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The brown howler monkey (Alouatta guariba clamitans) is endemic to South America’s Atlantic Forest, with a small population extending into the northern portion of Misiones province in northeastern Argentina. In 2012, the species was classified as Critically Endangered in Argentina due to its highly restricted distribution, low population density and dramatic declines from recent Yellow Fever outbreaks. In March 2013, we organized an international workshop in Misiones to evaluate population status in Argentina and conduct a threat analysis. We developed population viability models using Vortex and Outbreak software packages. These tools allowed us to explore how several biological and demographic parameters of brown howlers, as well as factors related to Yellow Fever epidemiology, affect the probability of species extinction. The discussion among diverse specialists and analysis of model results identified Yellow Fever as the main threat to brown howler population persistence in Argentina. Our threat analysis, focused on the dynamics of Yellow Fever outbreaks and their impact on howler populations, led to the identification of gaps in knowledge that helped prioritize objectives and actions for the development of a Species Conservation Strategy in Argentina.
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Conservation Letter
Building a Species Conservation Strategy for the
brown howler monkey (Alouatta guariba clamitans) in
Argentina in the context of yellow fever outbreaks
Ilaria Agostini1,2, Ingrid Holzmann1,2, Mario S. Di Bitetti1,2, Luciana I.
Oklander1,2, Martín M. Kowalewski3, Pablo M. Beldomnico4, Silvina
Goenaga5, Mariela Martínez1,6, Eduardo S. Moreno7, Eduardo
Lestani6, Arnaud L. J. Desbiez8,9 and Philip Miller9
1Instituto de Biología Subtropical (IBS)- nodo Iguazú, Consejo Nacional de Investigaciones Científicas y
Técnicas (CONICET) – Universidad Nacional de Misiones (UNaM); 2Asociación Civil Centro de
Investigaciones del Bosque Atlántico (CeIBA); 3Estación Biológica de Corrientes (EBCO)- MACN BR,
CONICET; 4Laboratorio de Ecología de Enfermedades, ICIVET LITORAL, UNL-CONICET; 5de Ecología de
Enfermedades, ICIVET LITORAL, UNL-CONICET; 5Instituto Nacional de Enfermedades Virales Humanas
(INEVH) Dr. Julio I. Maiztegui; 6Instituto Nacional de Medicina Tropical (INMeT); 7Ministerio da Saude
Brasil; 8) Royal Zoological Society of Scotland; 9Conservation Breeding Specialist Group (IUCN/SSC)
Corresponding author: Ilaria Agostini E-mail: agostini.ilaria@gmail.com
Abstract
The brown howler monkey (Alouatta guariba clamitans) is endemic to South America’s Atlantic Forest, with a small
population extending into the northern portion of Misiones province in northeastern Argentina. In 2012, the species was
classified as Critically Endangered in Argentina due to its highly restricted distribution, low population density and dramatic
declines from recent Yellow Fever outbreaks. In March 2013, we organized an international workshop in Misiones to evaluate
population status in Argentina and conduct a threat analysis. We developed population viability models using Vortex and
Outbreak software packages. These tools allowed us to explore how several biological and demographic parameters of brown
howlers, as well as factors related to Yellow Fever epidemiology, affect the probability of species extinction. The discussion
among diverse specialists and analysis of model results identified Yellow Fever as the main threat to brown howler population
persistence in Argentina. Our threat analysis, focused on the dynamics of Yellow Fever outbreaks and their impact on howler
populations, led to the identification of gaps in knowledge that helped prioritize objectives and actions for the development
of a Species Conservation Strategy in Argentina.
Key words:Alouatta guariba clamitans; Population Viability Analysis; Threat Analysis; Yellow Fever.
