'Phototaxis' in the absence of light? Locomotory patterns in unionid mussels.

Locomotion in benthic invertebrates can strongly affect habitat selection and ecosystem nutrient cycling. In the case of freshwater mussels, the drivers of locomotion are largely unresolved. Our aim was to assess the influence of light presence and intensity on the locomotory behaviour of freshwater mussels in controlled laboratory experiments. The species investigated in our study were Anodonta anatina and Unio pictorum, two widely distributed mussels in European lentic and lotic inland waters. At low algal concentrations, known to be associated with more frequent locomotory activities, we found that both species moved primarily in the absence of light (72.7% of all movements across experiments). However, the movements of both species were directed towards the light source, resembling a net-positive 'phototactic' response but in the absence of light. The distance to the light source, which was negatively correlated to light intensity, had a positive effect on the distance covered in locomotory activities by A. anatina but not by U. pictorum. Intraspecific variation in shell size had no impact on movement distance, indicating that the energetic costs of movement were not a limiting factor. We suggest that the observed movement towards brighter locations helps to enhance food quantity and quality, whilst movement in darkness mitigates predation risks.

The evolution of pair-living, sexual monogamy, and cooperative infant care: Insights from research on wild owl monkeys, titis, sakis, and tamarins.

"Monogamy" and pair bonding have long been of interest to anthropologists and primatologists. Their study contributes to our knowledge of human evolutionary biology and social evolution without the cultural trappings associated with studying human societies directly. Here, we first provide an overview of theoretical considerations, followed by an evaluation of recent comparative studies of the evolution of "social monogamy"; we are left with serious doubts about the conclusions of these studies that stem from the often poor quality of the data used and an overreliance on secondary sources without vetting the data therein. We then describe our field research program on four "monogamous" platyrrhines (owl monkeys, titis, sakis, and tamarins), evaluate how well our data support various hypotheses proposed to explain "monogamy," and compare our data to those reported on the same genera in comparative studies. Overall, we found a distressing lack of agreement between the data used in comparative studies and data from the literature for the taxa that we work with. In the final section, we propose areas of research that deserve more attention. We stress the need for more high-quality natural history data, and we urge researchers to be cautious about the uncritical use of variables of uncertain internal validity. Overall, it is imperative that biological anthropologists establish and follow clear criteria for comparing and combining results from published studies and that researchers, reviewers, and editors alike comply with these standards to improve the transparency, reproducibility, and interpretability of causal inferences made in comparative studies.

Disappearing in the Night: An Overview on Trade and Legislation of Night Monkeys in South and Central America.

The international trade in night monkeys (Aotus spp.), found throughout Central and South America, has been regulated by the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) since 1975. We present a quantitative analysis of this trade from all 9 range countries, over 4 decades, and compare domestic legislation to CITES regulations. Night monkeys were exported from 8 of the 9 habitat countries, totalling 5,968 live individuals and 7,098 specimens, with trade of live individuals declining over time. In terms of species, the most commonly traded was Aotus nancymaae (present in Brazil, Colombia, Peru) followed by A. vociferans (Brazil, Colombia, Ecuador, Peru) and A. zonalis (Colombia, Panama). There was no significant correlation between levels of trade and species' geographic range size or the number of countries in which a species occurs. Five countries have legislation that meets CITES requirements for implementation, whereas the other 4 countries' legislation showed deficiencies. Research conducted in Colombia, Peru, and Brazil suggests significant cross-border trade not captured in official international trade registers. Although international trade has diminished, current trends suggest that populations of rarer species may be under unsustainable pressure. Further research is needed to quantify real trade numbers occurring between habitat countries.

Correlates of genetic monogamy in socially monogamous mammals: insights from Azara's owl monkeys.

Understanding the evolution of mating systems, a central topic in evolutionary biology for more than 50 years, requires examining the genetic consequences of mating and the relationships between social systems and mating systems. Among pair-living mammals, where genetic monogamy is extremely rare, the extent of extra-group paternity rates has been associated with male participation in infant care, strength of the pair bond and length of the breeding season. This study evaluated the relationship between two of those factors and the genetic mating system of socially monogamous mammals, testing predictions that male care and strength of pair bond would be negatively correlated with rates of extra-pair paternity (EPP). Autosomal microsatellite analyses provide evidence for genetic monogamy in a pair-living primate with bi-parental care, the Azara's owl monkey (Aotus azarae). A phylogenetically corrected generalized least square analysis was used to relate male care and strength of the pair bond to their genetic mating system (i.e. proportions of EPP) in 15 socially monogamous mammalian species. The intensity of male care was correlated with EPP rates in mammals, while strength of pair bond failed to reach statistical significance. Our analyses show that, once social monogamy has evolved, paternal care, and potentially also close bonds, may facilitate the evolution of genetic monogamy.

