Intra- and Intergroup Spatial Dynamics of a Pair-Living Singing Primate,Indri indri: A Multiannual Study of Three Indri Groups in Maromizaha Forest,Madagascar

International Journal of Primatology - Territorial pair-living species tend to occupy and defend stable areas, assumed to contain all the resources needed for the lifetime of the group....     

Effects of anthropogenic disturbance on indri (Indri indri) health in Madagascar

Anthropogenic habitat disturbance impairs ecosystem health by fragmenting forested areas, introducing environmental contamination, and reducing the quality of habitat resources. The effect of this disturbance on wildlife health is of particular concern in Madagascar, one of the world's biodiversity hotspots, where anthropogenic pressures on the environment remain high. Despite the conservation importance of threatened lemur populations in Madagascar, few data exist on the effects of anthropogenic disturbance on lemur health. To examine these impacts, indri (Indri indri) populations were evaluated from two forest reserves that differ in their exposure to anthropogenic disturbance. We compared the health status of 36 indri individuals from two sites: one population from a protected, undisturbed area of lowland evergreen humid forest and the other population from a reserve exposed to frequent tourism and forest degradation. Comparison of indri health parameters between sites suggests an impact of anthropogenic disturbance, including significant differences in leukocyte count and differential, 12 serum parameters, 6 trace minerals, and a higher diversity of parasites, with a significant difference in the presence of the louse, Trichophilopterus babakotophilus. These data suggest that indri living in disturbed forests may experience physiological changes and increased susceptibility to parasitism, which may ultimately impair reproductive success and survival.     

Evidence of genetic monogamy in the lemur Indri (Indri indri)

Monogamy is a rare strategy among mammals but relatively common among primates. The study of the evolution of monogamy in mammals and primates is lacking empirical studies that assess the relationship between a pair‐living social organization and genetic monogamy. Sexual or genetic monogamy can only be assessed by performing molecular analyses and investigating rates of extra‐pair paternity (EPP). Studying the occurrence of EPP can provide valuable insights into reproductive strategies and their adaptive value. The indri is a pair‐living primate that lives in stable groups. Their social units are composed of the reproductive pair and up to four more individuals, but extra‐pair copulation (EPC) can occur. This raises the question of whether this event may or may not lead to EPP. Here, we investigated whether a pair‐living social organization corresponds to genetic monogamy in indris (Indri indri). We analyzed the paternity of 12 offspring from seven pairs using a set of six microsatellite loci on fecal samples (mean number of alleles 11.7 ± 1.8 (mean ± standard deviation). We found that in 92% of cases the genetic profile of the offspring matched the paired male of the group for all the loci considered. In the only case of paternity mismatch, the paternity assignment remained inconclusive. Our results show that I. indri genetic monogamy is the norm and supports the hypothesis that pair‐living social organization is associated with low EPP rate. Also, our results are in contrast with the hypothesis of infertility as a reason to engage in EPC for this species.     

Isolation and characterization of 20 microsatellite marker loci from the Indri (Indri indri) genome

Twenty novel polymorphic microsatellite loci were isolated and characterized from the Indri, Indri indri, genome. Along with sequence data, this marker suite will be used in future studies to establish population structure throughout its range and to verify the proposed subspecific nomenclature. Gene diversity (0.760 and 0.783) and allelic richness (5.8 and 6.43) were estimated in the Betampona and Andasibe populations, respectively.     

Food, Feeding Behavior and Feeding Ecology of Nemerteans

The feeding biology of nemerteans is reviewed, new informationis presented, and the role of nemerteans in natural communitiesis discussed and evaluated. Most nemerteans are carnivorous,the majority feeding on live, often specific, prey, while someare scavengers. Macrophagous feeding is found in the Palaeonemertea,Heteronemertea and some of the Hoplonemertea; the more specializedsuctorial feeding is limited to five of the hoplonemertean families,and suspension feeding (omnivorous diet) occurs only in thehighly specialized symbiotic monogeneric Bdellonemertea. Feeding adaptations seem to be related to the nature and employmentof the proboscis, the dilatability of the mouth, and the structureof the anterior part of the digestive tract. The transport ofdissolved organic materials from seawater has been demonstrated,but its role in nemertean nutrition is just being contemplated.Present meager information on predation has shown nemerteansto have actually and potentially large effects on prey populationsand thus on the communities in which they live. As the feedingbiology of only a relative handful of species has been studied,much basic comparative research is needed before we can corroborateor refute our present ideas concerning the ecological rolesof nemerteans.     