Resumen
El mono aullador marrón (Alouatta guariba clamitans) es endémico del Bosque Atlántico de América del Sur, con una pequeña
población que se extiende en la porción norte de la provincia de Misiones en el noreste de Argentina. En el año 2012, debido
a su reducida distribución geográfica, su baja densidad poblacional y al dramático impacto de los recientes brotes de Fiebre
Amarilla, la especie fue categorizada en Argentina como “en peligro crítico”. En el mes de marzo de 2013 organizamos un
taller internacional en Misiones con el objetivo de evaluar el estado de la población de esta especie en Argentina y llevar a
cabo un análisis de las principales amenazas para su conservación. Para alcanzar estos objetivos construimos modelos de
viabilidad poblacional utilizando los programas Vortex yOutbreak. Los mismos nos permitieron explorar cómo varios
parámetros biológicos y demográficos de la especie, así como diversos factores relacionados al impacto de la Fiebre Amarilla,
influyen sobre la probabilidad de extinción de la especie. La discusión entre los distintos especialistas y el análisis de los
resultados de los modelos identificaron a la Fiebre Amarilla como la principal amenaza para la subsistencia de esta población
en Argentina. El análisis de las amenazas se centró en la dinámica de los brotes de Fiebre Amarilla y la severidad de su impacto
sobre la población de esta especie, lo que permitió identificar huecos en el conocimiento que permitieron priorizar objetivos
y acciones a llevar a cabo para el desarrollo de una estrategia de conservación para esta especie en Argentina.
Palabras clave:Alouatta guariba clamitans; Análisis de Viabilidad Poblacional; Análisis de amenazas; Fiebre Amarilla.
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Introduction
The brown howler monkey (Alouatta guariba) is endemic to the Atlantic Forest, ranging from
the Brazilian states of Bahia and Espirito Santo in the north to Rio Grande do Sul and the
Argentine province of Misiones in the south [1]. The species has been re-classified globally from
“Near Threatened” to “Least Concern” by the IUCN due to its presence in most of the extant
conservation units of the Atlantic Forest in Brazil. However, the population trend is still
“decreasing” and the future of this species is quite uncertain, since the spatial extent of the
Brazilian Atlantic Forest is dramatically reduced and fragmented [2]. In Argentina, the brown
howler (Alouatta guariba ssp. clamitans) is restricted to Misiones and has been recently re-
classified from “endangered” to “critically endangered” [3]. Existing data indicate that
population density is very low, and its presence is confirmed in only five small protected areas
of Misiones [4-5].
In 2005 I. Agostini, I. Holzmann and M. S. Di Bitetti started the first study on the behavioral
ecology of brown howlers and the sympatric congener black and gold howler monkeys (Alouatta
caraya) in one protected area of Misiones, El Piñalito Provincial Park [6-10]. This study was
unexpectedly interrupted in January 2008, when a sudden outbreak of Yellow Fever (YF) killed
all study group members. The outbreak continued until 2009 and decimated howlers throughout
their southern distribution [11-14]. Due to the suspected high impact of these epidemics on the
brown howler in Argentina, there is a special concern about the current status of this small
population. In March 25-28, 2013, in order to establish conservation priorities and initiate the
development of a conservation plan for the species in Argentina, we carried out the First Brown
Howler Monkey Conservation Workshop in the Karadya Bio-Reserve near Comandante
Andresito and Puerto Iguazú (Misiones, Argentina). A group of nine experts in different fields
(primate ecology, eco-epidemiology, mosquito ecology and virology) dedicated themselves to
gathering, systematizing and discussing all available data and information on brown howlers and
Yellow Fever in the Atlantic Forest. The workshop was facilitated by members of the IUCN/SSC’s
Conservation Breeding Specialist Group (CBSG), who also provided expertise in the development
and use of quantitative risk assessment models used in data assembly and analysis.
Received: 17 October 2013; Accepted 7 November 2013; Published: 24 March 2014
Copyright: © Ilaria Agostini, Ingrid Holzmann, Mario S. Di Bitetti, Luciana I. Oklander, Martín M. Kowalewski, Pablo M.
Beldomnico, Silvina Goenaga, Mariela Martínez, Eduardo S. Moreno, Eduardo Lestani, Arnaud L. J. Desbiez, Philip Miller. This is
an open access paper. We use the Creative Commons Attribution 3.0 license http://creativecommons.org/licenses/by/3.0/us/.
The license permits any user to download, print out, extract, archive, and distribute the article, so long as appropriate credit is
given to the authors and source of the work. The license ensures that the published article will be as widely available as possible
and that your article can be included in any scientific archive. Open Access authors retain the copyrights of their papers. Open
access is a property of individual works, not necessarily journals or publishers.
