Examination of the Taxonomy and Diversification of <Emphasis Type="Italic">Leontopithecus</Emphasis> using the Mitochondrial Control Region

Leontopithecus comprises 4 taxa: black lion tamarins (L. chrysopygus), golden lion tamarins (L. rosalia), black-faced lion tamarins (L. caissara), and golden-headed lion tamarins (L. chrysomelas). Endemic to the Atlantic Forest of Brazil, they are endangered (Appendix I, CITES; IUCN Critically Endangered: Leontopithecus chrysopygus, L. caissara; IUCN Endangered: L. rosalia, L. chrysomelas). The 4 taxa are differentiated morphologically and geographically and occupy different habitat types. However, it is not clear if all of them are separate species, particularly Leontopithecus caissara, or how they are related to one another evolutionarily. Therefore, we investigated lion tamarin differentiation and radiation. We sequenced the mtDNA control region and performed phylogenetic analyses, population aggregation analyses, and Mantel tests for geographic/genetic correlation. Mitochondrial genetic data suggest 3 distinct lion tamarin clades (Leontopithecus chrysomelas; L. caissara; and L. chrysopygus/L. rosalia). Phylogenetic analysis also supports: 1) the basal lion tamarin is Leontopithecus chrysomelas, and not L. chrysopygus, 2) L. caissara is not subspecific to L. chrysopygus, and 3) Quaternary forest refugia may have shaped lion tamarin diversification via a pattern that does not follow the theory of metachromism. Even though mitochondrial genetic analyses do not unequivocally support the 4 lion tamarins as separate species, one should consider the 4 lion tamarins, with equal conservation priority based on the combination of morphological, genetic, and habitat differentiation. Each of them is an extremely valuable flagship species that focuses attention on the diminishing, highly endemic Atlantic Forest of Brazil.     

Craniometric sexual dimorphism inLeontopithecus Lesson, 1840 (Callitrichidae, Primates)

Lion tamarins are among the World's most critically endangered primates. Many studies have been produced under guidance of the International Management Committees for the preservation and management of these tamarins. Primates present morphological sexual differences in a wide range of characteristics, including cranial morphology. Studies of sexual dimorphism in the cranial morphology of theLeontopithecus are few in number and contradictory in their results. In order to check for the existence of sexual dimorphism in lion tamarins the present study analyzed 17 craniometric distances on 56 crania of three species of lion tamarins (Leontopithecus): 20L. rosalia (14 females and 6 males); 13L. chrysomelas (6 females and 7 males); and 23L. chrysopygus (8 females and 15 males). All crania are housed in the CPRJ-FEEMA collection (Primatological Center of Rio de Janeiro) and came from animals born in captivity.L. chrysopygus was more sexually dimorphic (10/17 measurements, 59%) thanL. chrysomelas (9/17 measurements, 53%) orL. rosalia (7/17 measurements, 41%). In all three species, male values are greater than the female ones, except for orbital breadth (m7) inL. rosalia. However, this distance is not sexually dimorphic in this species. This study reveals that some cranial distances, especially in the facial region, are sexually dimorphic in lion tamarins.     

Color Vision in <Emphasis Type="Italic">Leontopithecus chrysomelas</Emphasis>: A Behavioral Study

We assessed the color discriminations by golden-headed lion tamarins (Leontopithecus chrysomelas) via a series of tasks involving a behavioral paradigm that maximizes the naturalness of the stimuli. The stimuli were pairs of Munsell color chips used in earlier experiments with human dichromats. We tested 3 male and 3 female monkeys with stimuli of random brightness values in order to assure that discriminations were based on color rather than brightness cues. Results indicate that each male and one female presented random performances for stimuli resembling hue conditions under which tamarins forage: oranges vs. greens. Two females exhibited discriminations consistent with allelic trichromacy. Findings indicate the presence of an M/L cone opsin polymorphism, a condition of most platyrrhines that is characterized by dichromatic and/or trichromatic females and dichromatic males. Interspecific differences in allelic frequency among lion tamarins raises the possibility that habitat fragmentation is affecting heterozygous frequencies, a trend that could impact tamarin foraging efficiency.     

