Quantity and quality of seed dispersal by a large arboreal frugivore in small and large Atlantic forest fragments

Abstract

Seed dispersal is a key process driving the structure, composition, and regeneration of tropical forests. Larger frugivores play a crucial role in community structuring by dispersing large seeds not dispersed by smaller frugivores. We assessed the hypothesis that brown howler monkeys (Alouatta guariba clamitans) provide seed dispersal services for a wide assemblage of plant species in both small and large Atlantic forest fragments. Although fruit availability often decreases in small fragments compared with large ones, we predicted that brown howlers are efficient seed dispersers in quantitative and qualitative terms in both forest types given their high dietary flexibility. After a 36-month study period and 2,962 sampling hours, we found that howlers swallowed and defecated intact the vast majority of seeds (96%-100%) they handled in all study sites. Overall, they defecated ca. 315,600 seeds belonging to 98 species distributed in eight growth forms. We estimated that each individual howler dispersed an average of 143 (SD = 49) seeds >2 mm per day or 52,052 (SD = 17,782) seeds per year. They dispersed seeds of 58% to 93% of the local assemblages of fleshy-fruit trees. In most cases, the richness and abundance of seed species dispersed was similar between small and large fragments. However, groups inhabiting small fragments tended to disperse a higher diversity of seeds from rarely consumed fruits than those living in large fragments. We conclude that brown howlers are legitimate seed dispersers for most fleshy-fruit species of the angiosperm assemblages of their habitats, and that they might favor the regeneration of Atlantic forest fragments with the plentiful amount of intact seeds that they disperse each year.

Supplemented howler monkeys eat less wild fruits, but do not change their activity budgets

“…This strategy of maintaining a nutritional balance between supplemented and wild foods was also reported for baboons ( Papio hamadryas : Boug et al, ). A potential reduction in the dispersal of seeds of native species together with the promotion of the dispersal of seeds of alien, potentially invasive, species are undesired side effects of the reduced consumption of wild fruits due to the ingestion of cultivated fruits (Chaves et al, ), as this ecosystem role change can alter the vegetation structure of habitat remnants (Sengupta, McConkey, & Radhakrishna, ).…”

“…The adaptation of these highly arboreal monkeys has been related to the adjustment of their folivorous‐frugivorous diet (Crockett & Eisenberg, ; Neville, Glander, Braza, & Rylands, ) to resource availability (Bicca‐Marques, ; Chaves & Bicca‐Marques, ). They can exploit food that is common in anthropic environments, such as shrubs, lianas, and alien fruit trees (Asensio et al, ; Bicca‐Marques & Calegaro‐Marques, ; Chaves & Bicca‐Marques, , , ; Chaves, Bicca‐Marques, & Chapman, ), and even bird eggs (Bicca‐Marques, Muhle, Prates, Oliveira, & Calegaro‐Marques, ; Bicca‐Marques, Silveira, Martins, & Rabelo, ). A high level of resting (usually >65%) and a low level of social interaction (<4%) characterize the activity budget of howlers (Bicca‐Marques, ; Di Fiore, Link, & Campbell, ).…”

Howler monkey tolerance to habitat shrinking: Lifetime warranty or death sentence?

“…Therefore, restoring and reconnecting small habitat patches to promote metapopulation functioning can increase the odds of the persistence of a species in highly fragmented landscapes (Bonilla‐Sánchez et al, ; Boyle & Smith, ; Chapman et al, ; Cristóbal‐Azkarate & Arroyo‐Rodríguez, ; Galán‐Acedo et al, ; Mandujano et al, ; Marsh et al, ; Oklander et al, ; Silva & Bicca‐Marques, ). It is also critical to highlight that primates sometimes represent the largest remaining frugivores of the original fauna in these fragmented landscapes (Camaratta, Chaves, & Bicca‐Marques, ), playing important roles as seed dispersers and promoters of forest regeneration (Bufalo, Galetti, & Culot, ; Chaves, Bicca‐Marques, & Chapman, ).…”

Hematological and serum biochemistry data on southern brown howler monkeys (Alouatta guariba clamitans) in captivity in Brazil

“…[10][11][12][13][14] Howlers are considered a yellow fever sentinel species, indicating the circulation of the virus through epizootics. 15 Although ecological and behavioral aspects of these species have been broadly studied, [16][17][18][19][20][21][22][23] information on physiological parameters is scarce in the literature. 9,24 In this study, we determined some hematological and serum biochemistry parameters of a captive population of the A guariba clamitans subspecies in the South region of Brazil to provide standard base parameters for the optimal maintenance of this subspecies under captive conditions.…”