Cite this paper as: Agostini, I., Holzmann, I., Di Bitetti, M. S., Oklander, L. I., Kowalewski, M. M., Beldomnico, P. M., Goenaga, S.,
Martínez, M., Moreno, E. S., Lestani, E., Desbiez, A. L. J. and Miller, P. 2014. Building a Species Conservation Strategy for the
brown howler monkey (Alouatta guariba clamitans) in Argentina in the context of yellow fever outbreaks. Tropical Conservation
Science Vol.7 (1): 26-34. Available online: www.tropicalconservationscience.org
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The objectives of the workshop were:
1. To provide an updated review of our current knowledge of species status, ecology and
population dynamics in Misiones, thereby revealing key information gaps and
suggesting new directions for future research.
2. To synthesize our knowledge of the primary factors impacting population dynamics and
abundance (i.e., threats analysis).
3. To specify important goals and objectives for species recovery in Argentina.
4. To identify ways to enhance public awareness of the species and its conservation in
Misiones, and to specifically create a network of stakeholders committed to work on
the next step in brown howler management: a Species Conservation Strategy using the
guidelines defined by the IUCN/SSC Species Conservation Planning Handbook [15]. This
objective was not the focus of this letter, but will be addressed in another publication.
Status review, vision, challenges and threats analysis
For Objective (1) and part of Objective (2), we carried out a review of current knowledge on
brown howlers, especially in Argentina, YF dynamics, the biology and ecology of known and
potential vectors for this disease, and its impact on non-human primates. This process helped
to reveal how little we know about the small Argentinean brown howler monkey population.
Then, to address Objective (3), we developed the following vision statement about the “ideal
future” for brown howler monkeys in Misiones in 100 years:
“In 100 years’ time, the population of brown howler monkeys in Misiones is viable
in terms of demography, genetics and health, and ecologically functional in an
environment that maintains the original biodiversity of the region and in a human
society committed to its conservation”.
The development of this statement led us to point out the biggest threat to brown howler
conservation in Argentina (Objective 2): excessive mortality due to YF outbreaks. Specifically, we
identified as major challenges the need to integrate animal and public health, develop a more
effective pre- and post- YF epidemic monitoring strategy for brown howlers, acknowledge the
complexity of the system including human and non-human primates, other potential hosts, their
interface with the landscape, and the dynamics of YF outbreaks.
In order to understand the state of knowledge of YF dynamics and to help achieve Objective (3),
we created a system-level diagram of YF vectors, hosts, and the many ways in which those
entities interact to influence outbreaks of disease (Fig. 1).This diagram made evident the lack of
published data and studies on several critical variables needed to predict what could trigger a
YF outbreak (e.g. hosts and vectors densities, dispersal capacity of vectors and connectivity
among host sub-populations), and what could determine the impact of a YF outbreak on brown
howlers (e.g. genetic resistance to YF, immunological experience, and general
immunocompetence).
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Fig. 1. System-level diagram illustrating links and interactions between factors affecting YF vectors and hosts. Letters in red indicate
data quality as determined by workshop participants: D, specific data available to support diagram element; A, validity of diagram
element based on assumption; N, no specific data available to support diagram element.
Population modeling
In order to examine the factors that most influence the viability of the brown howler population
in Argentina (Objective 2), we examined and estimated input parameters and scenarios for two
modeling tools commonly used in CBSG workshop processes: Vortex 16] and Outbreak [17].
Vortex is a Monte Carlo simulation for population viability analysis that examines the effects of
deterministic forces as well as demographic, environmental, and stochastic genetic events on
wild populations. Vortex models population dynamics as discrete sequential events that occur
according to defined probabilities. The program is not intended to give absolute answers,
because it projects stochastically the interactions of the many parameters used as input to the
model, and because of the random processes involved in nature [18-19]. The objective of its use
was to identify potential threats by weighing the relative importance of specific factors to
predicted future population abundance trajectories.
Vortex models were run by A. Desbiez on the basis of input parameters provided by I. Agostini,
I. Holzmann, M. Kowalewski and M. S. Di Bitetti. First, a “baseline” model was created that left
out the probability of periodic disease outbreak. A simple form of sensitivity analysis [20] was
then used to identify key demographic parameters that contribute significantly to growth of
brown howler monkey populations. Vortex was then used to examine the relative impact of YF
when modeled as a catastrophe” affecting brown howler monkey survival (Fig. 2 a,b). This
approach does not explicitly consider the details of disease ecology and epidemiology that
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determine outbreak frequency, but instead simply treats disease outbreaks as generic periodic
events that occur according to a constant defined annual probability. Baseline survival values
across all age-sex classes are reduced by a specified amount if an “outbreak” occurs within a
given year of the simulation. Multiple scenarios were created that explored the relative
response of our simulated brown howler population to outbreak catastrophes of different
frequency or demographic severity.
