The matrix fill (number of occupied cells divided by total number of cells) given by the NODF program was only 18.18%. Nestedness temperature in the data matrix was 38.62°, which was statistically higher (*P* < 0.001) than the estimated temperature of 34.84° (± 0.68°). Furthermore, the observed BR index was also higher than the expected value (BR*observed* = 1,360, BR*expected* = 1,280.27 ± 5.76, *P* < 0.001). In addition, the observed NODF index was significantly lower from the estimated value (NODF*observed* = 5.37, NODF*expected* = 8.10 ± 0.15, *P* = 0.001). Although NODFr sub-index values were similar to global NODF, observed NODFc (nestedness based exclusively on sites) was significantly higher than the expected value (NODFc*observed* = 11.24, NODFc*expected* = 8.34 ± 0.38, *P* = 0.001). These results suggest that a genuine pattern of nestedness exists among regional faunas, although this pattern is concealed as a consequence of non-nested endemic species.

#### **3.4 Similarity among biogeographical regions**

The dendrogram of faunistic similarity based on Aphodiini species revealed that the Nearctic and the Neotropical regions are most similar (Figure 5A). The Palaearctic and the Oriental regions also are similar, and together are closer to the Australian region, and narrowly followed by the Palaeotropical. The ANOSIM test shows that the Neotropical-Nearctic and the Palaearctic-Oriental pairs are statistically significant. According to this analysis, the most probable similarity configuration is made up of the following three groups (Global *R* = 0.68, *P* = 0.08): i) Nearctic-Neotropical; ii) Palaearctic-Oriental-Australian; and, iii) Palaeotropical.

Composition and Distribution Patterns of Species at a Global Biogeographic Region Scale:

**4.1 Existence of non-random distribution patterns**

Sañudo & Lobo, 2009), this relationship turns significant.

and lineages (Cabrero-Sañudo & Lobo, 2009).

**4.2 Diversification and distribution range**

historical trait.

**4. Discussion**

Biogeography of Aphodiini Dung Beetles (Coleoptera, Scarabaeidae) Based on Species Geographic... 343

dissimilarity in ecoregions did not show any significant correlation with any biological or

These results imply that the faunistic composition of Aphodiini species present in different biogeographical regions follows a geographically structured pattern. Co-occurrence and nestedness analyses suggest that there is a reliable relationship among Aphodiini faunas, although each biogeographical region is singular on its own and holds more endemic species than shared ones (except for the Neotropical region, with most of its species also distributed in the Nearctic region, particularly at the Mexican Transition Zone). The most frequent distribution patterns of shared species are related to the 'Old World faunas' (Palaearctic, Oriental, Palaeotropical and Australian regions) or the 'New World faunas' (Nearctic and Neotropical regions), being these two groups of regions also supported by the similarity analyses. Mantel test revealed a nearly significant relationship between historical and biological traits, so long-term land continuity and proximity may play a unifying role in regional faunas. In fact, when higher taxa are tested (for example, genera, as in Cabrero-

The Palaearctic and Palaeotropical regions have the highest numbers of species and endemic species. These two regions have a considerable singular faunistic composition (for example, presence of more endemic lineages or genera; Cabrero-Sañudo & Lobo, 2009), or many more species than expected (as in the Palaeotropical region). This result may be partly due to the area or the environmental heterogeneity of these regions, although results show that the compositional differences do not seem to be related to ecoregional dissimilarity. This points

Taking into account all these results, two main types of regions for Aphodiini may be considered: macroevolutionary sources – those with a long history as producers or distribution centres for many lineages – and sink regions, which are those with colonization processes and recent radiations as important shapers of current faunas (Goldberg et al., 2005). Within the first type, both the Palaearctic and Palaeotropical regions may be included, although the Nearctic region to some extent and the nexus between the Nearctic and the Neotropical regions (the Mexican Transition Zone) should not be neglected. On the contrary, the Australian, Neotropical and Oriental regions, although with singular faunas, could be included within the second type, based on the lower numbers of species, endemic species

Regions with a lower Aphodiini diversity usually have widely distributed species. This may be due to the fact that the greatest percentage of regional Aphodiini faunas consists of endemic species, so those regions with fewer species will have a proportionately greater representation of widespread species. Widely distributed species are able to colonize more biogeographical regions because they usually have greater environmental tolerances. This could be interpreted as a variation of Rapoport's rule (the size of species distributional

to historical reasons that could have influenced current distribution patterns.

The dendrogram of faunistic similarity based on parsimony and shared species showed a unique tree (length = 2085, consistency index = 0.98, retention index = 0.80, autapomorphies included; Figure 5B). The Palaearctic-Oriental and Nearctic-Neotropical region pairs again are observed. The Palaearctic-Oriental clade is closer to the Palaeotropical region, and together are joined in a clade that is closer to the Australian region. Bootstrap validation confirmed the Palaearctic-Oriental (100%), the Palaearctic-Oriental-Palaeotropical-Australian (76%), and the Nearctic-Neotropical clades (100%). Bremer support also showed highest number of steps (>30) for the Palaearctic-Oriental and the Nearctic-Neotropical clades. Although the Palaeotropical region appears to be closer to the Palaearctic-Oriental clade than the Australian region; however, there was insufficient data for bootstrapping or Bremer supports to confirm similarity.

Fig. 5. Dendrogram of faunistic similarity among worldwide regions based on distributions of Aphodiini species. (A) Sequential agglomerative, hierarchical, and nested clustering analysis. Dotted clades are well supported, according to the ANOSIM test; (B) Parsimony analysis of endemicity. Left values refer to bootstrap support; right values to Bremer support. Regions: PTR, Palaeotropical; AUS, Australian; NEA, Nearctic; NEO, Neotropical; ORI, Oriental; PAR, Palaearctic

#### **3.5 Independence of regional traits**

The dissimilarity in the Aphodiini species composition among biogeographical regions was significantly and positively related to the genera composition of the Scarabaeinae dung beetles (Mantel test correlation coefficient (ρ) = 70.13%, *P* < 0.005; when both simple and sequential Bonferroni corrections are considered). A positive correlation between Aphodiini species composition and the geological time of separation among the biogeographical regions approaches significance (ρ = 43.83%, *P* = 0.059).

As showed in Cabrero-Sañudo & Lobo (2009), regional distribution of Scarabaeinae was positively related with mammal composition (ρ = 68.45%, *P* = 0.005) and the geological time of separation among biogeographical regions (ρ = 76.68%, *P* = 0.002; when both simple and sequential Bonferroni corrections are considered). Regional mammal distribution also was positively related with the geological time of separation among biogeographical regions (ρ = 62.78%, *P* = 0.006; when a sequential Bonferroni correction was used). The regional dissimilarity in ecoregions did not show any significant correlation with any biological or historical trait.

#### **4. Discussion**

342 Global Advances in Biogeography

The dendrogram of faunistic similarity based on parsimony and shared species showed a unique tree (length = 2085, consistency index = 0.98, retention index = 0.80, autapomorphies included; Figure 5B). The Palaearctic-Oriental and Nearctic-Neotropical region pairs again are observed. The Palaearctic-Oriental clade is closer to the Palaeotropical region, and together are joined in a clade that is closer to the Australian region. Bootstrap validation confirmed the Palaearctic-Oriental (100%), the Palaearctic-Oriental-Palaeotropical-Australian (76%), and the Nearctic-Neotropical clades (100%). Bremer support also showed highest number of steps (>30) for the Palaearctic-Oriental and the Nearctic-Neotropical clades. Although the Palaeotropical region appears to be closer to the Palaearctic-Oriental clade than the Australian region; however, there was insufficient data for bootstrapping or

PAR ORI AUS PTR NEA NEO PAR ORI AUS PTR NEA NEO

100

32

76

1

100

>30

3

>30 100 >30

Bremer supports to confirm similarity.