Diet and feeding behaviour of Indri indri in a low-altitude rain forest

The diet and feeding behaviour of Indri indri were investigated in the Betampona Reserve, eastern Madagascar, over 12 months from February 2000 to February 2001. The highly folivorous diet of this species was confirmed--feeding on foliage (leaves and petioles) accounting for 82% of feeding records. Immature leaves were the preferred dietary item, but at times of relative scarcity mature leaves, fruit, seeds, flowers and bark were substituted. The indri were observed to feed on parts from 22 plant families, 37 genera and at least 42 species. The most important plant families in the diet of Indri were Lauraceae, Clusiaceae and Myristicaceae. Most feeding at Betampona was observed at 5-20 m above the forest floor amongst small (2.1-5.0 cm), oblique/horizontal supports (0-45 degrees). The indri spent 41.4% of their active period feeding most commonly in above-branch postures. Studies such as this are important for the development of conservation management plans for this endangered species.     

Comparative Analysis of the Vocal Repertoires of the Indri (Indri indri) and the Diademed Sifaka (Propithecus diadema)

International Journal of Primatology - Strepsirrhine vocalisations are extraordinarily diverse and cross-species comparisons are needed to explore how this variability evolved. We contributed to...     

The song of the Indris (Indri indri; Primates: Lemuroidea): Natural history,form, and function

The song of the largest Malagasy lemur was extensively studied in the field between 1972 and 1984. The song’s structure is described, and the role of song in the natural history of Indriis examined by relating the naturally occurring variability of different song parameters to the behavior of habituated groups and the composition of other groups in the population. The function of an Indrigroup’s song is complex, varying according to the location and identity of animals hearing it. Territorial aspects of the song are considered in detail and the nature of primate territorial vocalizations is critically discussed.     

Madagascar Fish Eagle productivity in the Tsimembo-Manambolomaty Protected Area and surrounding habitat of western Madagascar

We monitored the productivity of the critically endangered Madagascar Fish Eagle Haliaeetus vociferoides inside and outside of the Tsimembo-Manambolomaty Protected Area (T-M PA), western Madagascar from 2010 to 2015. We recorded 14 breeding pairs inside and 13 outside T-M PA. The T-M PA and surrounding habitat hosted respectively 10 and six breeding polyandrous pairs, composed of one adult female and two adult males. During the six-year study period, 101 eggs were laid in nests in T-M PA of which 60 hatched and 58 young fledged. We recorded 62 eggs laid in nests outside the T-M PA of which 39 hatched and 36 young fledged. Productivity was similar at both sites, inside and outside T-M PA, with 0.84 (58/69) and 0.76 (36/47) fledgling per nesting attempt and 0.69 (58/84) and 0.5 (36/72) fledglings per territorial pair, respectively. Polyandrous pairs have higher productivity compared with normal pairs. Threats to Madagascar Fish Eagles and their habitat were low due to the existence of a community-based resource management system called the Local Management Secured System (GELOSE) inside and outside the T-M PA. This system is based on strengthening local traditional customs and rules, and involving local people in managing their natural resources sustainably along with biodiversity conservation.     

The Breeding Ecology of a Critically Endangered Salamander,Hynobius amjiensis(Caudata:Hynobiidae),Endemic to Eastern China