Results of simulations indicated that both the severity and the frequency of YF outbreaks have
an impact on the rate of extinction of simulated brown howler monkey populations. Survival
rates had more impact on model performance than frequency of outbreaks. However this is also
because the severity of the outbreak used in the baseline model was high (70% mortality),
although it was not an overestimate given the levels of mortality observed at El Piñalito [11].
Measuring the impact of YF outbreaks on survival of individuals from populations of howler
monkeys is important for population viability modeling purposes.
a)
Fig. 2. Abundance trajectories for
simulated populations of the brown
howler monkey in Misiones, Argentina,
in the absence (a, top) and presence (b,
bottom) of YF outbreaks. Each panel
shows 100 iterations of a demographic
model using the Vortex software
package. Note the severe population
declines that occur immediately
following the onset of YF outbreaks in
the bottom panel.
b)
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Finally, we constructed a simple simulated “metapopulation” of multiple brown howler sub-
populations (using general knowledge of known remnant groups and their distribution in
Misiones) that could exchange individuals at different rates among sub-populations. By adding
catastrophic outbreaks to this type of spatially explicit model, we investigated the influence that
dispersal can have on the spread of localized disease outbreaks and subsequently, on
metapopulation extinction risk. Results indicated that if YF does not impact all sub-populations
equally, fragmentation of the brown howler population could actually decrease its probability
of extinction. This result is common to many similar and more sophisticated modeling studies
(e.g. [21]), but the specific properties of these systems are highly dependent on the spatial
arrangement of sub-populations and the degree of connectivity among them.
Disease modeling
A major goal of this workshop was to apply new disease epidemiology simulation modeling tools
to the issue of YF epidemiology and transmission dynamics among brown howler monkey
populations in northeastern Argentina. We used the software package Outbreak [17] to build a
simple model of YF dynamics in brown howler monkeys, and to investigate model sensitivity to
a set of key epidemiology model input parameters, including rates of contact between individual
howlers, contact between howlers and other infected hosts, transmission probabilities, and
disease-based mortality rates.
Outbreak models of YF epidemiology were created with the use of input parameters provided
by E. Moreno, P. Beldomenico, S. Goenaga, M. Martinez and E. Lestani. Because we have very
little data on YF ecology and epidemiology in Misiones region of Argentina, we had to use data
from other regions or countries where similar types of YF outbreaks have occurred, e.g.,
southern Brazil. Although Outbreak was not specifically designed to deal with the complexities
of transmission dynamics of vector-borne diseases like YF, we created a basic model of YF
epidemiology that generated reasonable predictions of disease dynamics in brown howler
populations without requiring the explicit consideration of mosquito vector population density
or demographic dynamics.
Using new “metamodeling” software technology [22], we physically linked Vortex and Outbreak
models together to create more detailed and informative models of YF dynamics in brown
howler populations. This new technology allowed us to utilize the detailed demographic
structure of Vortex and the more sophisticated disease dynamics of Outbreak to more accurately
control sources of natural and disease-based mortality, respectively. Using this method, YF
outbreaks are not simple catastrophes as defined in Vortex but now become emergent events
that are a function of the underlying disease epidemiology controlled in Outbreak. When
epidemics occur in Outbreak, animals are randomly selected to die from the disease and this
information is then passed to Vortex, where the data are used to reduce overall population
abundance in the corresponding time step.
Sensitivity analysis featuring this metamodeling approach was used to evaluate the implications
of measurement uncertainty in a set of epidemiological input parameters within the Outbreak
model. Parameters collectively defining the rate of pathogen introduction and transmission into
a population were primary drivers of disease outbreak frequency, while other factors such as
disease-based mortality rates were important factors that determined the long-term
demographic viability of the howler population (Fig. 3). Although the input values of these
models have been estimated with considerable uncertainty, the analysis allowed the
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researchers to better understand which variables have more relative importance in YF dynamics
and the impact of the disease on brown howler monkey population.
With the insights gained from this simple and preliminary analysis, we hope to challenge these
tools further to create more realistic models of YF particularly in spatially structured
landscapes – to explore with greater accuracy the fate of brown howler monkeys in Misiones.