**100**

**80**

**60**

**40**

**20**

**0**

ORI, Oriental; PAR, Palaearctic

**3.5 Independence of regional traits**

regions approaches significance (ρ = 43.83%, *P* = 0.059).

**A B**

Fig. 5. Dendrogram of faunistic similarity among worldwide regions based on distributions of Aphodiini species. (A) Sequential agglomerative, hierarchical, and nested clustering analysis. Dotted clades are well supported, according to the ANOSIM test; (B) Parsimony analysis of endemicity. Left values refer to bootstrap support; right values to Bremer support. Regions: PTR, Palaeotropical; AUS, Australian; NEA, Nearctic; NEO, Neotropical;

The dissimilarity in the Aphodiini species composition among biogeographical regions was significantly and positively related to the genera composition of the Scarabaeinae dung beetles (Mantel test correlation coefficient (ρ) = 70.13%, *P* < 0.005; when both simple and sequential Bonferroni corrections are considered). A positive correlation between Aphodiini species composition and the geological time of separation among the biogeographical

As showed in Cabrero-Sañudo & Lobo (2009), regional distribution of Scarabaeinae was positively related with mammal composition (ρ = 68.45%, *P* = 0.005) and the geological time of separation among biogeographical regions (ρ = 76.68%, *P* = 0.002; when both simple and sequential Bonferroni corrections are considered). Regional mammal distribution also was positively related with the geological time of separation among biogeographical regions (ρ = 62.78%, *P* = 0.006; when a sequential Bonferroni correction was used). The regional

#### **4.1 Existence of non-random distribution patterns**

These results imply that the faunistic composition of Aphodiini species present in different biogeographical regions follows a geographically structured pattern. Co-occurrence and nestedness analyses suggest that there is a reliable relationship among Aphodiini faunas, although each biogeographical region is singular on its own and holds more endemic species than shared ones (except for the Neotropical region, with most of its species also distributed in the Nearctic region, particularly at the Mexican Transition Zone). The most frequent distribution patterns of shared species are related to the 'Old World faunas' (Palaearctic, Oriental, Palaeotropical and Australian regions) or the 'New World faunas' (Nearctic and Neotropical regions), being these two groups of regions also supported by the similarity analyses. Mantel test revealed a nearly significant relationship between historical and biological traits, so long-term land continuity and proximity may play a unifying role in regional faunas. In fact, when higher taxa are tested (for example, genera, as in Cabrero-Sañudo & Lobo, 2009), this relationship turns significant.

The Palaearctic and Palaeotropical regions have the highest numbers of species and endemic species. These two regions have a considerable singular faunistic composition (for example, presence of more endemic lineages or genera; Cabrero-Sañudo & Lobo, 2009), or many more species than expected (as in the Palaeotropical region). This result may be partly due to the area or the environmental heterogeneity of these regions, although results show that the compositional differences do not seem to be related to ecoregional dissimilarity. This points to historical reasons that could have influenced current distribution patterns.

Taking into account all these results, two main types of regions for Aphodiini may be considered: macroevolutionary sources – those with a long history as producers or distribution centres for many lineages – and sink regions, which are those with colonization processes and recent radiations as important shapers of current faunas (Goldberg et al., 2005). Within the first type, both the Palaearctic and Palaeotropical regions may be included, although the Nearctic region to some extent and the nexus between the Nearctic and the Neotropical regions (the Mexican Transition Zone) should not be neglected. On the contrary, the Australian, Neotropical and Oriental regions, although with singular faunas, could be included within the second type, based on the lower numbers of species, endemic species and lineages (Cabrero-Sañudo & Lobo, 2009).

#### **4.2 Diversification and distribution range**

Regions with a lower Aphodiini diversity usually have widely distributed species. This may be due to the fact that the greatest percentage of regional Aphodiini faunas consists of endemic species, so those regions with fewer species will have a proportionately greater representation of widespread species. Widely distributed species are able to colonize more biogeographical regions because they usually have greater environmental tolerances. This could be interpreted as a variation of Rapoport's rule (the size of species distributional

Composition and Distribution Patterns of Species at a Global Biogeographic Region Scale:

that have showed favourable conditions for Aphodiini along the time.

**4.4 Body size**

2005; but also see Meiri et al., 2008).

distributional areas (Brown, 1995).

**4.5 Regional characteristics**

Biogeography of Aphodiini Dung Beetles (Coleoptera, Scarabaeidae) Based on Species Geographic... 345

Another observed relationship is the positive relationship between the percentage of species from a genus and the percentage of endemic species from a genus, so regions with a greater number of species per genus do so at the expense of having a greater number of endemic species for that lineage. This again relates to the role as species generators of those regions

Among Aphodiini genera, body size is a trait that shows no significant pattern with respect to geographical distribution, although it may be noted that some large genera are endemic to a single region (Cabrero-Sañudo & Lobo, 2009). However, species mean body size does significantly vary among different biogeographic regions. Thus, both Aphodiini species and endemic species from Palaeotropical and Oriental regions are smaller than those in other regions, especially the Australian, Nearctic or Palaearctic regions. Those species distributed in areas of temperate or cold climates (Nearctic or Palaearctic) may be larger, as a variation of Bergmann's rule for endotherm animals (Bergmann, 1847) which has also been observed for some insects (Blanckenhorn & Demont, 2004). Yet a large size also could be a consequence of the presence of ancient lineages (a possible variation of Cope's rule: taxa increase in body size over evolutionary time; Cope, 1887) or insularity (Gould & MacFadden, 2004). The first of these alternatives may occur among Palaearctic Aphodiini, as it has also been observed for Scarabaeinae in the Palaeotropical region (A.L.V. Davis et al., 2002). On the other hand, 'island' gigantism may have occurred among Australian Aphodiini, as indicated by the giant wetas of New Zealand, Madagascan cockroaches and millipedes, deep sea gastropods (McClain et al., 2006), and island vertebrates (Lomolino,

Nevertheless, non-endemic species are generally significantly larger than endemic ones, although endemic Aphodiini species have a greater diversity of body sizes. Aphodiini are not very good dispersers (Roslin, 2000; Roslin & Koivunen, 2001), so larger species would probably have a greater advantage to move and occupy new territories than smaller ones. In other species groups (for example, mammals or birds), larger species tend to occupy broader

The Palaearctic region presents the highest number of total and endemic Aphodiini species; however, while the Palaearctic has the highest number of species and endemics of Aphodiina, it does not support any Proctophanina. Together with the Palaeotropical region, it also shows the highest ratio of endemic/non-endemic species, indicating the great importance of endemics to the composition of its fauna. In fact, the species inhabiting the Palaearctic show the second lowest mean number of regions per species compared with those of other regions. The mean percentage of species from genus is the highest, whereas the number of species per genus is the second highest with respect to the other regions; this may be pointing to a possibly greater speciation rate for Palaearctic lineages. Also, the mean percentage of endemic species from genus is the highest in relation to the other regions. Aphodiini are usually the most common species group in dung beetle communities in the Palaearctic (Hanski, 1991b). In this region, they display the highest diversity of lineages and endemic genera (Cabrero-Sañudo & Lobo, 2009) and the greatest abundance of individuals

ranges increases with latitude; Rapoport, 1975), as one explanation for this rule is that seasonal variability fosters a greater climatic tolerance, and therefore wider latitudinal ranges (Letcher & Harvey, 1994; Stevens, 1996).

