Sistema social de grupos mistos de espécies de bugios (Alouatta Caraya e Alouatta Clamitans) e potenciais híbridos no Alto Rio Paraná, Sul do Brasil

Abstract

Zonas híbridas são ambientes complexos e com alta variabilidade, que são balanceados por misturas e seleção. O pouco conhecimento sobre a hibridação entre Alouatta caraya e A. clamitans dificulta o entendimento do fenômeno na evolução das espécies do gênero Alouatta e o quanto a fragmentação pode influenciar. Não se sabe como a coexistência entre duas espécies morfologicamente diferentes, mas ecologicamente similares, afetaria seus parâmetros populacionais e seus sistemas sociais. Estudos ajudariam a entender os custos e as vantagens das interações nas raras áreas de simpatria. Aqui se estudou o sistema social (organização social, sistema de acasalamento e estrutura social) de grupos mistos e híbridos potenciais em um fragmento no Alto Rio Paraná, sul do Brasil, entre outubro de 2006 e junho de 2008 (1618 h em campo). Alouatta clamitans foi a espécie mais abundante, o que pode relacionar-se ao tipo de habitat (Mata Atlântica). A proporção de híbridos potenciais foi substancial (semelhante à de A. caraya), sendo a maior reportada para as zonas híbridas conhecidas das duas espécies, sugerindo influência da fragmentação na incidência de híbridos e de grupos mistos. Os grupos não foram maiores do que os monoespecíficos, sugerindo algum grau de competição em simpatria. Desvios ocorreram: grupos mistos apresentaram menor proporção de imaturos por FA do que os monoespecíficos, sugerindo menor aptidão deste tipo de associação; a classe mais abundante foi MA de A. clamitans; houve um baixo número de FA por grupo; e uma tendência para um maior número de FA entre os híbridos potenciais, sugerindo Regra de Haldane. Os híbridos foram polimórficos em coloração, assemelhando-se mais à A. clamitans e, também de acordo com a regra acima, alguns pareceram ginandromórficos. Grupos mistos foram instáveis, pouco coesos e dinâmicos espácio-temporalmente. Em um deles houve emigrações e indivíduos satélites de ambas as espécies. O grupo se deteriorou sem haver nascimentos. Este grupo possuiu área de vida transgredida por outros grupos e foi mais suplantado durante os confrontos. Outro grupo apresentou constituição estável e nascimentos, com dinâmica de fissão-fusão dos subgrupos de A. caraya e A. clamitans. Os subgrupos utilizaram a mesma área e a defenderam concomitantemente, suplantaram mais grupos em confrontos e não apresentaram área transgredida, sugerindo vantagens de associação entre heteroespecíficos. Quando associados, o grupo apresentou maior taxa de interação social (principalmente devido aos imaturos), mas não de descanso, deslocamento e alimentação, sugerindo baixo custo de associação. Indivíduos de uma espécie que mais se associaram a outra foram machos subordinados ou migrantes que foram tolerados pelos machos ou solicitados pelas fêmeas da outra espécie, obtendo vantagens sexuais. O grupo mais instável foi promíscuo, realizando mais cópulas extragrupo; e o mais estável foi poliginiândrico, com a maioria das cópulas interespecíficas. Comportamentos afiliativos e reprodutivos envolveram mais híbridos potenciais, com aparente preferência destes à espécie confenotípica A. clamitans. Estes comportamentos foram mais raros entre heteroespecíficos. Cópulas interespecíficas seguiram um padrão que está de acordo com o modelo baseado em escolhas de parceiros sexuais pelas fêmeas: foram sempre entre fêmeas da espécie mais rara com machos da espécie mais abundante. Comportamentos agonísticos intragrupais foram freqüentes, principalmente em contexto sexual, e ocorreram mais entre machos de A. clamitans, seguidos dos híbridos potenciais, e menos entre heteroespecíficos. O grupo instável apresentou como indivíduo dominante uma fêmea híbrida e o grupo estável apresentou codominância entre um macho de cada espécie, sendo a fêmea híbrida dominante sobre a fêmea de A. caraya. Encontros intergrupais sempre envolveram agonismo e o principal contexto foi o sexual. A maioria dos encontros entre conspecíficos escalonou para rugidos, sendo um número intermediário com híbridos potenciais, e menor entre heteroespecíficos. Um grupo de supostos híbridos venceu todos os confrontos. Este resultado, aliado às altas posições hierárquicas das fêmeas supostamente híbridas sugerem vigor híbrido. Híbridos de Alouatta podem ser mais comuns em fragmentos pequenos, cujas populações sofrem aglomeramento, relaxando as barreiras comportamentais. Nestas áreas, os custos para migrantes entrarem em grupos de conspecíficos podem ser maiores do que entrarem em grupos de heteroespecíficos, e grupos pequenos ou vestigiais de uma espécie podem se juntar a grupos da outra espécie formando grupos mistos. Embora a simpatria e a hibridação possam ser fenômenos naturais, a coexistência entre as duas espécies em um fragmento pequeno pareceu alterar a estrutura sexo-etária, influenciando uma maior disputa sexual. A coexistência das duas espécies e híbridos também pareceu produziu alta variabilidade de comportamentos, sistemas e associações, mas poucas foram as novidades observadas e, de fato, os grupos mistos funcionaram com padrões de atividade, dietas e sistemas sociais típicos de Alouatta. Por fim, os híbridos potenciais foram socialmente aceitos e viáveis, e desempenharam funções dentro da sociedade na qual estão integrados. Portanto, atenção conservacionista deve ser dada já que a degradação ambiental pode aumentar a hibridação entre os dois táxons, e os híbridos funcionais, com baixa discriminação, podem ajudar a diluir as populações, substituindo as espécies parentais em suas sociedades locais. A fertilidade e a viabilidade social dos morfotipos híbridos podem contribuir para que as zonas híbridas avancem com a contínua degradação dos ambientes florestais.