Fig. 3. Extinction risk trajectories for a simulated brown howler monkey
population in the presence of ocasional YFoutbreaks. The model structure used in
this analysis featured a Vortex demographic model linked to a model of YF
epidemiology using Outbreak, thereby creating a “metamodel” to address more
complex population dynamics. Curves feature different levels of disease-based
mortality simulated within Outbreak, with 50% mortality rate defining the
baseline disease model.
Recommendations
Based on the diagramming process and the population and disease modeling, we recommend a
list of actions that will address the most important current knowledge gaps. For each action, a
focal person of reference, a time frame, important collaborators, potential sources of financial
support and degree of difficulty for implementation were specified.
Recommendations and actions in order of priority are the following:
Action 1. Implement a regular surveillance program for alerting local authorities about
suspected YF outbreaks in monkeys and/or people.
Action 2. Estimate the population distribution and abundance of brown howler monkeys in
Misiones.
Action 3. Conduct health studies of brown howler monkeys in Misiones to evaluate and
compare physiological stress, innate and acquired immunity, hematology, etc., across different
sub-populations especially before and after YF outbreaks.
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Action 4. Isolate YF virus from mosquito adults and larvae.
Action 5. Conduct a thorough literature and archive review of the interactions (environmental
and anthropogenic) involved in the maintenance and dynamics of YF outbreaks in South
America.
Action 6. Capture adult mosquitoes where monkeys sleep or capture adult mosquitoes
through monkey baited capture stations to identify YF vectors and monitor presence of the
virus.
Action 7. Define the potential distribution of brown howlers in Argentina.
Action 8. Attempt to isolate or detect the YF virus in suspected vertebrate hosts using
virological assays, cell cultures and molecular techniques.
Action 9. Conduct a systematic review of YF virus virulence from different strains in different
vertebrate hosts in Misiones and Brazil.
Action 10. Understand the factors that define carrying capacity for brown howler monkeys and
their habitat requirements (limiting factors, food, threats).
We hope this letter will stimulate research designed to tackle these actions. Improving
knowledge on these issues is vital for understanding and therefore effectively managing the
small brown howler population and impact of YF outbreaks in Argentina. Ultimately this will help
us develop an effective Species Conservation Strategy for this brown howler population. To
ensure that recommendations are effectively implemented, we created the Brown Howler
Monkey Conservation group (BHMC group), to which members can be added as they get
involved in the actions
(https://www.facebook.com/pages/Brown-Howler-Monkey-Conservation-Group-
BHMCG/182361558615174).
Acknowledgements
We are grateful to the IUCN/SSC Species Conservation Planning Sub-committee (SCPSC),
Conservation International –Margot Marsh Biodiversity Foundation – Primate Action Fund and
the Banham Zoo of England for supporting the workshop with grants. We are thankful to the
Karadya Bio-Reserve (Andresito, Misiones) for hosting the workshop; special thanks to Julián
Baigorria for his excellent logistic organization during the days in the Reserve. The Centro de
Investigaciones Ecológicas Subtropicales (CIES)–AdministraciónParques Nacionales of Argentina
provided lodging facilities in Iguazú. We thank an anonymous reviewer for critical comments on
an early version of this manuscript.
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... The western boundary is marked by the limits of the Atlantic Forest. In Argentina, the species occurs in the province of Misiones (Agostini et al. 2014). Although with some uncertainty, two subspecies are recognized: the southern brown howler, A. guariba clamitans, and the northern brown howler, Alouatta g. guariba, north of the rios Jequitinhonha or Doce (Rylands et al. 2000;Glander 2013). ...
... Southern brown howlers (Alouatta guariba clamitans) occur in lowland forests along Brazil's coast, as well as in higher elevation submontane and montane forests and seasonal semi-deciduous forests inland . In southern Brazil and northeast Argentina, they also occupy a transition of mixed Upper Paraná Atlantic Forest and Araucaria Moist Forest (Miranda and Passos 2005;Agostini et al. 2014). Aguiar et al. (2007) recorded the species in periodically flooded and semi-deciduous forests in the Paraná river floodplains. ...
... Although some local population census data are available for Brazil, the total remaining population is unknown, but certainly declining. In Argentina, the situation is even worse; only a few populations persist with no more than 20-50 adult individuals (Agostini et al. 2014). ...
Chapter
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Howlers are highly susceptible to yellow fever, and two recent outbreaks have severely affected their numbers.