Moreover, the phylogenetic relationships among species in a biogeographic region are likely higher within the region than with species from other regions. This has been indicated by the fact that regions with large numbers of species carry a greater number of species per genus and a higher percentage of species per genus. Thus, those regions with favourable environmental conditions to accommodate a greater number of Aphodiini species also could have functioned as speciation centers (macroevolutionary source regions, as the Palaearctic and Palaeotropical).

It has been pointed that the environmental tolerance of species may be related to ecophysiological adaptations at higher taxonomic levels (Hawkins et al., 2006; Ricklefs, 2006). Although the geographic distribution of a lineage (genus) could then be related to its tolerance at a large scale, favourability and diversity of environmental conditions could promote an ecological diversification (spatial, seasonal, altitudinal, feeding, etc.) even among related species (Del Rey & Lobo, 2006; Finn & Gittings, 2003; Gittings & Giller, 1997; Hanski, 1991b). This ecological diversification would act on endemic or non-endemic lineages equally, as it has been noted that the number of species per genus within a region and the number of species per endemic genus are positively related.

#### **4.3 Endemic and non-endemic species**

The total species richness and the number of endemic species are related; this is probably due to a greater percentage of endemic species *versus* non-endemic ones. Actually there is a significant difference in regional species numbers between endemic and non-endemic species. A total of 1,891 out of the 2,052 Aphodiini species (92%) are endemic to a single region; less than one tenth of species are shared among regions. Widely distributed species usually correspond to those of a known wide ecological spectrum and opportunistic nature. For example, the three most widely distributed species, *Calamosternus granarius* (Linnaeus, 1767) (present in all biogeographical regions), and *Aphodius fimetarius* (Linnaeus, 1758) and *Labarrus pseudolividus* (Balthasar, 1941) (present in five biogeographical regions), show a higher climatic tolerance, are not strictly coprophagous, and can alternatively behave as saprophagous, fungivorous or cleptoparasites (Cabrero-Sañudo et al., 2010; Veiga, 1998).

The correlation between total numbers of endemic and non-endemic species is almost nonexistent, probably because world biogeographical regions have partially independent evolutionary histories. In fact, regions with the least number of non-endemic species are the Palaeotropical and the Australian (27 and 11 non-endemic species, respectively), while the other regions have from 65 to 84 non-endemic species registered. This may indicate that recent continental isolation of these two regions could have prevented introduction of many broadly distributed species. Moreover, regions with a lower number of non-endemic Aphodiini tend to have more species per endemic genus. This fact could point to competition between widespread, better adapted and more competitive species and endemic, more specialized species (although see Finn & Gittings, 2003) or certain speciation process that could occur in isolated territories (Gillespie & Roderick, 2002).

Another observed relationship is the positive relationship between the percentage of species from a genus and the percentage of endemic species from a genus, so regions with a greater number of species per genus do so at the expense of having a greater number of endemic species for that lineage. This again relates to the role as species generators of those regions that have showed favourable conditions for Aphodiini along the time.

#### **4.4 Body size**

344 Global Advances in Biogeography

ranges increases with latitude; Rapoport, 1975), as one explanation for this rule is that seasonal variability fosters a greater climatic tolerance, and therefore wider latitudinal

Moreover, the phylogenetic relationships among species in a biogeographic region are likely higher within the region than with species from other regions. This has been indicated by the fact that regions with large numbers of species carry a greater number of species per genus and a higher percentage of species per genus. Thus, those regions with favourable environmental conditions to accommodate a greater number of Aphodiini species also could have functioned as speciation centers (macroevolutionary source regions, as the Palaearctic

It has been pointed that the environmental tolerance of species may be related to ecophysiological adaptations at higher taxonomic levels (Hawkins et al., 2006; Ricklefs, 2006). Although the geographic distribution of a lineage (genus) could then be related to its tolerance at a large scale, favourability and diversity of environmental conditions could promote an ecological diversification (spatial, seasonal, altitudinal, feeding, etc.) even among related species (Del Rey & Lobo, 2006; Finn & Gittings, 2003; Gittings & Giller, 1997; Hanski, 1991b). This ecological diversification would act on endemic or non-endemic lineages equally, as it has been noted that the number of species per genus within a region

The total species richness and the number of endemic species are related; this is probably due to a greater percentage of endemic species *versus* non-endemic ones. Actually there is a significant difference in regional species numbers between endemic and non-endemic species. A total of 1,891 out of the 2,052 Aphodiini species (92%) are endemic to a single region; less than one tenth of species are shared among regions. Widely distributed species usually correspond to those of a known wide ecological spectrum and opportunistic nature. For example, the three most widely distributed species, *Calamosternus granarius* (Linnaeus, 1767) (present in all biogeographical regions), and *Aphodius fimetarius* (Linnaeus, 1758) and *Labarrus pseudolividus* (Balthasar, 1941) (present in five biogeographical regions), show a higher climatic tolerance, are not strictly coprophagous, and can alternatively behave as saprophagous, fungivorous or cleptoparasites (Cabrero-Sañudo et al., 2010; Veiga, 1998).

The correlation between total numbers of endemic and non-endemic species is almost nonexistent, probably because world biogeographical regions have partially independent evolutionary histories. In fact, regions with the least number of non-endemic species are the Palaeotropical and the Australian (27 and 11 non-endemic species, respectively), while the other regions have from 65 to 84 non-endemic species registered. This may indicate that recent continental isolation of these two regions could have prevented introduction of many broadly distributed species. Moreover, regions with a lower number of non-endemic Aphodiini tend to have more species per endemic genus. This fact could point to competition between widespread, better adapted and more competitive species and endemic, more specialized species (although see Finn & Gittings, 2003) or certain speciation

process that could occur in isolated territories (Gillespie & Roderick, 2002).

and the number of species per endemic genus are positively related.

ranges (Letcher & Harvey, 1994; Stevens, 1996).

**4.3 Endemic and non-endemic species**

and Palaeotropical).

Among Aphodiini genera, body size is a trait that shows no significant pattern with respect to geographical distribution, although it may be noted that some large genera are endemic to a single region (Cabrero-Sañudo & Lobo, 2009). However, species mean body size does significantly vary among different biogeographic regions. Thus, both Aphodiini species and endemic species from Palaeotropical and Oriental regions are smaller than those in other regions, especially the Australian, Nearctic or Palaearctic regions. Those species distributed in areas of temperate or cold climates (Nearctic or Palaearctic) may be larger, as a variation of Bergmann's rule for endotherm animals (Bergmann, 1847) which has also been observed for some insects (Blanckenhorn & Demont, 2004). Yet a large size also could be a consequence of the presence of ancient lineages (a possible variation of Cope's rule: taxa increase in body size over evolutionary time; Cope, 1887) or insularity (Gould & MacFadden, 2004). The first of these alternatives may occur among Palaearctic Aphodiini, as it has also been observed for Scarabaeinae in the Palaeotropical region (A.L.V. Davis et al., 2002). On the other hand, 'island' gigantism may have occurred among Australian Aphodiini, as indicated by the giant wetas of New Zealand, Madagascan cockroaches and millipedes, deep sea gastropods (McClain et al., 2006), and island vertebrates (Lomolino, 2005; but also see Meiri et al., 2008).