Double effort: Parental behavior of wild Azara's owl monkeys in the face of twins.

In species of mammals that habitually bear single offspring, like most anthropoid primates, the occurrence of twins is expected to impose considerable energetic costs on the caretakers. The question then arises of how caregivers cope with the potentially increased costs of raising twins. These increased costs should lead to differing developmental rates in twins when compared to singletons, and/or to changes in the caregivers' behavior. Likewise, time budgets of parents of singletons are expected to differ from those of adults without offspring. Additionally, if twinning was an adaptive response to favorable ecological conditions, it should be more likely in years with high food abundance. Following the birth in 2011 of two sets of twins in a wild population of pair-living Azara's owl monkeys (Aotus azarae) in Northern Argentina, we used long-term demographic, behavioral, and phenological data to compare (a) the proportion of time that singleton and twin infants were carried by either parent; (b) adult time budgets and ranging behavior in groups with zero, one, or two infants; and (c) the availability of food in 2011 with food availability in other years. Twins, like singletons, were carried nearly exclusively by the male, and they were carried slightly more than singletons, suggesting a relatively inflexible pattern of infant care in the species. Time budgets showed that twin parents foraged more and moved less than singleton parents or groups without infants, despite the fact that phenological data indicate that fruit availability in 2011 was not substantially higher than in some of the other years. Overall, twinning thus presumably increased costs to breeders, especially males, but its effect on animals' long-term reproductive success remains unclear.

Analyses of least cost paths for determining effects of habitat types on landscape permeability: wolves in Poland.

Determining ecological corridors is crucial for conservation efforts in fragmented habitats. Commonly employed least cost path (LCP) analysis relies on the underlying cost matrix. By using Ecological Niche Factor Analysis, we minimized the problems connected with subjective cost assessment or the use of presence/absence data. We used data on the wolf presence/absence in Poland to identify LCPs connecting patches of suitable wolf habitat, factors that influence patch occupancy, and compare LCPs between different genetic subpopulations. We found that a lower proportion of cities and roads surrounds the most densely populated patches. Least cost paths between areas where little dispersal takes place (i.e., leading to unpopulated patches or between different genetic subpopulations) ran through a higher proportion of roads and human settlements. They also crossed larger maximal distances over deforested areas. We propose that, apart from supplying the basis for direct conservation efforts, LCPs can be used to determine what factors might facilitate or hinder dispersal by comparing different subsets of LCPs. The methods employed can be widely applicable to gain more in-depth information on potential dispersal barriers for large carnivores.

Sexual dimorphism in the loud calls of Azara's owl monkeys (Aotus azarae): evidence of sexual selection?

Primates use different types of vocalizations in a variety of contexts. Some of the most studied types have been the long distance or loud calls. These vocalizations have been associated with mate defense, mate attraction, and resource defense, and it is plausible that sexual selection has played an important role in their evolution. Focusing on identified individuals of known sex and age, we evaluated the sexual dimorphism in a type of loud calls (hoots) in a population of wild owl monkeys (Aotus azarae) in Argentina. We found evidence of sexual dimorphism in call structure, with females and males only emitting one type of call, each differing in dominant frequency and Shannon entropy. In addition, both age-related and sex-specific differences in call usage were also apparent in response to the removal of one group member. Future acoustic data will allow us to assess if there are individual characteristics and if the structure of hoot calls presents differences in relation to the social condition of owl monkeys or specific sex responses to variants of hoot calls' traits. This will provide deeper insights into the evolution of vocal mechanisms regulating pair bonding and mate choice strategies in this and other primate species.

Till death (or an intruder) do us part: intrasexual-competition in a monogamous primate.