Infection with Trypanosoma cruzi TcII and TcI in free-ranging population of lion tamarins (Leontopithecus spp): an 11-year follow-up

Here, we present a review of the dataset resulting from the 11-years follow-up of Trypanosoma cruzi infection in free-ranging populations of Leontopithecus rosalia (golden lion tamarin) and Leontopithecus chrysomelas (golden-headed lion tamarin) from distinct forest fragments in Atlantic Coastal Rainforest. Additionally, we present new data regarding T. cruzi infection of small mammals (rodents and marsupials) that live in the same areas as golden lion tamarins and characterisation at discrete typing unit (DTU) level of 77 of these isolates. DTU TcII was found to exclusively infect primates, while TcI infected Didelphis aurita and lion tamarins. The majority of T. cruzi isolates derived from L. rosalia were shown to be TcII (33 out 42) Nine T. cruzi isolates displayed a TcI profile. Golden-headed lion tamarins demonstrated to be excellent reservoirs of TcII, as 24 of 26 T. cruzi isolates exhibited the TcII profile. We concluded the following: (i) the transmission cycle of T. cruzi in a same host species and forest fragment is modified over time, (ii) the infectivity competence of the golden lion tamarin population fluctuates in waves that peak every other year and (iii) both golden and golden-headed lion tamarins are able to maintain long-lasting infections by TcII and TcI.     

Cross-generic Food Sharing in Tamarins

Adult-infant food-sharing behavior is a major component of the infant care strategies of callitrichids (marmosets and tamarins). It is particularly well-developed in cotton-top tamarins (Saguinus Oedipus) and lion tamarins (Leontopithecus spp), which show frequent adult-initiated food offering, as well as sharing of food in response to begging by infants. This report documents a case of cross-generic food sharing, in which a male golden-headed lion tamarin (Leontopithecus chrysomelas) shared food with an infant cotton-top tamarin. The lion tamarin provided more food to the infant than its mother did. This emphasizes the importance of this behavior in the reproductive strategies of the communally-rearing Callitrichidae and raises questions about mechanisms that underly it.     

Conspecific and heterospecific attraction in assessments of functional connectivity

Functional connectivity is known to have an important, positive influence on species persistence. Measurements of functional connectivity traditionally focus on structural attributes of landscapes such as the distance and matrix type between habitat patches as well as on how species interact with those structural attributes. However, we propose that the social behavior of a species, through conspecific and heterospecific attraction, will also impact connectivity by changing how dispersers move with respect to each other and occupied patches. We analyzed functional connectivity patterns using circuit and graph theory for golden-headed lion tamarins (Leontopithecus chrysomelas) in Brazil under three scenarios. In the first scenario, we looked at connectivity without the effects of attraction under varying maximum dispersal distance and ecological movement cost thresholds. In the second scenario, we allowed dispersers to travel over more hostile matrix than they normally would to reach an occupied patch. In the final scenario, we allowed dispersers to move only to occupied patches. We found that, according to the first scenario, range-wide functional landscape connectivity for golden-headed lion tamarins is low at realistic maximum dispersal distance and movement cost thresholds. Incorporating the effects of conspecific or heterospecific attraction would increase functional connectivity, in the case of scenario two, or decrease functional connectivity, in the case of scenario three. Because conspecific/heterospecific attraction can have an impact on movement for some species, this factor should be incorporated in assessments of functional connectivity patterns for social species and others where patch occupancy is likely to influence the movements of dispersers.     

Long-call structure and its relation to taxonomy in lion tamarins

Recent evidence on craniodental morphology suggests the acceptance of three species of lion tamarins (Leontopithecus). Confirmatory evidence is presented here using the morphology of long-call vocalizations recorded from several individuals of each type of lion tamarin. Recordings were made of Leontopicthecus rosalia, Leontopithecus chrysopygus, and Leontopithecus chrysomelas at the Centro de Primatologia do Rio de Janeiro (FEEMA) and of L. rosalia at Monkey Jungle in Florida. Thirty separate parameters were measured, and 17 of them differed significantly between populations. In general, L. chrysomelas had higher pitched calls with shorter note duration, while L. chrysopygus, the larger of the animals, had lower pitched calls with longer note duration. L. rosalia was either intermediate to the other two populations or resembled L. chrysopygus. Thus, the results from the analysis of vocal structures closely paralleled the results obtained with more traditional taxonomic methods and suggests that the quantitative analysis of vocal strucures can be a useful adjunct in taxonomy.     