Nevertheless, non-endemic species are generally significantly larger than endemic ones, although endemic Aphodiini species have a greater diversity of body sizes. Aphodiini are not very good dispersers (Roslin, 2000; Roslin & Koivunen, 2001), so larger species would probably have a greater advantage to move and occupy new territories than smaller ones. In other species groups (for example, mammals or birds), larger species tend to occupy broader distributional areas (Brown, 1995).

#### **4.5 Regional characteristics**

The Palaearctic region presents the highest number of total and endemic Aphodiini species; however, while the Palaearctic has the highest number of species and endemics of Aphodiina, it does not support any Proctophanina. Together with the Palaeotropical region, it also shows the highest ratio of endemic/non-endemic species, indicating the great importance of endemics to the composition of its fauna. In fact, the species inhabiting the Palaearctic show the second lowest mean number of regions per species compared with those of other regions. The mean percentage of species from genus is the highest, whereas the number of species per genus is the second highest with respect to the other regions; this may be pointing to a possibly greater speciation rate for Palaearctic lineages. Also, the mean percentage of endemic species from genus is the highest in relation to the other regions. Aphodiini are usually the most common species group in dung beetle communities in the Palaearctic (Hanski, 1991b). In this region, they display the highest diversity of lineages and endemic genera (Cabrero-Sañudo & Lobo, 2009) and the greatest abundance of individuals

Composition and Distribution Patterns of Species at a Global Biogeographic Region Scale:

prospecting efforts, and/or recent Aphodiini species diversification.

no fossil evidence for Aphodiini in the Oriental region (Krell, 2007).

Oligocene, a little more recent than those of the Palaearctic (Krell, 2007).

Biogeography of Aphodiini Dung Beetles (Coleoptera, Scarabaeidae) Based on Species Geographic... 347

size of endemic species is also the second lowest. The Palaeotropical region holds the second highest mean percentage of species from genus, the second highest mean percentage of endemic species from genus, and the highest mean number of species per genus. In addition, the relatively recent isolation of the Palaeotropical region with respect to other regions could explain its having the second lowest number of non-endemic species and the largest number of species per endemic genus. So, together with the Palaearctic region, the Palaeotropical region can be considered as a macroevolutionary source region, possibly acting as a refuge and/or a recent diversification centre for Aphodiini species. However, there is as yet no record for Tertiary or Quaternary Aphodiini fossils within the Palaeotropical region (Krell, 2007), possibly a consequence of limited preservation,

The Oriental region is the fourth most prominent in terms of number of species, all of which are from the subtribe Aphodiina. Although this region hosts a few more species than expected according to its area, it is the third lowest in terms of endemic species, has the second lowest endemic/non-endemic species ratio, and has one of the greatest mean species distribution ranges, sharing many species with the Palaearctic region (61 out of 65 nonendemic species). This region has the second lowest mean body size per species, the lowest mean body size of endemic species, the second lowest percentage of species from genus, the lowest mean percentage of endemic species from genus, the second lowest number of species per genus, and the lowest number of species per endemic genus. The Oriental region may have had less environmentally favourable conditions for Aphodiini species, so that widely distributed species would have been proportionately more successful. This suggests the Oriental region to be mainly a macroevolutionary sink for Aphodiini species. Studies on dung beetle communities carried out in the Oriental region frequently omit results for Aphodiini or show that they represent a small proportion of local Scarabaeidae richness (c. 4-10% of species; A.J. Davis, 2000; A.J. Davis et al., 2001; Hanski & Krikken, 1991; Shahabuddin et al., 2005). However, most of those studies were conducted on island communities, and there is a conspicuous lack of study of continental communities, particularly considering the likely species richness and abundances for Aphodiini. As for the Palaeotropical region, there is as yet

The Nearctic region has the highest number of Aphodiini species and endemic species in the New World, hosting representatives from the three tribes, although only Aphodiina and Didactyliina contain endemic species. In relation to the other regions, the Nearctic has the third highest number of species and endemics. Moreover, the Nearctic region supports the third highest mean percentage of species from genus, endemic species from genus, and number of species per genus. These facts define the Nearctic as a mainly macroevolutionary source region for Aphodiini. Several Nearctic species are shared with the Neotropical region (77 out of 84 non-endemic species), and many of them are endemic to the Mexican Transition Zone, although with a Nearctic or Holarctic origin (Cabrero-Sañudo et al., 2007, 2010). Aphodiini are usually the dominant species group in northern dung beetle communities in the Nearctic region (Lobo, 2000, and references therein). Also, Nearctic region total and endemic species have the second greatest mean body size per species, probably due to colder climates or presence of older lineages. This region also has displayed an ancient presence of Aphodiini, with the first Nearctic fossil records dating from the

in northern communities compared with other scarabaeid taxa (Hanski, 1991b; Gittings & Giller, 1997, 1998; Roslin & Koivunen, 2001; Finn & Gittings, 2003). The best studied area in the world has traditionally been the Western Palaearctic, in which Aphodiini taxonomy has attracted much attention, although many Aphodiini species may still remain undiscovered (Cabrero-Sañudo & Lobo, 2003). The only phylogenetic studies conducted on Aphodiini evolution were based on Iberian species within the Palaearctic (Cabrero-Sañudo & Zardoya, 2004; Cabrero-Sañudo, 2007) and showed that most of the earlier branches of Aphodiini are of Palaearctic or Holarctic in distribution. While this may support the hypothesis of a Laurasian origin of Aphodiini, the geographical and taxonomic scope of those studies was limited. Nevertheless, the oldest known fossil evidence for Aphodiini is from the Paleocene, with many other fossils from subsequent epochs (Figure 6; Krell, 2007).

Fig. 6. Sites where extinct Aphodiini fossil species have been found, according to Krell (2007). For each site, a list of described species is provided. In most cases, the genus of the species is *Aphodius* Illiger, 1758, as they have not been yet classified into suitable genera. Geologic epoch of lagerstätten represented by geometric figures: i) triangle, Paleocene; ii) square, Eocene; iii) pentagon, Oligocene; and, iv) circle, Pleistocene.

The Palaeotropical region also shows important numbers of total and endemic species of Aphodiini. Its endemic/non-endemic species ratio is the highest and almost three times that of the next highest region, the Palaearctic. Thus, the mean number of regions per species is the lowest compared with other regions. Aphodiina is well represented, with both second highest numbers of species and endemic species. Also, both Didactyliina and Proctophanina show the highest species and endemic species richness in this region. Although Palaeotropical dung beetle communities tend to be dominated by Scarabaeinae individuals (Cambefort, 1991; A.L.V. Davis et al., 2002; Doube, 1991), some studies show that the abundance of Aphodiini in some localities can sometimes be very high, or even the highest (Bernon, 1981; Krell et al., 2003; D. Rougon & C. Rougon, 1991). However, the mean body size of Palaeotropical species is the lowest in relation to other regions, and the mean body

in northern communities compared with other scarabaeid taxa (Hanski, 1991b; Gittings & Giller, 1997, 1998; Roslin & Koivunen, 2001; Finn & Gittings, 2003). The best studied area in the world has traditionally been the Western Palaearctic, in which Aphodiini taxonomy has attracted much attention, although many Aphodiini species may still remain undiscovered (Cabrero-Sañudo & Lobo, 2003). The only phylogenetic studies conducted on Aphodiini evolution were based on Iberian species within the Palaearctic (Cabrero-Sañudo & Zardoya, 2004; Cabrero-Sañudo, 2007) and showed that most of the earlier branches of Aphodiini are of Palaearctic or Holarctic in distribution. While this may support the hypothesis of a Laurasian origin of Aphodiini, the geographical and taxonomic scope of those studies was limited. Nevertheless, the oldest known fossil evidence for Aphodiini is from the Paleocene,

