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AbstractDemographic data are essential to assessments of the status of endangered species. However, establishing an integrated monitoring program to obtain useful data on contemporary and future population trends requires both the identification of priority areas and populations and realistic evaluations of the kinds of data that can be obtained under different monitoring regimes. We analyzed all known populations of a critically endangered primate, the muriqui (genus: Brachyteles) using population size, genetic uniqueness, geographic importance (including potential importance in corridor programs) and implementability scores to define monitoring priorities. Our analyses revealed nine priority populations for the northern muriqui ( B. Hypoxanthus) and nine for the southern muriqui ( B.

In addition, we employed knowledge of muriqui developmental and life history characteristics to define the minimum monitoring intensity needed to evaluate demographic trends along a continuum ranging from simple descriptive changes in population size to predictions of population changes derived from individual based life histories. Our study, stimulated by the Brazilian government’s National Action Plan for the Conservation of Muriquis, is fundamental to meeting the conservation goals for this genus, and also provides a model for defining priorities and methods for the implementation of integrated demographic monitoring programs for other endangered and critically endangered species of primates. Materials and methodsTo define priority areas for the demographic monitoring of all known muriqui populations (, ), we expand on the demographic and geographic criteria used by the IUCN Standards and Petitions Subcommittee in their evaluations of the threatened status of taxa. Specifically, our assessments of priority areas for monitoring are based on the following criteria: (i) Population size (and composition); (ii) Genetic uniqueness of the population; and (iii) Geographic importance of the population (ecological uniqueness of the habitat and/or its strategic location for optimizing connectivity). Locality names and coordinates of known populations of the northern muriqui ( Brachyteles hypoxanthus) and southern muriqui ( B.

Arachnoides).Points correspond to locations in.In addition, for each population that meets at least one of the priority criteria, we assessed the (iv) feasibility of implementing a systematic demographic monitoring program. This assessment of “implementability” is based on current knowledge of accessibility and logistics and thus provides a basis for identifying sites where demographic monitoring would be most likely to succeed.The initial demographic data collected in any population will correspond to the first count of individuals in the population. However, even among areas identified as priorities, the frequency of monitoring and the degree to which individuals can be recognized will affect the kinds of questions that can be addressed. To identify criteria for determining the optimal monitoring intensity, we drew on our collective experiences of observing wild northern and southern muriquis and considered (i) the degree to which individuals in the population can be identified; (ii) the frequency of monitoring; and (iii) the period of time over which the population is monitored. We then used these considerations to evaluate the information that each level of monitoring intensity can yield. Population size (and composition).The IUCN Standards and Petitions Subcommittee defines a taxon’s population size as “the number of mature individuals.” However, we distinguish (by sex) other age classes in our demographic assessments because information on the composition of a population can provide insights into its potential for growth versus decline (see for evidence from the RPPN-FMA population of muriquis).The IUCN Red List criteria consider the smallest populations (.

Genetic uniqueness.Only limited data on population genetics are available for either species of muriqui. Nonetheless, comparative analyses permit us to identify some initial priority populations based on the uniqueness and diversity of haplotypes across a subset of populations of each species. Analyses of the mitochondrial DNA control region from 152 northern muriqui individuals from eight populations revealed that the total number of haplotypes (3–8, of 23 haplotypes), the number of unique haplotypes (3–5), and haplotype diversity (0.626–0.846) were highest in the populations occupying the largest forests. However, 42% of the individuals sampled were from one population (RPPN Feliciano Miguel Abdala), which could influence these results.Preliminary genetic analyses of 60 southern muriqui individuals from 10 populations found 39 haplotypes in 612bp of the mtDNA Control Region, with haplotype diversity of 0.976 and 13 out of 14 nuclear microsatellite loci polymorphic in 55 individuals, an average of 6.86 alleles (range = 3–12 alleles) and observed heterozygosity ranging from 0.074 to 0.778. These results indicate a high diversity with no clear evidence of geographical structuring and one population (PE Carlos Botelho) as possessing most of this diversity, with no concrete evidence of a recent genetic bottleneck for this population inhabiting the largest forest for this species. Thus, in contrast to the very patchy distribution of genetic diversity of the northern muriqui, there is still at least one population of the southern muriqui in which most of this species’ genetic diversity is represented.

However, almost 60% of the sampled individuals were obtained from this population, which could bias the results.Further genetic studies are clearly needed to better understand both the historical and current genetic relationships among extant populations of each species, and to resolve the relationships between the two species, including specifically whether both species occur in the state of Rio de Janeiro ,. We anticipate that any populations of northern and southern muriquis identified as having occurred sympatrically in the past (with the potential for hybridization) would also fall within our criteria for monitoring priority. Reasons such as these resulted in our scoring the genetic uniqueness of a population for which no genetic data are yet available as “expected” for both species. Implementability.For each population that meets the demographic, genetic, or ecological criteria, or is expected to meet one or more of these criteria as more information about the population becomes available, we also consider criteria that facilitate or represent obstacles to long-term monitoring. The implementability of demographic monitoring can be assessed qualitatively from current knowledge based on three parameters: 1) Whether researchers have access (e.g., in terms of trails, permission to enter the forest) to monitor the muriqui population at a site; 2) Whether there is institutional encouragement and support for the monitoring; and 3) Whether monitoring of the population is considered to be feasible in terms of terrain, logistics and personnel or financial resources. When all three of these parameters are met (i.e., Implementability = 1,2,3), demographic monitoring of the population is considered to be highly feasible; when no parameters are met (Implementability = 0), it may be difficult or impossible to implement the monitoring program without improving accessibility and logistical issues.