Assessing Extinction Risk in Small Metapopulations of Golden‐headed Lion Tamarins (Leontopithecus chrysomelas) in Bahia State,Brazil

Golden‐headed lion tamarins (GHLTs; Leontopithecus chrysomelas) are endangered primates endemic to the Brazilian Atlantic Forest, where loss of forest and its connectivity threaten species survival. Understanding the role of habitat availability and configuration on population declines is critical for guiding proactive conservation for this, and other, endangered species. We conducted population viability analysis to assess vulnerability of ten GHLT metapopulations to habitat loss and small population size. Seven metapopulations had a low risk of extirpation (or local extinction) over the next 100 years assuming no further forest loss, and even small populations could persist with immediate protection. Three metapopulations had a moderate/high risk of extirpation, suggesting extinction debt may be evident in parts of the species’ range. When deforestation was assumed to continue at current rates, extirpation risk significantly increased while abundance and genetic diversity decreased for all metapopulations. Extirpation risk was significantly negatively correlated with the size of the largest patch available to metapopulations, underscoring the importance of large habitat patches for species persistence. Finally, we conducted sensitivity analysis using logistic regression, and our results showed that local extinction risk was sensitive to percentage of females breeding, adult female mortality, and dispersal rate and survival; conservation or research programs that target these aspects of the species’ biology/ecology could have a disproportionately important impact on species survival. We stress that efforts to protect populations and tracts of habitat of sufficient size throughout the species’ distribution will be important in the near‐term to protect the species from continuing decline and extinction.     

Census and distribution of the golden lion tamarin (Leontopithecus rosalia)

During 1990–1992, a survey of the golden lion tamarin, Leontopithecus rosalia, was carried out throughout its known distribution area. Forest remnants were identified by visual interpretation of Landsat‐TM satellite images. Localities occupied by L. rosalia were first identified by interviews with local people. All forests more than 20 ha in size, and for which two or more interviews suggested the presence of the species, were surveyed using “play‐back” recordings of lion tamarin long calls. The total wild population of L. rosalia, including that of the Poço das Antas Biological Reserve, was estimated to be 562 individuals in 109 groups. The lion tamarins were generally found in four major areas of forest (six or more groups per forest, not including Poço das Antas), with a further 12 groups isolated in small forest patches. Currently the species' distribution is restricted to just four municipalities in the state of Rio de Janeiro: Silva Jardim, Cabo Frio, Saquarema, and Araruama. Although they are typically confined to lowland forest of <300 m altitude, L. rosalia was recorded at an altitude of 550 m in one locality. Average group size varied from 3.6 to 5.7 individuals, and densities from 0.39 groups/km² to 2.35 groups/km² (2.17 individuals/ km² to 8.53 individuals/km²). Six of the isolated groups found during the survey were successfully translocated to a forest of 2,400 ha. There is now also a significant population of reintroduced lion tamarins. Overall, however, the possibilities for further expansion of the wild population are severely limited. Am. J. Primatol. 59:29–44, 2003. © 2003 Wiley‐Liss, Inc.     

Integrating climate and landscape models to prioritize areas and conservation strategies for an endangered arboreal primate