> **MENAT (FRANCE)**

**ÖHNINGEN (GERMANY)**

*Aphodius anteactus* Krell, 2000 *Aphodius brevippenis* Heer, 1862 *Aphodius meyeri* Heer, 1847

*Aphodius charauxi* Piton, 1940

*Aphodius theobaldi* Krell, 2000

Fig. 6. Sites where extinct Aphodiini fossil species have been found, according to Krell (2007). For each site, a list of described species is provided. In most cases, the genus of the species is *Aphodius* Illiger, 1758, as they have not been yet classified into suitable genera. Geologic epoch of lagerstätten represented by geometric figures: i) triangle, Paleocene; ii)

The Palaeotropical region also shows important numbers of total and endemic species of Aphodiini. Its endemic/non-endemic species ratio is the highest and almost three times that of the next highest region, the Palaearctic. Thus, the mean number of regions per species is the lowest compared with other regions. Aphodiina is well represented, with both second highest numbers of species and endemic species. Also, both Didactyliina and Proctophanina show the highest species and endemic species richness in this region. Although Palaeotropical dung beetle communities tend to be dominated by Scarabaeinae individuals (Cambefort, 1991; A.L.V. Davis et al., 2002; Doube, 1991), some studies show that the abundance of Aphodiini in some localities can sometimes be very high, or even the highest (Bernon, 1981; Krell et al., 2003; D. Rougon & C. Rougon, 1991). However, the mean body size of Palaeotropical species is the lowest in relation to other regions, and the mean body

square, Eocene; iii) pentagon, Oligocene; and, iv) circle, Pleistocene.

*Aphodius bosniaskii* Handlirsch, 1907

**SANNOISIEN DU GARD (FRANCE)**

> **GABBRO (ITALY)**

**BORYSLAW (POLAND)**

**ROTT (GERMANY)**

*Aphodius helvolus* Statz, 1952 *Aphodius krantzi* Heyden & Heyden, 1866 *Aphodius schlickumi* Statz, 1952

> *Aphodius boryslavicus* Łomnicki, 1894 *Aphodius rhinocerontis* Łomnicki, 1894 *Aphodius ruthenus* Łomnicki, 1894 *Aphodius subater* Łomnicki, 1894

with many other fossils from subsequent epochs (Figure 6; Krell, 2007).

**BONE CAVES OF PORT KENNEDY (USA)**

*Aphodius precursor* Horn, 1876

**FLORISSANT (USA)**

*Aphodius aboriginalis* Wickham, 1912 *Aphodius florissantensis* Wickham, 1911 *Aphodius granarioides* Wickham, 1913 *Aphodius inundatus* Wickham, 1914 *Aphodius laminicola* Wickham, 1910 *Aphodius mediaevus* Wickham, 1914 *Aphodius praeemptor* Wickham, 1913 *Aphodius restructus* (Wickham, 1912) *Aphodius senex* Wickham, 1914 *Aphodius shoshonis* Wickham, 1912 *Oxyomus nearcticus* Wickham, 1914

size of endemic species is also the second lowest. The Palaeotropical region holds the second highest mean percentage of species from genus, the second highest mean percentage of endemic species from genus, and the highest mean number of species per genus. In addition, the relatively recent isolation of the Palaeotropical region with respect to other regions could explain its having the second lowest number of non-endemic species and the largest number of species per endemic genus. So, together with the Palaearctic region, the Palaeotropical region can be considered as a macroevolutionary source region, possibly acting as a refuge and/or a recent diversification centre for Aphodiini species. However, there is as yet no record for Tertiary or Quaternary Aphodiini fossils within the Palaeotropical region (Krell, 2007), possibly a consequence of limited preservation, prospecting efforts, and/or recent Aphodiini species diversification.

The Oriental region is the fourth most prominent in terms of number of species, all of which are from the subtribe Aphodiina. Although this region hosts a few more species than expected according to its area, it is the third lowest in terms of endemic species, has the second lowest endemic/non-endemic species ratio, and has one of the greatest mean species distribution ranges, sharing many species with the Palaearctic region (61 out of 65 nonendemic species). This region has the second lowest mean body size per species, the lowest mean body size of endemic species, the second lowest percentage of species from genus, the lowest mean percentage of endemic species from genus, the second lowest number of species per genus, and the lowest number of species per endemic genus. The Oriental region may have had less environmentally favourable conditions for Aphodiini species, so that widely distributed species would have been proportionately more successful. This suggests the Oriental region to be mainly a macroevolutionary sink for Aphodiini species. Studies on dung beetle communities carried out in the Oriental region frequently omit results for Aphodiini or show that they represent a small proportion of local Scarabaeidae richness (c. 4-10% of species; A.J. Davis, 2000; A.J. Davis et al., 2001; Hanski & Krikken, 1991; Shahabuddin et al., 2005). However, most of those studies were conducted on island communities, and there is a conspicuous lack of study of continental communities, particularly considering the likely species richness and abundances for Aphodiini. As for the Palaeotropical region, there is as yet no fossil evidence for Aphodiini in the Oriental region (Krell, 2007).

The Nearctic region has the highest number of Aphodiini species and endemic species in the New World, hosting representatives from the three tribes, although only Aphodiina and Didactyliina contain endemic species. In relation to the other regions, the Nearctic has the third highest number of species and endemics. Moreover, the Nearctic region supports the third highest mean percentage of species from genus, endemic species from genus, and number of species per genus. These facts define the Nearctic as a mainly macroevolutionary source region for Aphodiini. Several Nearctic species are shared with the Neotropical region (77 out of 84 non-endemic species), and many of them are endemic to the Mexican Transition Zone, although with a Nearctic or Holarctic origin (Cabrero-Sañudo et al., 2007, 2010). Aphodiini are usually the dominant species group in northern dung beetle communities in the Nearctic region (Lobo, 2000, and references therein). Also, Nearctic region total and endemic species have the second greatest mean body size per species, probably due to colder climates or presence of older lineages. This region also has displayed an ancient presence of Aphodiini, with the first Nearctic fossil records dating from the Oligocene, a little more recent than those of the Palaearctic (Krell, 2007).

Composition and Distribution Patterns of Species at a Global Biogeographic Region Scale:

species distributions.

periods.

Biogeography of Aphodiini Dung Beetles (Coleoptera, Scarabaeidae) Based on Species Geographic... 349

Aphodiini would have remained within Laurasia, although it is possible that a few Aphodiini lineages survived on Gondwanan continents, as shown by some genera and

Due to the extinction of dinosaurs (K/T boundary, late Cretaceous, c. 66 Ma) dung from mammals became increasingly more common, providing a resource that could be consumed gradually by new Aphodiini taxa. Eurasia and North America approached each other and were intermittently connected (from late Cretaceous to Eocene periods, 66-38 Ma; Scotese, 2003), helping explain why the first Aphodiini fossils registered in North America date from these ages. The faunas from the rest of the regions probably had little contact in these

During the Miocene (26-12 Ma), Eurasia and Africa collided and a secondary radiation of Aphodiini (similar to that of Scarabaeinae; A.L.V. Davis & Scholtz, 2001; A.L.V. Davis et al., 2002) may have resulted as a consequence of mixing faunas and the establishment of new dispersal routes between the two continents (Potts & Behrensmeyer, 1993). This interchange culminated during the late Miocene period (12 Ma), when the Indian peninsula collided against Eurasia and several Aphodiini taxa probably colonized that territory. Also, prairies and savannas became more common as aridity and climate cooling increased (Cambefort, 1991b; Scotese, 2003), and the radiation of Artiodactyla (Bovini) (30+ Ma; Cumming, 1982; Silva & Downing, 1995) brought new high-quality soft-fibrous droppings. Mantel tests results highlight the relationships between Aphodiini and Scarabaeinae, mammal faunas,

