or Zambia (C. aluwala, C. bechuana and C. subquadrata).
Clusters D & E: these two groups are not significantly different. Cluster D is associated with the highest number of vegetation types, and includes species that are more widespread in the Afrotropical region (AFT = 57.1%; PAF = 14.50%; EAF = 14.3%): C. wollastoni, C. pulla, C. ki bonotensis and C. ljuba (Fig. 7). Although cluster E also includes species that commonly occur across the Afrotropical region, a significant proportion of this cluster is more characteristically "tropical", including species with a AIT (23.5%) chorotype, such as C. coletta, C. miloensis, C. nigripennis and C. pastoria, which are all associated with tropical forests and/or savannahs.

CONCLUSIONS
The geographical ranges of a large percentage (67.3%) of the endemic and sub-endemic species of Chaetocnema in the Afrotropical region are mainly restricted to Central Africa, southern Africa or Madagascar. Relatively few species (11.6%) are widespread in Sub-Saharan Africa and Madagascar. Though this result may in part be attributed to insufficient data, in our view it reflects the true geographical ranges of these species, a phenomenon most likely related to the trend in Chaetocnema towards specialisation and differentiation (Biondi & D'Alessandro, 2006a).
The number of species along latitudinal and longitudinal gradients reveals that the highest species richness occurs in the Equatorial belt and in southern Africa, especially in montane areas. Endemic species of Chaetocnema are very well represented in Madagascar (61.1%), which is higher than that recorded for birds (58.4%) and freshwater fish (59.1%) (Critical Ecosystems Partnership Fund, 2014 a, b).  In the Afrotropical region, each species of Chaetocnema is associated with a limited number of vegetation types. The extent of their distribution is significantly and positively correlated with the number of associated vegetation types. For example, species that occur in the largest number of vegetation types, such as C. wollastoni, C. pulla, C. kibonotensis and C. ljuba (Fig. 7), are also the most common and widespread. The correlation between the number of species and the total area for each associated vegetation type is moderately high (Fig. 8).
Chaetocnema species that occur in Sub-Saharan Africa clearly prefer vegetation types that include open grassland environments associated with savannah, and mainly occur in Central and southern Africa. These species do not occur in desert areas and are rarely present in dry open woodlands. However, the highest number of "ecologically characteristic species" occur in forest ecosystems (Fig. 12): tropical lowland and montane humid forests host several endemic species of Chaetocnema, mainly in Madagascar and Western Africa; endemic species are also associated with warm temperate forests in southern Africa. A significant number of endemic species of Chaetocnema are associated with Mediterranean-type vegetation (Fynbos, Renosterveld, Strandveld and Cape Thicket) in South-Western Africa.
Notwithstanding the relatively limited extent of the habitats surveyed, a number of the vegetation types considered host a large number of species with high levels of microendemism. This trend is particularly evident in temperate grasslands and forests in montane areas of South Africa, i.e. the Drakensberg region and Mediterranean ecosystems in the Western Cape Province.
Superimposing the general distribution of Afrotropical species of Chaetocnema on the biodiversity hotspots