Species distributions are influenced by both climate conditions and landscape structure. Here we propose an integrated analysis of climatic and landscape niche-based models for a forest-dependent primate, the endangered black lion tamarin (Leontopithecus chrysopygus). We applied both climate and landscape variables to predict the distribution of this tamarin and used this information to prioritize strategic areas more accurately. We anticipated that this approach would be beneficial for the selection of pertinent conservation strategies for this flagship species. First, we built climate and landscape niche-based models separately, combining seven algorithms, to infer processes acting on the species distribution at different scales. Subsequently, we combined climate and landscape models using the EcoLand Analysis. Our results suggest that historic and current landscape fragmentation and modification had profoundly adverse effects on the distribution of the black lion tamarins. The models indicated just 2096 km² (out of an original distribution of 92,239 km²) of suitable areas for both climate and landscape. Of this suitable area, the species is currently present in less than 40%, which represents less than 1% of its original distribution. Based on the combined map, we determined the western and southeast regions of the species range to be priority areas for its conservation. We identified areas with high climatic and high landscape suitability, which overlap with the remaining forest fragments in both regions, for habitat conservation and population management. We suggest that areas with high climatic but low landscape suitability should be prioritized for habitat management and restoration. Areas with high landscape suitability and low climatic suitability, such as the Paranapiacaba mountain range should be considered in light of projected climate change scenarios. Our case study illustrates that a combined approach of climatic and landscape niche-based modeling can be useful for establishing focused conservation measures that may increase the likelihood of success.     

Hepatocellular carcinoma in two captive golden‐headed lion tamarins (Leontopithecus chrysomelas)

Two cases of hepatocellular carcinoma (HCC) in 2 female captive golden‐headed lion tamarins (Leontopithecus chrysomelas) are described. HCC was diagnosed in both, with pulmonary metastasis in one of them. Neoplastic cells were positive for hepatocyte‐specific antigen (HSA) by immunohistochemistry, confirming the diagnosis.     

Mixed‐species Groups of Marmosets and Tamarins Across a Gradient of Agroforestry Intensification

Polyspecific associations are commonly observed in social animals, including primates, and have been interpreted as adaptations either to improve access to resources or to provide protection against predators. Mixed‐species associations between Wied's marmosets (Callithrix kuhlii) and golden‐headed lion tamarins (Leontopithecus chrysomelas) have been documented, and are unique among Atlantic forest primates. Both species are endemic to southern Bahia where part of the forest has been converted into cacao agroforests, which have been subjected to management intensification. Tree density and canopy connectivity decrease in more intensively managed agroforests, potentially increasing predation risk and the frequency of mixed‐species groups between these primates. Here, we test this hypothesis using a standardized, large spatial‐scale data set obtained from camera‐trapping in 30 sites across an agroforestry landscape mosaic. As expected, the frequency of mixed‐species groups increased in more intensively managed agroforests, but only relative to the total number of records of tamarins. Our results highlight that the benefits of mixed‐species groups can be asymmetrical among species and variable across the landscape. They corroborate that predation avoidance is an important advantage of mixed‐species groups in callitrichids, especially for conspicuous species living in smaller groups, such as the tamarin. Despite the importance of agroforests to conservation, our results indicate that management intensification can increase predation risk for species of conservation concern. To maintain the conservation value of agroforests, management practices should be planned to avoid any loss of canopy connectivity, taking into account the biodiversity vs. productivity trade‐off associated with shade management.     

Restoration Strategies to Improve Connectivity for Golden-Headed Lion Tamarins (<Emphasis Type="Italic">Leontopithecus chrysomelas</Emphasis>) in the Bahian Atlantic Forest,Brazil

Habitat loss and fragmentation are the leading causes of biodiversity decline world-wide. Animals sensitive to fragmentation experience reduced dispersal, breeding opportunities, and genetic diversity, making them vulnerable to local extinction. Over the last few decades the Atlantic Forest of Brazil has been extremely fragmented, with only 11–16% of forest remaining. The Brazilian government and nongovernmental organizations have taken actions through legislation and conservation initiatives to restore forest. Using computer modeling, we compared how alternative forest restoration strategies could improve functional connectivity for golden-headed lion tamarins (Leontopithecus chrysomelas) in Southern Bahia, Brazil. Strategies differed by restoration configuration, including Within- and Across-Property approaches, and restoration amount (0–20% restoration). Increasing restoration amounts resulted in greater species functional connectivity, and Within-Property and Across-Property strategies both had significantly more connectivity than the Random strategy. We suggest restoration management consider the size and placement of restored forest, and that riparian forest be restored first to create dispersal corridors and reestablish essential ecosystem services. We further suggest the importance of forming canopy bridges across narrow sections of rivers during the early stages of the restoration process to promote increased connectivity of these newly restored areas. Our findings can aid managers and landowners in understanding the implications of different restoration strategies for highly arboreal, matrix-sensitive species.     