An increase in prairie lands also occurred in North America, and the Beringian land bridges permitted the passage of Bovini and other mammals from Eurasia to the Nearctic region during the Miocene and Pliocene (Potts & Behrensmeyer, 1993). However, the most important American event was the closure of the Isthmus of Panama during the late Miocene and Pliocene (13-7 Ma; Coates et al., 2004), which caused the Great American Interchange of species (Webb, 1985), and also range expansions of many dung beetle taxa, such as the Scarabaeinae (A.L.V. Davis & Scholtz, 2001). A certain number of current Neotropical Aphodiini species are the likely survivors of a specialized and hardly

The principal characteristic of the Australian continent has been its prolonged isolation from the rest of the regions, and the lack of placental mammals until the Pleistocene (2.5 Ma-10 ka; Cox, 2000). Hence, older Australian Aphodiini lineages would have been adapted to exploiting excrements from marsupials. Land connections during the Pleistocene between Eurasia and Australia probably allowed the dispersal of mammals towards the latter region, together with a number of Aphodiini species associated with them. The mass extinction of monotremes and marsupials (Murray, 1984) may have caused the extinction of some endemic Aphodiini, but newcomer Aphodiini species may have proliferated with the

Middle-late Pleistocene (420-18 ka) glacial-interglacial cycles (Imbrie et al., 1993), could have played an important role as modifying factors of Aphodiini distributions and diversity, especially in the Holarctic regions (Hanski, 1991b). Fossil evidence (Coope, 1978, 1990; Coope & Angus, 1975; Lindroth, 1948) confirms that insects underwent range shifts during the Pleistocene in relation to changes in climate and vegetation. Thus, in the Northern

and land connectivity, all of which are probably related to these events.

diversified fauna previously present at this region.

advent of soft-fibrous droppings.

The Neotropical region holds the second lowest richness for species and endemic species, and holds the least number of species on the basis of the region's land area. Although it hosts species from the three different subtribes, there are only endemic representatives from the Aphodiina and Didactyliina. It shares several Aphodiini species with the Nearctic region (all its non-endemic species), mainly endemic from the Mexican Transition Zone (Cabrero-Sañudo et al., 2007, 2010). Its ratio of endemic/non-endemic genera and the mean number of species per genus are the lowest, and the mean number of species per endemic genus is the second lowest. These facts point to the Neotropical having probably acted as a macroevolutionary sink region. Few studies on Neotropical dung beetle communities have taken Aphodiini into consideration. Although very few Aphodiini species are represented in those communities, they can be very abundant (Andresen, 2002). No Aphodiini fossil records have been found for this region.

The Australian region shows the lowest numbers of Aphodiini species and endemic species, with only two subtribes (Aphodiina and Proctophanina) represented in the region. The mean percentage of species from genus is also the lowest, whereas the mean percentage of endemic species from genus is the second lowest, after the Oriental region. However, the number of species per endemic genus is the highest, in relation to other regions. Due to its isolation, the Australian region seems to have received occasional representatives (widely distributed, generalist species) of different lineages over time. Some of these colonizing species likely led to the emergence of endemic genera, which then diversified. Consequently, the Australian region appears to have acted as a macroevolutionary sink with regard to Aphodiini lineages, but has served as a source region with regard to species. Australian species also display the largest mean body size per species and per endemic species compared with other regions, indicating a possible island gigantism or the presence of ancient lineages. With regard to abundance and species richness, Scarabaeinae dominate northern Australian dung beetle communities, while southern Australian communities are dominated by endemic species of Aphodiini (Doube et al., 1991; Steinbauer & Weir, 2007). There is as yet no fossil record for Aphodiini in this region, due to causes similar to those of the Palaeotropical, Oriental and Neotropical regions.

#### **4.6 A synthesis of Aphodiini evolution and historical biogeography**

The main radiation of Scarabaeoidea dates from the Mesozoic and Cenozoic ages (A.L.V. Davis et al., 2002; Krell, 2000; Scholtz & Chown, 1995), but Aphodiini probably did not separate from the Scarabaeidae main lineage and from the other Aphodiinae subfamilies until the Jurassic or Cretaceous (Krell, 2000). The radiation of coprophagous beetles presumably happened as dung from vertebrates (dinosaurs and/or small mammals) increased (Arillo & Ortuño, 2008; A.L.V. Davis, 1990, 2002; Halffter & Matthews, 1966; Jeannel, 1942; Philips, 2011). The first Aphodiini probably developed before or around the early Jurassic age (200-170 Ma), when most continents were joined in Pangea. Most Aphodiini have temperate to temperate-cold and/or subalpine preferences, so they may have arisen at the northern territories of contemporary Eurasia (Cabrero-Sañudo & Zardoya, 2004), where the climate was cool with temperate conditions, compared to the rest of the world, which was very arid and hot (Scotese, 2003). Some of the first lineages of Aphodiini could have spread later to other Pangean southern territories before their break-up. After the fragmentation of Pangea (middle Jurassic to early Cretaceous; 160-130 Ma), most

The Neotropical region holds the second lowest richness for species and endemic species, and holds the least number of species on the basis of the region's land area. Although it hosts species from the three different subtribes, there are only endemic representatives from the Aphodiina and Didactyliina. It shares several Aphodiini species with the Nearctic region (all its non-endemic species), mainly endemic from the Mexican Transition Zone (Cabrero-Sañudo et al., 2007, 2010). Its ratio of endemic/non-endemic genera and the mean number of species per genus are the lowest, and the mean number of species per endemic genus is the second lowest. These facts point to the Neotropical having probably acted as a macroevolutionary sink region. Few studies on Neotropical dung beetle communities have taken Aphodiini into consideration. Although very few Aphodiini species are represented in those communities, they can be very abundant (Andresen, 2002). No Aphodiini fossil

The Australian region shows the lowest numbers of Aphodiini species and endemic species, with only two subtribes (Aphodiina and Proctophanina) represented in the region. The mean percentage of species from genus is also the lowest, whereas the mean percentage of endemic species from genus is the second lowest, after the Oriental region. However, the number of species per endemic genus is the highest, in relation to other regions. Due to its isolation, the Australian region seems to have received occasional representatives (widely distributed, generalist species) of different lineages over time. Some of these colonizing species likely led to the emergence of endemic genera, which then diversified. Consequently, the Australian region appears to have acted as a macroevolutionary sink with regard to Aphodiini lineages, but has served as a source region with regard to species. Australian species also display the largest mean body size per species and per endemic species compared with other regions, indicating a possible island gigantism or the presence of ancient lineages. With regard to abundance and species richness, Scarabaeinae dominate northern Australian dung beetle communities, while southern Australian communities are dominated by endemic species of Aphodiini (Doube et al., 1991; Steinbauer & Weir, 2007). There is as yet no fossil record for Aphodiini in this region, due to causes similar to those of

records have been found for this region.

the Palaeotropical, Oriental and Neotropical regions.