Polygynous animals are often highly dimorphic, and show large sex-differences in the degree of intra-sexual competition and aggression, which is associated with biased operational sex ratios (OSR). For socially monogamous, sexually monomorphic species, this relationship is less clear. Among mammals, pair-living has sometimes been assumed to imply equal OSR and low frequency, low intensity intra-sexual competition; even when high rates of intra-sexual competition and selection, in both sexes, have been theoretically predicted and described for various taxa. Owl monkeys are one of a few socially monogamous primates. Using long-term demographic and morphological data from 18 groups, we show that male and female owl monkeys experience intense intra-sexual competition and aggression from solitary floaters. Pair-mates are regularly replaced by intruding floaters (27 female and 23 male replacements in 149 group-years), with negative effects on the reproductive success of both partners. Individuals with only one partner during their life produced 25% more offspring per decade of tenure than those with two or more partners. The termination of the pair-bond is initiated by the floater, and sometimes has fatal consequences for the expelled adult. The existence of floaters and the sporadic, but intense aggression between them and residents suggest that it can be misleading to assume an equal OSR in socially monogamous species based solely on group composition. Instead, we suggest that sexual selection models must assume not equal, but flexible, context-specific, OSR in monogamous species.

Spatio-genetic population structure in mustached tamarins, Saguinus mystax.

Dispersal and philopatry influence gene flow and thus the spatio-genetic structure within and between populations. In callitrichids the flexible social and mating system corresponds with a variable migration pattern where both sexes might be philopatric or might disperse. We investigated the relationship between the spatio-genetic structure and migration patterns in a population of mustached tamarins, Saguinus mystax. Using the rapidly evolving hypervariable region I (HVI) of the mitochondrial control region and 11 microsatellite markers we detected a high variation (HVI: 16 haplotypes in 69 individuals; microsatellites: H(O) = 0.75, average: 7.45 alleles/locus), with mating partners usually not sharing the same haplotype, indicating that matings are generally between partners that are not closely related. Similar high variance of haplotype differences for male-male and female-female pairs, along with a slightly higher number of haplotype differences in males show that both sexes habitually migrate. Spatial analyses suggest that females usually migrate longer distances, corresponding to very limited breeding positions for females in a polyandrous social mating system.

Grooming relationships between breeding females and adult group members in cooperatively breeding moustached tamarins (Saguinus mystax).

Grooming is the most common form of affiliative behavior in primates that apart from hygienic and hedonistic benefits offers important social benefits for the performing individuals. This study examined grooming behavior in a cooperatively breeding primate species, characterized by single female breeding per group, polyandrous matings, dizygotic twinning, delayed offspring dispersal, and intensive helping behavior. In this system, breeding females profit from the presence of helpers but also helpers profit from staying in a group and assisting in infant care due to the accumulation of direct and indirect fitness benefits. We examined grooming relationships of breeding females with three classes of partners (breeding males, potentially breeding males, (sub)adult non-breeding offspring) during three reproductive phases (post-partum ovarian inactivity, ovarian activity, pregnancy) in two groups of wild moustached tamarins (Saguinus mystax). We investigated whether grooming can be used to regulate group size by either "pay-for-help" or "pay-to-stay" mechanisms. Grooming of breeding females with breeding males and non-breeding offspring was more intense and more balanced than with potentially breeding males, and most grooming occurred during the breeding females' pregnancies. Grooming was skewed toward more investment by the breeding females with breeding males during the phases of ovarian activity, and with potentially breeding males during pregnancies. Our results suggest that grooming might be a mechanism used by female moustached tamarins to induce mate association with the breeding male, and to induce certain individuals to stay in the group and help with infant care.

Long-term patterns of sleeping site use in wild saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax): effects of foraging, thermoregulation, predation, and resource defense constraints.

Sleeping sites are an important aspect of an animal's ecology given the length of time that they spend in them. The sleep ecology of wild saddleback and mustached tamarins is examined using a long-term data set covering three mixed-species troops and 1,300+ tamarin nights. Seasonal changes in photoperiod accounted for a significant amount of variation in sleeping site entry and exit times. Time of exit was more closely correlated with sunrise than time of entry was with sunset. Both species entered their sleeping sites when light levels were significantly higher than when they left them in the morning. Troops of both species used >80 individual sites, the majority being used once. Mustached tamarins never used the same site for more than two consecutive nights, but saddlebacks reused the same site for up to four consecutive nights. Mustached tamarins slept at significantly greater heights than saddleback tamarins. There were consistent interspecific differences in the types of sites used. Neither the presence of infants, season, nor rainfall affected the types or heights of sites chosen. Sleeping sites were located in the central area of exclusive use more often than expected, and their position with respect to fruiting trees indicated a strategy closer to that of a multiple central place forager than a central place forager. These findings are discussed in light of species ecology, with particular reference to predation risk, which is indicated as the major factor influencing the pattern of sleeping site use in these species.