Hynobius amjiensis is a critically endangered salamander species(IUCN Red List) endemic to eastern China. It currently has three known populations: one in Longwangshan, Zhejiang Province(type locality), and two in Qingliangfeng between Anhui and Zhejiang Provinces. We examined the relatively unstudied breeding ecology of this species in the field and at laboratory from March 2007 to May 2014. Adult males and females were year-round terrestrial, except for the February–April breeding season. During this period, we captured only a total of 16 breeding adults(11 males and 5 females). As few as 100 breeding females were estimated based on the number of egg sacs observed since 2007. This number was significantly reduced from the estimated number between 1992 and 1998. Males(mean total length = 16.21 cm, mean body mass = 18.8 g) were slightly smaller than females(16.51 cm, 19.2 g). Size of breeding pools ranged from 0.2 m~2 to 1.2 m~2(0.1–1.2 m depths). Each female deposits a pair of egg sacs by attaching the adhesive tips of the sacs to aquatic plants or dead twigs. Fifteen pairs of egg sacs had an average length of 28.6 cm and a diameter of 3.3 cm. On average, each egg sac contained 75 eggs with a diameter of 0.3 cm. Our field survey revealed that H. amjiensis used oviposition sites in small, cool, and weakly acidic pools at high elevations(1 300–1 600 m) where peat moss was abundant. Reduction in wetland size and disappearance of suitable breeding pools suggest that this salamander species is under threat of extinction, particularly at Longwangshan, where 5 of the 9 breeding pools have either dried up or disappeared. Combined size of the remaining 4 pools is less than 2 m~2. We urge immediate implementation of more effective conservation measures and suggest that preservation priority should be given to habitat that contains suitable breeding pools.     

Feeding Ecology of Sympatric Mouse Lemur Species in Northwestern Madagascar

We performed a comparative pilot study on vertical space use and feeding ecology of 2 closely related sympatric mouse lemur species in northwestern Madagascar. We recorded feeding behavior and the use of vertical forest strata for 6 gray and 4 golden-brown mouse lemur females that we followed for 120 h. We carried out feeding experiments and analyzed fecal samples for food remains. Both species showed no significant difference in use of forest strata. They had a similar overall diet, with insect secretions and gum as main plant food resources; arthropod remains occurred in about half of all fecal samples. Both lemurs used in common >50% of the plant species that each consumed, which accounts for ≥70% of all individual plants used. However, both species used >40% of their feeding plant species exclusively and seemed to differ in their degree of specialization on certain plant species.     

Sexually dimorphic phrase organization in the song of the indris (Indri indri)

Animal acoustic communication often takes the form of complex sequences, composed of multiple distinct acoustic units, which can vary in their degree of stereotypy. Studies of sequence variation may contribute to our understanding of the structural flexibility of primates' songs, which can provide essential ecological and behavioral information about variability at the individual, population, and specific level and provide insights into the mechanisms and drivers responsible for the evolutionary change of communicative traits. Several methods have been used for investigating different levels of structural information and sequence similarity in acoustic displays. We studied intra and interindividual variation in the song structuring of a singing primate, the indri (Indri indri), which inhabits the montane rain forests of Madagascar. Indri groups emit duets and choruses in which they combine long notes, short single units, and phrases consisting of a variable number of units (from two to six) with slightly descending frequency. Males' and females' contributions to the song differ in the temporal and frequency structure of song units and repertoire size. We calculated the similarity of phrase organization across different individual contributions using the Levenshtein distance, a logic distance that expressed the minimum cost to convert a sequence into another and can measure differences between two sequences of data. We then analyzed the degree of similarity within and between individuals and found that: (a) the phrase structure of songs varied between reproductive males and females: female structuring of the song showed a higher number of phrases if compared to males; (b) male contributions to the song were overall more similar to those of other males than were female contributions to the song of other females; (c) male contributions were more stereotyped than female contributions, which showed greater individual flexibility. The picture emerging from phrase combinatorics in the indris is in agreement with previous findings of rhythmic features and song repertoire size of the indris, which also suggested that female songs are potentially less stereotyped than those of males.     

Population and Conservation Genetics in an Endangered Lemur, <Emphasis Type="Italic">Indri indri</Emphasis>, Across Three Forest Reserves in Madagascar

Population decline and fragmentation often lead to reduced genetic diversity and population differentiation. Habitat destruction throughout Madagascar has caused population decline and extinction of many endemic species. Lemur populations, including those of the largest extant lemur, Indri indri, have been fragmented into remaining forest patches. We assessed the level of genetic diversity in indri populations in three protected reserves by genotyping a total of 43 individuals at 17 microsatellite loci. Genetic diversity in terms of heterozygosity was high in all three reserves, with no differences between reserves. Population structure and F _ST analyses revealed Analamazaotra Forest Station and the Torotorofotsy Conservation Area, which are separated by ca. 18 km to be genetically differentiated from each other with some admixture. Betampona Strict Nature Reserve, which is separated from the other reserves by ca. 130 km, exhibited clear population genetic differentiation, with no signs of admixture with the other reserves. Our genetic diversity estimates are similar to those for other Indridae in similar habitats and may reflect past rather than current population processes, given that populations have declined recently. Our results suggest that Betampona may be genetically isolated and that it is important to maintain gene flow between remaining populations to prevent loss of genetic diversity for the future conservation of Indri indri.     