**4.6 A synthesis of Aphodiini evolution and historical biogeography**

The main radiation of Scarabaeoidea dates from the Mesozoic and Cenozoic ages (A.L.V. Davis et al., 2002; Krell, 2000; Scholtz & Chown, 1995), but Aphodiini probably did not separate from the Scarabaeidae main lineage and from the other Aphodiinae subfamilies until the Jurassic or Cretaceous (Krell, 2000). The radiation of coprophagous beetles presumably happened as dung from vertebrates (dinosaurs and/or small mammals) increased (Arillo & Ortuño, 2008; A.L.V. Davis, 1990, 2002; Halffter & Matthews, 1966; Jeannel, 1942; Philips, 2011). The first Aphodiini probably developed before or around the early Jurassic age (200-170 Ma), when most continents were joined in Pangea. Most Aphodiini have temperate to temperate-cold and/or subalpine preferences, so they may have arisen at the northern territories of contemporary Eurasia (Cabrero-Sañudo & Zardoya, 2004), where the climate was cool with temperate conditions, compared to the rest of the world, which was very arid and hot (Scotese, 2003). Some of the first lineages of Aphodiini could have spread later to other Pangean southern territories before their break-up. After the fragmentation of Pangea (middle Jurassic to early Cretaceous; 160-130 Ma), most Aphodiini would have remained within Laurasia, although it is possible that a few Aphodiini lineages survived on Gondwanan continents, as shown by some genera and species distributions.

Due to the extinction of dinosaurs (K/T boundary, late Cretaceous, c. 66 Ma) dung from mammals became increasingly more common, providing a resource that could be consumed gradually by new Aphodiini taxa. Eurasia and North America approached each other and were intermittently connected (from late Cretaceous to Eocene periods, 66-38 Ma; Scotese, 2003), helping explain why the first Aphodiini fossils registered in North America date from these ages. The faunas from the rest of the regions probably had little contact in these periods.

During the Miocene (26-12 Ma), Eurasia and Africa collided and a secondary radiation of Aphodiini (similar to that of Scarabaeinae; A.L.V. Davis & Scholtz, 2001; A.L.V. Davis et al., 2002) may have resulted as a consequence of mixing faunas and the establishment of new dispersal routes between the two continents (Potts & Behrensmeyer, 1993). This interchange culminated during the late Miocene period (12 Ma), when the Indian peninsula collided against Eurasia and several Aphodiini taxa probably colonized that territory. Also, prairies and savannas became more common as aridity and climate cooling increased (Cambefort, 1991b; Scotese, 2003), and the radiation of Artiodactyla (Bovini) (30+ Ma; Cumming, 1982; Silva & Downing, 1995) brought new high-quality soft-fibrous droppings. Mantel tests results highlight the relationships between Aphodiini and Scarabaeinae, mammal faunas, and land connectivity, all of which are probably related to these events.

An increase in prairie lands also occurred in North America, and the Beringian land bridges permitted the passage of Bovini and other mammals from Eurasia to the Nearctic region during the Miocene and Pliocene (Potts & Behrensmeyer, 1993). However, the most important American event was the closure of the Isthmus of Panama during the late Miocene and Pliocene (13-7 Ma; Coates et al., 2004), which caused the Great American Interchange of species (Webb, 1985), and also range expansions of many dung beetle taxa, such as the Scarabaeinae (A.L.V. Davis & Scholtz, 2001). A certain number of current Neotropical Aphodiini species are the likely survivors of a specialized and hardly diversified fauna previously present at this region.

The principal characteristic of the Australian continent has been its prolonged isolation from the rest of the regions, and the lack of placental mammals until the Pleistocene (2.5 Ma-10 ka; Cox, 2000). Hence, older Australian Aphodiini lineages would have been adapted to exploiting excrements from marsupials. Land connections during the Pleistocene between Eurasia and Australia probably allowed the dispersal of mammals towards the latter region, together with a number of Aphodiini species associated with them. The mass extinction of monotremes and marsupials (Murray, 1984) may have caused the extinction of some endemic Aphodiini, but newcomer Aphodiini species may have proliferated with the advent of soft-fibrous droppings.

Middle-late Pleistocene (420-18 ka) glacial-interglacial cycles (Imbrie et al., 1993), could have played an important role as modifying factors of Aphodiini distributions and diversity, especially in the Holarctic regions (Hanski, 1991b). Fossil evidence (Coope, 1978, 1990; Coope & Angus, 1975; Lindroth, 1948) confirms that insects underwent range shifts during the Pleistocene in relation to changes in climate and vegetation. Thus, in the Northern

Composition and Distribution Patterns of Species at a Global Biogeographic Region Scale:

newborn daughter and future 'bug lover' (I hope so…).

Verlag, ISBN<PHONE_NUMBER>, New York, NY

Vol. 3, pp. 75-84, ISSN 1366-638X

University, Bowling Green, OH

0471906913, New York, NY

www.catalogueoflife.org/col/

Biology, Vol. 44, pp. 413-424, ISSN 1540-7063

Göttinger Studien, Vol. 3, pp. 595-708

**7. References**

0307-6946

2933

Biogeography of Aphodiini Dung Beetles (Coleoptera, Scarabaeidae) Based on Species Geographic... 351

indirectly provided most of the Aphodiini description references by means of the bibliography databases they have compiled. I wish to dedicate this chapter to Julieta, my

Ádám, L. (1994). A check-list of the Hungarian Scarabaeoidea with the description of ten new taxa. *Folia Entomologica Hungarica*, Vol. 55, pp. 5-17, ISSN 0373-9465 Almeida-Neto, M., Guimarães, P., Guimarães, Jr.P.R., Loyola, R.D. & Ulrich, W. (2008). A

Andresen, E. (2002). Dung beetles in a Central Amazonian rainforest and their ecological

Arillo, A. & Ortuño, V.M. (2008). Did dinosaurs have any relation with dung-beetles (the

Atmar, W. & Patterson, B.D. (1993). The measure of order and disorder in the distribution of species in fragmented habitat. *Oecologia*, Vol. 96, pp. 373-382, ISSN 0029-8549 Bailey, R.G. (1998). *Ecoregions: the ecosystem geography of the oceans and continents*. Springer

Baraud, J. (1985). *Coleóptères Scarabaeoidea. Faune du Nord de l'Afrique, du Maroc au Sinaï. Encyclopédie Entomologique 46*, Lechevalier, ISBN 272050517X, Paris, France Baraud, J., (1992). *Coléoptères Scarabaeoidea d'Europe. Faune de France 78*. Féderation Française

Barbero, E.; Palestrini, C. & Rolando, A. (1999). Dung beetle conservation: effects of habitat

Bergmann, C. (1847). Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse.

