Urban growth threatens the lowland Amazonian Manaus harlequin frog which represents an evolutionarily significant unit within the genus Atelopus (Amphibia: Anura: Bufonidae)

Abstract

The Manaus harlequin frog is an evolutionarily significant clade within the Atelopus hoogmoedi species complex. Analyses of 16S and COI concatenated sequences support Atelopus from the Manaus region as an evolutionary significant unit, sister of all species of a Guiana Shield clade. A previous study showed that subtle changes in stream characteristics influence the Manaus harlequin frog occurrence and density variation at local‐scale in a reserve on the outskirts of Manaus. As deforestation is approaching areas where the Manaus harlequin frog occurs, we asked how site and landscape heterogeneity influence the geographic boundaries, occurrence patterns, and density variation of the Manaus harlequin frog. We searched for the frog in 80 plots that measured 250 m by 4 m on banks of first‐ to third‐order streams during the rainy seasons in 2012–2013 and 2016–2019. The plot distribution covered all likely areas of occurrence of the Manaus harlequin frog and extended to the areas where it is substituted by its geographically closest relative on the Guiana Shield. Ecological drivers related to climate, flooding events, and forest structure apparently restrict the Manaus harlequin frog to a patchy distribution in a narrow portion of the interfluve between the Negro and Uatuma Rivers. Densities of individuals varied in response to subtle changes in floodplain and stream characteristics. The Manaus harlequin frog is associated with a very specific habitat that is directly affected by the growth of Manaus, the largest city in Amazonia. We conclude that it is endangered and urgent actions are required for its conservation.

Out of Bound: A New Threatened Harlequin Toad (Bufonidae, Atelopus) from the Outer Borders of the Guiana Shield in Central Amazonia Described through Integrative Taxonomy

“…Anapu, A. barbotini "B", A. oxapampae, A. tricolor, and R. marina (IDs 7; 14; 26-28 in Table 1, respectively). Overall, we obtained the same phylogenetic relationships and statistical support as obtained by Jorge et al [29], with a slight difference regarding the relationships of the French Guiana species, which is likely because of the addition of new samples (see Results section, Section 3.1). Phylogenetic relationships were estimated using Maximum Likelihood (ML) and Bayesian Inference (BI).…”

“…Another Atelopus species known from Brazil is A. hoogmoedi, which is distributed in the states of Amapá and Pará, but its type locality is in French Guiana. As is the case for several of its congeners, A. manauensis has a small area of occurrence (approximately 4500 km 2 ) and is critically threatened by urban expansion of the largest city in Brazilian Amazonia-Manaus [29].…”

“…For example, the pathogenic fungus Batrachochytrium dendrobatidis (BD) has caused the extinction of numerous species of Atelopus [58], and the deforestation that is reaching Central Amazonia via highway BR-174 (Manaus-Boa Vista) could very likely facilitate its invasion into the area of occurrence of the new species. Although BD has not been found in populations of A. manauensis [29], an ongoing study indicates that BD infection would cause high mortality rates for the new species [59]. In addition to the threat of BD, the urban expansion of Manaus and other nearby cities is fragmenting areas with aggregations of individuals of A. manauensis.…”

“…nov. is limited to the interfluve between the Negro and the Uatumã Rivers in the Alter do Chão formation (absent from the Guiana Shield and the Trombetas Group), within a narrow altitudinal range (61-125 m a.s.l. ), and restricted to the micro-interfluve between the east bank of the Cuieiras River and the west bank of the Urubu River (Figure 10), which are tributaries of the Negro and the Amazon Rivers, respectively [29]. In this region, Atelopus manauensis sp.…”

“…Suggested partitions and models were as follows: 16S = GTR + G; COI\1 = SYM; COI\2 = F81; COI\3 = HKY. We used for phylogenetic inference the same 20 16S and all COI sequences used in Jorge et al [29], including those sequences of the new species, only adding eight new sequences, as follows: A. hoogmoedi (three sequences from the municipality of Monte Alegre, state of Pará, Brazil-IDs 8-10 in Table 1), A. sp. Anapu, A. barbotini "B", A. oxapampae, A. tricolor, and R. marina (IDs 7; 14; 26-28 in Table 1, respectively).…”