... The western boundary is marked by the limits of the Atlantic Forest. In Argentina, the species occurs in the province of Misiones (Agostini et al. 2014). Although with some uncertainty, two subspecies are recognized: the southern brown howler, A. guariba clamitans, and the northern brown howler, Alouatta g. guariba, north of the rios Jequitinhonha or Doce (Rylands et al. 2000;Glander 2013). ...
... Southern brown howlers (Alouatta guariba clamitans) occur in lowland forests along Brazil's coast, as well as in higher elevation submontane and montane forests and seasonal semi-deciduous forests inland . In southern Brazil and northeast Argentina, they also occupy a transition of mixed Upper Paraná Atlantic Forest and Araucaria Moist Forest (Miranda and Passos 2005;Agostini et al. 2014). Aguiar et al. (2007) recorded the species in periodically flooded and semi-deciduous forests in the Paraná river floodplains. ...
... Although some local population census data are available for Brazil, the total remaining population is unknown, but certainly declining. In Argentina, the situation is even worse; only a few populations persist with no more than 20-50 adult individuals (Agostini et al. 2014). ...
... The western boundary is marked by the limits of the Atlantic Forest. In Argentina, the species occurs in the province of Misiones (Agostini et al. 2014). Although with some uncertainty, two subspecies are recognized: the southern brown howler, A. guariba clamitans, and the northern brown howler, Alouatta g. guariba, north of the rios Jequitinhonha or Doce (Rylands et al. 2000;Glander 2013). ...
... Although some local population census data are available for Brazil, the total remaining population is unknown, but certainly declining. In Argentina, the situation is even worse; only a few populations persist with no more than 20-50 adult individuals (Agostini et al. 2014). ...
... The western boundary is marked by the limits of the Atlantic Forest. In Argentina, the species occurs in the province of Misiones (Agostini et al. 2014). Although with some uncertainty, two subspecies are recognized: the southern brown howler, A. guariba clamitans, and the northern brown howler, Alouatta g. guariba, north of the rios Jequitinhonha or Doce (Rylands et al. 2000;Glander 2013). ...
... Although some local population census data are available for Brazil, the total remaining population is unknown, but certainly declining. In Argentina, the situation is even worse; only a few populations persist with no more than 20-50 adult individuals (Agostini et al. 2014). ...
... We believe that this could be due to the lower population densities at which howler monkeys persist in Misiones, following the last yellow fever outbreak of (Holzmann et al. 2010). The consequences of this outbreak have led howler species, and especially brown howlers, to the verge of regional extinction, while leaving black-horned capuchin populations relatively unchanged (Agostini et al. 2014(Agostini et al. , 2015. At the same time, the lack of photographic records of howlers may also be the result of the relatively low height at which camera traps were positioned on trees. ...
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Canopy camera trapping is being increasingly used to characterize assemblages of arboreal mammals. In this study we compared, for the first time, the assemblage of arboreal mammals of the Atlantic Forest, surveyed using canopy camera trapping at two protected areas of Mis-iones, Argentina: Piñalito (11 camera-trap stations) and Cruce Caballero (9 stations), with the assemblage recorded at ground-level with a camera-trapping survey conducted at another protected area, the nearby private reserve Valle del Alegría (18 stations). We calculated the number of independent photo-events for each species and site, and we built species rank abundance curves to compare the recorded species diversity among sites. We recorded six mammal species at Piñalito and Cruce Caballero, and 23 at Valle del Alegría. Canopy-survey sites showed lower diversity but a different and non-nested species composition when compared to the ground-level survey. One of the most frequently recorded species in the canopy, the brown-eared woolly opossum, Caluromys lanatus, categorized as Vulnerable in Argentina, has not been photographed in ground-level camera-trap surveys in Misiones before. Our results suggest that canopy camera trapping represents a robust method to sample arboreal species that are missed in ground-level camera-trap surveys, thus improving forest species inventories.
... Of the four decision-support PVAs we identified (Appendix S2), the majority excelled at providing a clear application that motivated model development. Agostini et al. (2014) described the background on the protection of brown howler monkeys (Alouatta guariba clamitans) by the International Union for Conservation of Nature and developed a PVA to inform future conservation strategies and research priorities. Model scenarios represented uncertainties about disease transmission and were used to identify important metrics for monitoring (third question). ...