Bernon, G. (1981). *Species abundance and diversity of the Coleoptera component of a South African*

Birks, H.J.B. (1986). Late-Quaternary biotic changes in terrestrial and lacustrine

Bisby, F.A.; Roskov, Y.R.; Orrell, T.M.; Nicolson, D.; Paglinawan, L.E.; Bailly, N.; Kirk, P.M.;

Blanckenhorn, W.U. & Demont, M. (2004). Bergmann and converse Bergmann latitudinal

Bordat, P. (1999) *Ammoecioides*, nouveau genre et ses espèces (Coleoptera, Scarabaeoidea, Aphodiidae). *Nouvelle Revue d'Entomologie*, Vol. 16, pp. 161-182, ISSN 0374-9797

and resource selection (Coleoptera: Scarabaeoidea). *Journal of Insect Conservation*,

*cow dung community, and associated insect predators*. PhD Thesis, Bowling Green State

environments, with particular reference to north-west Europe. In: *Handbook of Holocene palaeoecology and palaeohydrology*, B.E. Berglund (Ed.), 39-56, Wiley, ISBN

Bourgoin, T.; Baillargeon, G. & Ouvrard, D. (2011). Species 2000 & ITIS Catalogue of Life, 26th July 2011. In: *Species 2000*, 15.08.2011, Available from:

clines in arthropods: two ends of a continuum? Integrative and Comparative

des Sociétés de Sciences Naturelles, ISBN<PHONE_NUMBER>, Paris, France

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role as secondary seed dispersers. *Ecological Entomology*, Vol. 27, pp. 257-270, ISSN

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Hemisphere, Aphodiini should have shifted their distribution ranges southwards during glacial periods, and northwards during interglacials (Cabrero-Sañudo & Lobo, 2006). The mixing of fauna should then have been more frequent among Old World regions and between New World regions, as the ice sheets interrupted the interchanges across Beringia. The Oriental region probably was isolated by the glaciated ice sheets of mountain ranges, and therefore may not have served as a refuge for northern Aphodiini lineages. This possibly favoured the role of the Palaeotropical region as a refuge and recent diversification centre for a great number of Old World Aphodiini lineages, helping explain its high levels of endemism.

During the Holocene (10 ka to the present), cattle, horses and other domesticated animals, as well as human movements, have contributed particularly to the dispersion of Aphodiini. Human-induced changes have been especially important in the Western Palaearctic during the late Quaternary (Birks, 1986; Hanski, 1991b) and over the past few centuries for the other regions (P.A. Delcourt & H.R. Delcourt, 1987; Doube et al., 1991; Kohlmann, 1991; Mirol et al., 2003). Recent changes in soil uses, modifications through livestock and agricultural practices, chemical contamination and urban development have negatively influenced Aphodiini diversity, distribution and populations (Barbero et al., 1999; Gittins & Giller, 1999; Gittings et al., 1994; Hutton & Giller, 2003; Lobo et al., 1997, 2001, 2006; Lumaret, 1986, 1990; Lumaret & Kirk, 1911; Lumaret & Martínez, 2005; Lumaret et al., 1993; Romero-Samper & Lobo, 2006; Roslin & Koivunen, 2001).

#### **5. Conclusions**

Even when phylogenetic information is available, the lack of comprehensive fossil information and shifts in the distribution of species makes it extremely difficult to disentangle past dispersal patterns, complicating the formulation of reliable hypotheses that allow explanation of current distribution by means of past events (Gaston & Blackburn, 1996; Losos & Glor, 2003; Pulquério & Nichols, 2007; Thomas et al., 2006). One of the main challenges for biogeographers continues to be the formulation of reliable hypotheses about the underlying historical processes based on present-day biogeographical data. In this chapter, through statistical tests and a simple methodology, I have attempted to show that it is possible to identify signatures of the processes from which current distributional patterns originated, and to elucidate a likely past biogeography of the Aphodiini.

In relation to Aphodiini, it has been suggested that Palaeotropical and Palaeartic regions, together with the Nearctic, have been primary diversification centres after the break-up of Pangea. Consequently, these three regions may have acted jointly as macroevolutionary source regions in different times, also sustaining migration processes and extinctions that obscure linkage between past events and present-day distributions. Future phylogenetic data are needed to more completely resolve taxonomic issues and confirm internal relationships among the Aphodiini lineages. Such results also will help to confirm or to reject the hypotheses herein presented.

#### **6. Acknowledgment**

This chapter was supported by a MCI project (CGL 2010-16944) and an UCM-BSCH project (GR35/10-a). I thank Fernando Zagury Vaz de Mello and Paul Schoolmeesters, who indirectly provided most of the Aphodiini description references by means of the bibliography databases they have compiled. I wish to dedicate this chapter to Julieta, my newborn daughter and future 'bug lover' (I hope so…).

#### **7. References**

350 Global Advances in Biogeography

Hemisphere, Aphodiini should have shifted their distribution ranges southwards during glacial periods, and northwards during interglacials (Cabrero-Sañudo & Lobo, 2006). The mixing of fauna should then have been more frequent among Old World regions and between New World regions, as the ice sheets interrupted the interchanges across Beringia. The Oriental region probably was isolated by the glaciated ice sheets of mountain ranges, and therefore may not have served as a refuge for northern Aphodiini lineages. This possibly favoured the role of the Palaeotropical region as a refuge and recent diversification centre for a great number of Old World Aphodiini lineages, helping explain its high levels of

During the Holocene (10 ka to the present), cattle, horses and other domesticated animals, as well as human movements, have contributed particularly to the dispersion of Aphodiini. Human-induced changes have been especially important in the Western Palaearctic during the late Quaternary (Birks, 1986; Hanski, 1991b) and over the past few centuries for the other regions (P.A. Delcourt & H.R. Delcourt, 1987; Doube et al., 1991; Kohlmann, 1991; Mirol et al., 2003). Recent changes in soil uses, modifications through livestock and agricultural practices, chemical contamination and urban development have negatively influenced Aphodiini diversity, distribution and populations (Barbero et al., 1999; Gittins & Giller, 1999; Gittings et al., 1994; Hutton & Giller, 2003; Lobo et al., 1997, 2001, 2006; Lumaret, 1986, 1990; Lumaret & Kirk, 1911; Lumaret & Martínez, 2005; Lumaret et al., 1993; Romero-

Even when phylogenetic information is available, the lack of comprehensive fossil information and shifts in the distribution of species makes it extremely difficult to disentangle past dispersal patterns, complicating the formulation of reliable hypotheses that allow explanation of current distribution by means of past events (Gaston & Blackburn, 1996; Losos & Glor, 2003; Pulquério & Nichols, 2007; Thomas et al., 2006). One of the main challenges for biogeographers continues to be the formulation of reliable hypotheses about the underlying historical processes based on present-day biogeographical data. In this chapter, through statistical tests and a simple methodology, I have attempted to show that it is possible to identify signatures of the processes from which current distributional patterns

In relation to Aphodiini, it has been suggested that Palaeotropical and Palaeartic regions, together with the Nearctic, have been primary diversification centres after the break-up of Pangea. Consequently, these three regions may have acted jointly as macroevolutionary source regions in different times, also sustaining migration processes and extinctions that obscure linkage between past events and present-day distributions. Future phylogenetic data are needed to more completely resolve taxonomic issues and confirm internal relationships among the Aphodiini lineages. Such results also will help to confirm or to

This chapter was supported by a MCI project (CGL 2010-16944) and an UCM-BSCH project (GR35/10-a). I thank Fernando Zagury Vaz de Mello and Paul Schoolmeesters, who

originated, and to elucidate a likely past biogeography of the Aphodiini.

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**5. Conclusions**

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### *Edited by Lawrence Stevens*

Global Advances in Biogeography brings together the work of more than 30 scientific authorities on biogeography from around the world. The book focuses on spatial and temporal variation of biological assemblages in relation to landscape complexity and environmental change. Global Advances embraces four themes: biogeographic theory and tests of concepts, the regional biogeography of individual taxa, the biogeography of complex landscapes, and the deep-time evolutionary biogeography of macrotaxa. In addition, the book provides a trove of new information about unusual landscapes, the natural history of a wide array of poorly known plant and animal species, and global conservation issues. This book is well illustrated with numerous maps, graphics, and photographs, and contains much new basic biogeographical information that is not available elsewhere. It will serve as an invaluable reference for professionals and members of the public interested in global biogeography, evolution, taxonomy, and conservation.

Global Advances in Biogeography

Global Advances in

Biogeography

*Edited by Lawrence Stevens*

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