Hybrid zones are complex and highly variable environments, which are balanced by crosses and selection. The sparse knowledge of hybridization between the two howler species, Alouatta caraya and A. clamitans, impedes understanding of this phenomenon in the evolution of species of the genus Alouatta, and the degree to which it may be influenced by habitat fragmentation. It is not known how coexistence between these two morphologically different but ecologically similar species might affect their population parameters and social systems. Studies will aid in understanding the costs and advantages of the interactions in the few areas of sympatry. The social system (social organization, mating system, and social structure) of mixed groups consisting of both species and putative hybrids was studied in a forest fragment on the Upper Paraná River in southern Brazil, from October 2006 through June 2008 (1618 h in the field). Alouatta clamitans was the more abundant species, which may be a result of the kind of habitat (Atlantic Forest). The proportion of putative hybrids was substantial (similar to the proportion of A. caraya), and is the highest yet reported for the known hybrid zones of these two species, suggesting that the fragmentation affected the incidence of hybrids and mixed groups. The mixed groups were not larger than the monospecific groups, suggesting some degree of competition in sympatry. There were some differences: mixed groups showed a smaller proportion of immatures to AF (adult females) than did the monospecifics, suggesting a lower fitness of this type of association; the most abundant class was AM (adult males) of A. clamitans; and there was a small number of AF per group, with a bias toward AF among the putative hybrids, suggesting Haldane’s Rule. The putative hybrids were polymorphic in coloration, and more closely resembled A. clamitans. Some of them appeared to be gynandromorphic, also in accord with Haldane’s Rule. The mixed groups were unstable and spatio-temporally dynamic. Both of them had low cohesion. In one of them, there were emigrations and satellite individuals of both species, and the group deteriorated, with no births. Other groups transgressed into the home range of this group, and the group was more often supplanted during confrontations. Another group showed a stable composition and births, with a system of fission-fusion of the subgroups of A. caraya and A. clamitans. The subgroups used the same home range and defended it concurrently, supplanting more groups in confrontations, and no other group transgressed into their area, suggesting that the association between heterospecifics conferred some advantages. When the subgroups were together, the group showed a higher rate of social interaction (mainly because of interactions between immatures and AM), but not of resting, traveling, and feeding, suggesting that the cost of association was low. The individuals of one species that most often associated with the other species were subordinate or migrant males, which were tolerated by males or solicited by females of the other species, obtaining sexual advantages. The most unstable group was promiscuous, performing more extra-group copulations; the most stable was polygynandrous, with the majority of copulations interspecific. Affiliative and reproductive behaviors involved more hybrids, which apparently preferred the conphenotypic species A. clamitans. These behaviors were rarer between heterospecifics. The pattern of interspecies copulations agreed with the model based on a female-choice mating system: these were always between females of the less-abundant species and males of the more-abundant species. Intra-group agonistic behaviors were frequent, principally in a sexual context, and occurred most often between males of A. clamitans, next most often between putative hybrids, and least often between heterospecifics. In the unstable group, the dominant individual was a hybrid female; in the stable group, a male of each species was co-dominant, with the hybrid female dominant over the female of A. caraya. Inter-group encounters always involved agonism, mainly in a sexual context. Most of the encounters between conspecifics escalated to roaring; an intermediate number of encounters between hybrids reached this stage, and even fewer between heterospecifics. One group of putative hybrids prevailed in all the confrontations. These observations, together with the high hierarchical positions of the putative hybrid females, suggest hybrid vigor. Hybrids of Alouatta may be more common in small fragments where the populations become crowded and behavioral barriers are relaxed. In these areas, the costs for migrants to join groups of conspecifics may be higher than to join groups of heterospecifics, and small or vestigial groups of one species may join a group of the other species, forming a mixed group. Although sympatry and hybridization may be natural phenomena for howlers, the coexistence between the two species in a small fragment appeared to alter the age-sex structure, intensifying sexual competition. The coexistence of the two species and their hybrids also appeared to produce a high variability of behaviors, systems, and associations, but few novelties were observed, and in fact the mixed groups functioned with the time budget, diet, and social systems typical of Alouatta. In the end, the presumed hybrids were socially accepted and viable, and functioned within the society into which they were integrated. Therefore, attention should be given to conservation, since environmental degradation may increase the rate of hybridization between the two taxa, and the functional hybrids, which show little discrimination between the species, may help to dilute the populations, replacing the parental species in their local societies. The fertility and social viability of the hybrid morphotypes may contribute to the advancement of the hybrid zones as their forest environments continue to be degraded.