Level of individual identification.The specificity of demographic data obtained can range from counts of the number of animals observed, to counts of the number of animals represented in different age and/or sex classes, to counts of distinct individuals, whose age-sex classes may or may not be known to precision. The ability to distinguish individuals usually requires repeated observations over extended periods of time, whereas the ability to identify animals by age and sex class may be possible based on visible physical characteristics that correspond to obvious developmental stages. Sometimes these physical traits can be combined with landmarks in behavioral development, documented for that species, such as the age at which infants shift from being carried ventrally to dorsally.

Examples of these behavioral and physical characteristics for distinguishing muriqui age-sex classes are provided in the Supporting Information ( and Figures A-R in ). Monitoring frequency.The frequency of demographic monitoring is defined as the number of counts made per unit time. These may occur daily or nearly daily, in the case of continuous field studies, or at longer intervals, in the case of targeted expeditions. Counts of the same populations over time will permit analyses of demographic trends. The shorter the intervals between successive counts, the more precise the estimates of demographic trends will be.

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However, factors such as limited resources for maintaining the continuity of observations and poor implementability may necessitate less frequent monitoring. Monitoring duration.Variation in monitoring duration, or the period of time over which the population is monitored, will affect the accuracy of detecting real demographic trends.

We used the median interbirth interval to calibrate the minimum monitoring duration needed for assessing population trends, and the median ages of first birth for females and first reproduction (based on first complete copulation or paternity) for males to set the minimum monitoring duration to evaluate the role of individual life histories in demographic trends. Northern muriqui monitoring priorities.The largest populations of northern muriquis (≥ 100 individuals total; ≥ 50 mature individuals), and thus, those prioritized for systematic monitoring based on demographic criteria, are summarized in.

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The same four populations (RPPN-FMA, PESB, PERD, and SMJ) were also prioritized as genetically “discrete management units” in an analysis of genetic data from eight populations of northern muriquis. Additional analyses of the genetics of other populations of northern muriquis may lead to adjustments or additions to this list. Optimal monitoring intensityRegardless of the frequency of observations or the duration over which population demography is monitored, the maintenance of consistent, detailed records is essential for analyses of demographic trends (See ). Interpretations of these demographic trends must be sensitive to differences in the intensity of monitoring and the accuracy of the demographic data obtained. At the most extreme monitoring intensity for muriquis (, far right column) are populations in which all individuals can be recognized by their natural markings and these individuals have been monitored for decades.

In these cases, changes in group sizes and composition can be tracked on the basis of individual reproductive, survivorship, and dispersal events, often to the precision of days or weeks, depending on the monitoring frequency. However, in cases where such intensive monitoring may be unfeasible or undesirable, less intensive monitoring efforts can still yield valuable demographic data that permit systematic assessments of demographic trends. Factors affecting the intensity of demographic monitoring and estimates of demographic trends.The ability to recognize individuals may increase over time if the animals become habituated to observers and observers become more familiar with their subjects. However, poor visibility due to tall forest or dense vegetation, difficult terrain, or lack of distinctly visible markings can also preclude individual recognition. Southern muriquis, for example, have completely black faces and are therefore more difficult to identify individually than northern muriquis, which have distinct patterns of facial and genital depigmentation.The advantages of being able to recognize individuals for demographic monitoring pertain mainly to precision, as the risks of over-estimating group and population size due to redundant counts of the same animals are reduced. Individual recognition also allows for the potential to monitor the variance in female reproductive rates, which can contribute to a better understanding of the processes, such as changes in fertility rates, that may underlie demographic trends e.g.,.

However, it is important to note that trends in population size can still be evaluated with counts of individuals in general, and projected trends in population size can be made based on changes in sex ratios, the percentage of fertile females (estimated from the percentage of females carrying infants), and calculations of age-sex class composition.Trends in population sizes can be assessed whenever at least two counts of the population have been made, provided that these counts are conducted in a comparable, systematic ways. Thus, efforts to conduct the counts at the same time of day (due to diurnal variation in activities and its potential effects of visibility) or times of year (relative to seasonal variation in behavior and the seasonal timing of births) should be made to reduce potential sources of error in estimates of demographic trends.Incorporation of muriqui life history data provides a rationale for interpreting population trends. For example, we can assume that if a population increases over the duration of a median IBI (i.e., 3 yrs for muriquis ), then it is likely that births (and immigrations) have outweighed deaths (and emigrations), whereas the opposite could be inferred if the population declined.

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Shorter monitoring durations would be less likely to detect these dynamics. Longer monitoring durations (minimally 6 years, corresponding to 2 IBIs for muriquis) are necessary to document changes in fertility patterns and even longer monitoring durations are necessary to document the effects of variation in individual life histories on demographic trends.