基于“空间形态-破碎化-聚集度”的粤港澳大湾区森林景观格局时空演变

森林景观格局的时空演变研究能够帮助理解区域森林变化过程。传统的景观指数方法多以均值为计算结果且空间信息表达不足，基于形态学方法能够从空间上直观辨别景观类型，综合破碎化和聚集度的定量分析有助于进一步认识森林景观格局的演变特征。以1990、2000、2010、2020年粤港澳大湾区土地利用数据为基础，建立基于“空间形态-破碎化-聚集度”的综合研究框架，开展大湾区森林景观格局的时空演变研究。结果表明：(1)近30年大湾区森林形态以核心区为主，森林面积逐渐减少，而2010—2020年减少速率降低，各类型森林斑块均有所恢复；(2)整体破碎化程度较低，中部破碎化地区表现为先上升后下降的变化趋势；(3)聚集度结果表明，距离森林边界500 m内的森林斑块面积最大，约占研究区总面积的30%,而距离大于4.5 km的非森林斑块面积几乎翻倍增加，应重点关注该区域的森林损失。研究有助于全面理解森林景观格局的变化特征，相关结果可为粤港澳大湾区的森林生态修复工程、国土空间规划以及城市可持续发展提供科学依据。     

Remnants fragments preserve genetic diversity of the old forest lichen <Emphasis Type="Italic">Lobaria pulmonaria</Emphasis> in a fragmented Mediterranean mountain forest

Fragmentation represents a serious threat to biodiversity worldwide, however its effects on epiphytic organisms is still poorly understood. We study the effect of habitat fragmentation on the genetic population structure and diversity of the red-listed epiphytic lichen, Lobaria pulmonaria, in a Mediterranean forest landscape. We tested the relative importance of forest patch quality, matrix surrounding fragments and connectivity on the genetic variation within populations and the differentiation among them. A total of 855 thalli were sampled in 44 plots (400 m²) of 31 suitable forest fragments (beeches and oaks), in the Sierra de Ayllón in central Spain. Variables related to landscape attributes of the remnant forest patches such as size and connectivity and also the nature of the matrix or tree species had no significant effects on the genetic diversity of L. pulmonaria. Values of genetic diversity (Nei’s) were only affected by habitat quality estimated as the age patches. Most of the variation (76%) in all populations was observed at the smallest sampled unit (plots). Using multiple regression analysis, we found that habitat quality is more important in explaining the genetic structure of the L. pulmonaria populations than spatial distance. The relatively high level of genetic diversity of the species in old forest patches regardless of patch size indicates that habitat quality in a highly structured forest stand determines the population size and distribution pattern of this species and its associated lichen community. Thus, conservation programmes of Mediterranean mountain forests have to prioritize area and habitat quality of old forest patches.     

广西黑叶猴栖息地景观格局破碎化分析及其对种群的影响

黑叶猴(Trachypithecus francoisi)是仅分布于喀斯特石山生境的珍稀濒危灵长类动物。由于非法捕杀和人类活动干扰,其种群数量正在急剧减少。同时,随着森林砍伐和土地开垦的加速,其栖息地严重破碎化。因此,了解栖息地破碎化对黑叶猴种群的影响对于保护这一珍稀濒危物种具有重要意义。基于遥感影像、土地利用数据以及黑叶猴种群调查数据,通过Fragstats软件开展广西黑叶猴栖息地景观破碎化分析,并通过相关性和多元逐步回归分析,探讨了景观格局对广西黑叶猴种群数量的影响。结果表明：(1)广西黑叶猴栖息地呈现破碎化严峻、斑块形状复杂化、斑块团聚程度较弱且分散化的现象;栖息地以林地景观占据重要优势,但人为景观的干扰十分强烈;在不同地区中,生境破碎化程度、人为干扰强度以及景观配置均呈现不同的特征,其中扶绥地区人为干扰最为强烈,德保地区的景观块数破碎化程度较为严重,而龙州地区的人为干扰程度最小,其森林景观最为聚集。(2)蔓延度指数、平均斑块分维指数、林地面积、林地斑块大小、裸岩面积和裸岩面积比重等景观指数与黑叶猴种群数量有显著正向关系,Shannon多样性指数则是显著负向关系;而耕地面积、耕地...     