... The entire geographic distribution of A. guariba clamitans in Argentina was sampled after the outbreak and the species had disappeared from most sites, implying that YFV had swept through all the regions they inhabited . Based on these studies, the impact of the outbreak was conservatively estimated to decimate 80% of the Alouatta population (Agostini et al., 2014;Moreno et al., 2015). This outbreak was potentially exacerbated by the deforestation of the Atlantic forest over the last 50 years (Di Bitetti, Placci, Brown, & Rode, 1994;Holzmann et al., 2010). ...
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Background In 2007–2009, a major yellow fever virus (YFV) outbreak in Northern Argentina decimated the local howler monkey (Alouatta) population. Aims To evaluate whether the surviving howler monkeys possess advantageous genetic variants inherited from monkeys alive prior to the YFV outbreak, we explored the relationship between Toll‐like receptor (TLR) 7 and TLR8 gene variation and YFV susceptibility. Methods We used samples from Alouatta individuals in Misiones, Argentina alive before the YFV outbreak, individuals that died during the outbreak, and individuals that survived the outbreak and are alive today. We measured genetic divergence between Alouatta YFV exposure groups and evaluated Alouatta‐specific substitutions for functional consequences. Results We did not find different allele frequencies in the post‐YFV exposure Alouatta group compared to the pre‐exposure group. We identified three nonsynonymous variants in TLR7 in Alouatta guariba clamitans. Two of these substitutions are under positive selection in functionally important regions of the gene. Discussion and Conclusions Our results did not indicate that surviving howler monkey spossess advantageous genetic variants at greater frequency than those alive before the YFV outbreak. However, the positively selected unique coding differences in A. guariba clamitans are in the region important in pathogen detection which may affect YFV resistance. Morework is necessary to fully explore this hypothesis
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Habitat loss and fragmentation are major threats to the conservation of nonhuman primates. Given that species differ in their responses to fragmented landscapes, identifying the factors that enable them to cope with altered environments or that cause their extirpation is critical to design conservation management strategies. Howler monkeys ( Alouatta spp.) are good models for studying the strategies of tolerant arboreal taxa and how they cope with spatial restriction, because they live in habitats ranging from vast pristine forests to small disturbed fragments and orchards. While some aspects of their ecology and behavior are conserved, others vary in predictable ways in response to habitat shrinking and decreasing resource availability. We argue that the ability of individual howler monkeys to inhabit low-quality environments does not guarantee the long-term persistence of the small populations that live under these conditions. Their local extirpation explains why few forest fragments below a given area threshold are frequently inhabited in landscapes where recolonization and gene flow are compromised by long isolation distances or less permeable matrices. In sum, howlers’ ability to cope with habitat restriction at the individual level in the short-term may mask the inevitable fate of isolated populations, thereby compromising the persistence of the species at a regional scale in the long-term if howlers’ need for protection in large forests is undervalued.
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en Negative impacts of discrete, short‐term disturbances to wildlife populations are well‐documented. The consequences of more gradual environmental change are less apparent and harder to study because they play out over longer periods and are often indirect in their action. Yet, they can drive the decline of wildlife populations even in seemingly pristine and currently well‐protected habitats. One such environmental change is a successional shift in a community's species composition as it regenerates from disturbance caused by past human land use. Early and middle successional tree species often provide key foods to folivores and frugivores, but the abundance of these resources drops as the forest matures, with adverse repercussions for these consumers. Our 44‐year record (1974–2018) of howler monkey (Alouatta palliata ) group sizes and demographic composition from Barro Colorado Island, Panama, a protected reserve, documents an example of this phenomenon. After 70 years of relative stability, the mean size of howler monkey groups exhibited a marked decline, beginning in 2003. This downward trajectory in group size has continued through the most recent census in 2018. The composition of howler groups also changed significantly during the study period, with the patterns of decline differing among age/sex classes. There is no evidence that these changes were caused by increased rates of emigration, group fission, predation, parasitism, or disease. Rather, they are best explained by an island‐wide, succession‐driven decline in the densities of two species of free‐standing fig trees, Ficus yoponensis and F. insipida , which together were providing ~36% of BCI howlers’ annual diet. Abstract in Spanish is available