Paternity and kinship patterns in polyandrous moustached tamarins (Saguinus mystax).

We studied patterns of genetic relatedness and paternity in moustached tamarins, small Neotropical primates living in groups of 1-4 adult males and 1-4 adult females. Generally only one female per group breeds, mating with more than one male. Twin birth are the norm. In order to examine the genetic consequences of this mating pattern, DNA was extracted from fecal samples collected from two principal and six neighboring groups. DNA was characterized at twelve microsatellite loci (average: seven alleles/locus). We addressed the following questions: Do all adult males have mating access to the reproductive female of the group? How is paternity distributed across males in a group? Can polyandrous mating lead to multiple paternity? Are nonparental animals more closely related to the breeders than to the population mean? And, are mating partners unrelated? Breeding females mated with all nonrelated males. In at least one group the father of the older offspring did not sire the youngest infant although he was still resident in the group. We also found evidence for multiple paternity in a supposed twin pair. Yet, within each group the majority (67-100%) of infants had the same father, suggesting reproductive skew. Relatedness within groups was generally high (average R = 0.31), although both nonrelated males and females occurred, i.e., immigrations of both sexes are possible. Mating partners were never found to be related, hence inbreeding seems to be uncommon. The results suggest that while the social mating system is polyandry, paternity is often monopolized by a single male per group.

Demographic parameters and events in wild moustached Tamarins (Saguinus mystax).

This paper examines demographic events in the context of population structure and genetic relationships in groups of wild moustached tamarins (Saguinus mystax). We used a combination of long-term behavioral observations and genetic data from a total of eight groups from a population in northeastern Peruvian Amazonia. The mean group size was 6.0 (range = 4-9), including 2.5 adult males and 1.8 adult females. Within-group relatedness was generally high (r = 0.3), and most nonbreeding individuals were either natal or closely related to the respective same-sex breeder. The mean annual persistence of adults in the groups was 70% and 68% for males and females, respectively, and the reproductive tenure of one breeding pair lasted for at least 6 years. Migrations predominantly occurred after stability-disrupting events such as the immigration of new individuals and/or the loss of breeding individuals, or when groups were rather large. Migrations of both breeding and nonbreeding males and females occurred. Our results show that the hypothesis of Ferrari and Lopes Ferrari [Folia Primatologica 52:132-147, 1989] that tamarins live in smaller and less stable groups with lower relatedness compared to marmosets does not generally hold true. In contrast, we found that tamarin groups can consist of predominantly related individuals, and are stable as well. It is also apparent that a single demographic event can produce a chain of subsequent complex demographic changes.

Proximate mechanisms of reproductive monopolization in male moustached tamarins (Saguinus mystax).

In moustached tamarin (Saguinus mystax) groups, the single breeding female mates polyandrously with most or all nonrelated adult males. Nonetheless, paternity is monopolized in many groups by a single male. No evidence for male endocrine suppression has been found in this species. The proximate mechanisms of monopolization thus remain poorly understood. The aim of this study was to investigate the possible impact of agonistic interactions and mate-guarding on the monopolization of paternity in male moustached tamarins. Furthermore, we evaluated the likely costs of these behaviors, and whether olfactory cues might be used for its timing. We used behavioral data on proximity, agonistic interactions, time budgets, and scent-marking behavior to answer these questions. While direct agonistic competition does not play a prominent role, fertile females were consorted in some periods by one male, the sire of the previous and next litter. Consorting was instigated nearly exclusively by the male. It probably occurred during the female's periods of highest fertility, and thus likely functions as mate-guarding. The timing of the consortship was probably guided by olfactory cues in the female's scent marks. While we did not obtain direct evidence for energy costs in terms of increased energy expenditure or decreased food intake, we found that consorting males are more conspicuous and therefore may be more vulnerable to predators.