3.3.1 Alouatta caraya (Humboldt, 1812)

Type: No type preserved.

Type locality: Paraguay.

Common name: Black and gold howler, Paraguayan howler.

This species has a broad distribution including Brazil (Pantanal, and parts of the Cerrado and Caatinga), northern Argentina, Paraguay, and Bolivia (Fig. 3.1). Most authors have recognized this taxon as a full species given the presence of a distinct sexual dichromatism: males are mostly black and females have a yellowish or brindled tawny color (Groves 2001). Morphological analyses of the hyoid bone in males distinguish this species from other howlers, particularly by the lack of a tentorium (see Hershkovitz 1949; Gregorin 2006). Alouatta caraya has a diploid number of 2n = 52, which does not vary in specimens from distinct localities (de Oliveira et al. 2002). This species presents a sex chromosome system of X 1 X 1 X 2 X 2 /X 1 X 2 Y 1 Y 2 (Mudry et al. 2001; de Oliveira et al. 2002), also observed in taxa of the A. seniculus group (A. macconnelli, A. sara, A. arctoidea) (Seuánez et al. 2005) and in A. pigra (Steinberg et al. 2008). This quadrivalent sex chromosome system differs from those of A. guariba, A. belzebul, and A. palliata (see chapter by Mudry et al. 2015). Chromosome painting with human chromosome probes suggests that the rearrangements that gave rise to this system in A. caraya and the A. seniculus group may have a single origin (Mudry et al. 2001), whereas the origin of the A. pigra quadrivalent sex chromosome system seems to be separate (see chapter by Mudry et al. 2015). The possible single origin of the sex chromosome system between A. caraya and the A. seniculus group suggests that A. caraya may have a close phylogenetic affinity with the Amazonian red howler taxa. Indeed, A. caraya shares one chromosome painting association pattern with the red howlers (A. seniculus, A. sara, A. macconnelli) and A. guariba, but not with A. belzebul (see Stanyon et al. 2011). A phylogenetic reconstruction by de Oliveira et al. (2002) based on parsimony analysis of chromosomal changes in different species of Alouatta places A. caraya as a sister group of A. belzebul, but phylogenetic studies based on mitochondrial and/or nuclear sequence data include A. caraya in a clade with species from the A. seniculus group (Cortés-Ortiz et al. 2003; Nascimento et al. 2005; Perelman et al. 2011), or show this species as basal to all howlers (e.g., Bonvicino et al. 2001). The actual phylogenetic position of A. caraya in the genus may require additional multilocus analyses that contain representatives of all the main lineages of howler monkeys, and include multiple samples from distinct geographic localities for each taxon.

Nascimento et al. (2005, 2007) and Ascunce et al. (2007) analyzed interspecific variation in A. caraya using mitochondrial DNA markers (the control region and the cytochrome b gene). In both cases they found evidence of divergent mitochondrial haplotypes consistent with individuals from different geographical regions (Mato Grosso, Brazil vs. Santa Cruz, Bolivia vs. Goiás, Brazil in Nascimento et al. 2005, and Mato Grosso, Brazil vs. northern Argentina/Paraguay vs. Goiás, Brazil in Ascunce et al. 2007). However, some of these divergent haplotypes can be found in both Argentina and Brazil and therefore they may be the result of ancestral polymorphism or the expansion and secondary contact of formerly allopatric populations (Ascunce et al. 2007). The structuring of mitochondrial haplotypes in these localities suggests that these populations could represent different subspecies. Whether these populations constitute different taxa, however, remains to be explored with further studies that include samples of individuals from a wider range of locations.