with online material. Resumen fr Los impactos negativos de perturbaciones cortas y discretas en las poblaciones de fauna silvestres han sido bien documentadas. Las consecuencias de cambios ambientales más graduales son menos aparentes y más difíciles de estudiar por su efecto a largo plazo y su acción indirecta. Sin embargo, estos cambios pueden influir en las poblaciones de fauna silvestres, incluso en hábitats protegidos. Uno de tales cambios ambientales es el cambio sucesional en la composición de especies durante la regeneración de una comunidad tras una perturbación causada por el pasado uso humano de la tierra. Los árboles típicos de las etapas sucesionales iniciales e intermedias proveen alimentos clave para folívoros y frugívoros, pero la abundancia de estos recursos baja conforme el bosque madura, con repercusiones adversas para estos consumidores. Nuestro registro de monos aulladores (Alouatta palliata ) durante 44 años (1974–2018), con respeto a su tamaño de grupo y composición demográfica en la Isla Barro Colorado, Panamá, una reserva protegida, documenta un ejemplo de este fenómeno. Después de 70 años de estabilidad relativa, el promedio del tamaño de grupos de monos aulladores muestra una caída desde 2003. Esta trayectoria negativa en el tamaño del grupo ha continuado hasta el censo mas reciente en 2018. La composición de grupos de monos aulladores también ha cambiado significativamente durante el periodo estudiado, con los patrones de disminución que difieren entre las clases de edad/sexo. No hay evidencia que estos cambios hayan sido causados por un aumento de emigración, fisión de grupos, depredación, parasitismo, o enfermedades. En cambio, la tendencia es mejor explicada por la disminución de densidad de dos especies de árboles, Ficus yoponensis y F. insípida , causada por sucesión a nivel de toda la isla, que juntos proveen ~36% de la dieta anual de los monos aulladores en la isla.
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The natural transmission cycle of Yellow Fever (YF) involves tree hole breeding mosquitoes and a wide array of nonhuman primates (NHP), including monkeys and apes. Some Neotropical monkeys (howler monkeys, genus Alouatta) develop fatal YF virus (YFV) infections similar to those reported in humans, even with minimum exposure to the infection. Epizootics in wild primates may be indicating YFV circulation, and the surveillance of such outbreaks in wildlife is an important tool to help prevent human infection. In 2001, surveillance activities successfully identified YF-related death in a black-and-gold howler monkey (Alouatta caraya), Rio Grande do Sul State (RGS) in southern Brazil, and the YFV was isolated from a species of forest-dwelling mosquito (Haemagogus leucocelaenus). These findings led the State Secretariat of Health to initiate a monitoring program for YF and other 18 arboviral infections in Alouatta monkeys. The monitoring program included monkey captures, reporting of monkey casualties by municipalities, and subsequent investigations. If monkey carcasses were found in forests, samples were collected in a standardized manner and this practice resulted in increased reporting of outbreaks. In October 2008, a single howler monkey in a northwestern RGS municipality was confirmed to have died from YF. From October 2008 to June 2009, 2,013 monkey deaths were reported (830 A. caraya and 1,183 A. guariba clamitans). Viruses isolation in blood, viscera, and/or immunohistochemistry led to the detection of YF in 204 of 297 (69%) (154 A. g. clamitans and 50 A. caraya) dead Alouatta monkeys tested. The number of municipalities with confirmed YFV circulation in howlers increased from 2 to 67 and 21 confirmed human cases occurred. This surveillance system was successful in identifying the largest YF outbreak affecting wild NHP ever recorded.
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A recent (2008-2009) outbreak of sylvatic yellow fever caused the death of seven people and over 2,000 howler monkeys (black-and-gold, Alouatta caraya, and brown, A. guariba clamitans) in the state of Rio Grande do Sul, Brazil, spreading panic among the population. The fear of the disease and the misinformation about its relationship with howler monkeys led inhabitants of several regions to exterminate these primates from the forests near their homes. In this paper we describe the theoretical background supporting the idea that howler monkeys play an important role in fighting yellow fever via the surveillance of virus circulation and stress that they are not responsible for the re-emergence of this African infectious disease, its transmission, or its fast spread through the highly fragmented landscape of the state of Rio Grande do Sul. We also describe how this scientific information has been used in the campaign "Protect our Guardian Angels" that was launched to inform the public and the media about the actual relationship of these regionally threatened species to the disease. The campaign is run and supported by educational, scientific, governmental (health-and environment-related) and religious institutions, and NGOs, an alliance in favor of biodiversity conservation and public health that has been effective in changing the quality of the news media, but that still requires a great effort to achieve the necessary level of population awareness.
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