宁夏黄河流域景观破碎化时空变化特征

基于RS和GIS技术,以土地利用数据为基础,采用有效粒度尺寸对宁夏黄河流域1985年和2010年的景观破碎化进行时空变化分析。结果显示:流域整体的有效粒度尺寸(meff)从1985年的6326.62 km2下降到2010年的2974.32 km2,破碎化程度呈显著加剧变化;从流域内部来看,景观破碎化程度最大的是黄左区间,破碎化程度最小的是苦水河和红柳沟;除引黄区间外,其余分区景观破碎化程度在25年间均有所加剧。特征尺度分析结果显示研究区景观破碎化空间变异分析的合适尺度为4500 m;景观破碎化指数的空间变异结果表明破碎化程度较大的区域面积明显多于破碎化程度弱的区域,景观破碎化空间异质性在25年间表现出明显的上升趋势。在海拔背景条件下,2400 m以下区域的景观破碎化程度较高,2400m以上区域破碎化程度较低,且随海拔的升高有降低的趋势;流域景观破碎化受人为干扰影响强烈,在人为干扰较强的1000—1500 m区段的景观破碎化程度最大;景观破碎化在时间上的变化受人为干扰影响产生的变化最为显著,由自然条件改变产生的影响有限。研究结果可为西北地区景观格局及景观破碎化的研究提供参考,并为区域景观格局优化和土地的有效管理提供依据。     

黔中喀斯特山地城市景观稳定性评价与特征分析

城市景观稳定性是对城市生态环境进行分析和评价的基础,对城市景观生态安全格局和景观可持续性具有十分重要的意义。以典型喀斯特山地城市贵阳市为研究对象,以2008年、2013年和2017年景观类型为主要数据。运用蔓延度指数、斑块密度和总边缘对比度构建景观稳定性评价模型,在分析2008-2017年景观格局变化状况的基础上评价景观稳定性时空特征。并运用探索性空间数据分析方法揭示贵阳市景观稳定性时空演变规律和冷热点特征。结果表明:(1)2008-2017年贵阳市景观格局发生剧烈变化,耕地面积大幅减少,林地和建设用地面积持续增加,景观破碎化程度加剧,但破碎化趋势有所减缓。(2)10年间,贵阳市景观稳定性水平整体较低,以不稳定和较不稳定为主,表现出"先降低、后提高,总体略有降低"的趋势。(3)贵阳市景观稳定性的空间分布与演变具有明显空间聚集效应,全局Moran''s I指数介于0.2008-0.4005之间,但聚集趋势呈"总体减弱,小幅提高"的特征;此外,景观稳定性热点区主要集中在城镇建设用地或林地斑块相对集中连片、完整的区域。研究结果可为喀斯特山地城市景观空间格局优化、生态安全网络格局构建和生态文明城市建设提供重要的科学依据。     

Associations Between Golden-Headed Lion Tamarins and the Bird Community in the Atlantic Forest of Southern Bahia

We examined the presence of birds accompanying and foraging in proximity to golden-headed lion tamarins at Una Biological Reserve, Bahia, Brazil. We followed 3 groups of golden-headed lion tamarins over 3 yr. We noted all birds ≤5 m of a lion tamarin during 20-min observation periods. We found 11 different bird species in the presence of the lion tamarins. We most often found insectivores, such as woodcreepers and nunbirds, in association with them, eating prey the tamarins flushed. Associations were most frequent in mature and shade-cocoa forests. The group that spent most of its time in mature and shade-cocoa forest was also the group that foraging birds followed most frequently. Differences in resource availability among forest types, such as the abundance of microforaging environments, may affect the frequency and diversity of birds seen in association with golden-headed lion tamarins.