Abstract: Hybrid zones are complex and highly variable environments, which are balanced by crosses and selection. The sparse knowledge of hybridization between the two howler species, Alouatta caraya and A. clamitans, impedes understanding of this phenomenon in the evolution of species of the genus Alouatta, and the degree to which it may be influenced by habitat fragmentation. It is not known how coexistence between these two morphologically different but ecologically similar species might affect their population parameters and social systems. Studies will aid in understanding the costs and advantages of the interactions in the few areas of sympatry. The social system (social organization, mating system, and social structure) of mixed groups consisting of both species and putative hybrids was studied in a forest fragment on the Upper Paraná River in southern Brazil, from October 2006 through June 2008 (1618 h in the field). Alouatta clamitans was the more abundant species, which may be a result of the kind of habitat (Atlantic Forest). The proportion of putative hybrids was substantial (similar to the proportion of A. caraya), and is the highest yet reported for the known hybrid zones of these two species, suggesting that the fragmentation affected the incidence of hybrids and mixed groups. The mixed groups were not larger than the monospecific groups, suggesting some degree of competition in sympatry. There were some differences: mixed groups showed a smaller proportion of immatures to AF (adult females) than did the monospecifics, suggesting a lower fitness of this type of association; the most abundant class was AM (adult males) of A. clamitans; and there was a small number of AF per group, with a bias toward AF among the putative hybrids, suggesting Haldane’s Rule. The putative hybrids were polymorphic in coloration, and more closely resembled A. clamitans. Some of them appeared to be gynandromorphic, also in accord with Haldane’s Rule. The mixed groups were unstable and spatio-temporally dynamic. Both of them had low cohesion. In one of them, there were emigrations and satellite individuals of both species, and the group deteriorated, with no births. Other groups transgressed into the home range of this group, and the group was more often supplanted during confrontations. Another group showed a stable composition and births, with a system of fission-fusion of the subgroups of A. caraya and A. clamitans. The subgroups used the same home range and defended it concurrently, supplanting more groups in confrontations, and no other group transgressed into their area, suggesting that the association between heterospecifics conferred some advantages. When the subgroups were together, the group showed a higher rate of social interaction (mainly because of interactions between immatures and AM), but not of resting, traveling, and feeding, suggesting that the cost of association was low. The individuals of one species that most often associated with the other species were subordinate or migrant males, which were tolerated by males or solicited by females of the other species, obtaining sexual advantages. The most unstable group was promiscuous, performing more extra-group copulations; the most stable was polygynandrous, with the majority of copulations interspecific. Affiliative and reproductive behaviors involved more hybrids, which apparently preferred the conphenotypic species A. clamitans. These behaviors were rarer between heterospecifics. The pattern of interspecies copulations agreed with the model based on a female-choice mating system: these were always between females of the less-abundant species and males of the more-abundant species. Intra-group agonistic behaviors were frequent, principally in a sexual context, and occurred most often between males of A. clamitans, next most often between putative hybrids, and least often between heterospecifics. In the unstable group, the dominant individual was a hybrid female; in the stable group, a male of each species was co-dominant, with the hybrid female dominant over the female of A. caraya. Inter-group encounters always involved agonism, mainly in a sexual context. Most of the encounters between conspecifics escalated to roaring; an intermediate number of encounters between hybrids reached this stage, and even fewer between heterospecifics. One group of putative hybrids prevailed in all the confrontations. These observations, together with the high hierarchical positions of the putative hybrid females, suggest hybrid vigor. Hybrids of Alouatta may be more common in small fragments where the populations become crowded and behavioral barriers are relaxed. In these areas, the costs for migrants to join groups of conspecifics may be higher than to join groups of heterospecifics, and small or vestigial groups of one species may join a group of the other species, forming a mixed group. Although sympatry and hybridization may be natural phenomena for howlers, the coexistence between the two species in a small fragment appeared to alter the age-sex structure, intensifying sexual competition. The coexistence of the two species and their hybrids also appeared to produce a high variability of behaviors, systems, and associations, but few novelties were observed, and in fact the mixed groups functioned with the time budget, diet, and social systems typical of Alouatta. In the end, the presumed hybrids were socially accepted and viable, and functioned within the society into which they were integrated. Therefore, attention should be given to conservation, since environmental degradation may increase the rate of hybridization between the two taxa, and the functional hybrids, which show little discrimination between the species, may help to dilute the populations, replacing the parental species in their local societies. The fertility and social viability of the hybrid morphotypes may contribute to the advancement of the hybrid zones as their forest environments continue to be degraded.