Reproductive Behavior, Captive Breeding, and Restoration Ecology of Endangered Fishes

Species recovery efforts generally focus on in situ actions such as habitat protection. However, captive breeding can also provide critical life history information, as well as helping supplement existing or restoring extirpated populations. We have successfully propagated nine species in captivity, including blackside dace, spotfin chubs, bloodfin darters, and boulder darters. Threatened blackside dace, Phoxinus cumberlandensis, were induced to spawn in laboratory aquaria by exposing them to milt from a reproductively mature male stoneroller, Campostoma anomalum or river chub, Nocomis micropogon. The latter are nest-building minnows, with which Phoxinus may spawn in nature. Eggs are broadcast among gravel and pebbles. Blackside dace individuals reared in captivity were used for translocation. Threatened spotfin chubs, Cyprinella monacha, fractional crevice spawners, deposited eggs in laboratory aquaria in the spaces created between stacks of ceramic tiles. Captively produced spotfin chubs were used as part of a larger stream restoration and fish reintroduction project in the Great Smoky Mountains National Park. The bloodfin darter, Etheostoma sanguifluum, was first used as a surrogate to develop techniques for spawning a closely related species, the endangered boulder darter, E. wapiti. Both darter species mated in a wedge created between two ceramic tiles. Our efforts have had variable but generally high success, with survival rates of 50–90% of eggs deposited. Captive production of nongame fishes can aid recovery of rare species or populations, aid in watershed restoration, and can help to refine water quality standards. In addition, captive breeding allows discovery of important behavioral or life history characteristics that may constrain reproduction of rare species in altered natural habitats.     

An ethmoid exposure (os planum) in the orbit of Indri indri (Primates, Lemuriformes).

In 6 of 17 skulls of Indri indri retaining distinct sutures in the medial orbital wall, a small separate bony element intervenes between the frontal and the maxillolacrimal suture. This element is demonstrably continuous with the ethmoid on one such skull. The occurrence of an ethmoid exposure in the orbit of Indri suggests that this trait is not a simple function of orbital size and convergence. Since such an exposure is found in non-cheirogaleine lemuriforms, its distribution provides no support for the hyothesis that lorises and galagos are derived from cheirogaleines.     

Human-Assisted Spread of a Maladaptive Behavior in a Critically Endangered Bird

Conservation management often focuses on counteracting the adverse effects of human activities on threatened populations. However, conservation measures may unintentionally relax selection by allowing the ‘survival of the not-so-fit’, increasing the risk of fixation of maladaptive traits. Here, we report such a case in the critically-endangered Chatham Island black robin (Petroica traversi) which, in 1980, was reduced to a single breeding pair. Following this bottleneck, some females were observed to lay eggs on the rims of their nests. Rim eggs left in place always failed to hatch. To expedite population recovery, rim eggs were repositioned inside nests, yielding viable hatchlings. Repositioning resulted in rapid growth of the black robin population, but by 1989 over 50% of all females were laying rim eggs. We used an exceptional, species-wide pedigree to consider both recessive and dominant models of inheritance over all plausible founder genotype combinations at a biallelic and possibly sex-linked locus. The pattern of rim laying is best fitted as an autosomal dominant Mendelian trait. Using a phenotype permutation test we could also reject the null hypothesis of non-heritability for this trait in favour of our best-fitting model of heritability. Data collected after intervention ceased shows that the frequency of rim laying has strongly declined, and that this trait is maladaptive. This episode yields an important lesson for conservation biology: fixation of maladaptive traits could render small threatened populations completely dependent on humans for reproduction, irreversibly compromising the long term viability of populations humanity seeks to conserve.     

Novel Data on the Ecology of Cochranella mache (Anura: Centrolenidae) and the Importance of Protected Areas for This Critically Endangered Glassfrog in the Neotropics

We studied a population of the endangered glassfrog, Cochranella mache, at Bilsa Biological Station, northwestern Ecuador, from 2008 and 2009. We present information on annual abundance patterns, behavioral ecology, habitat use and a species distribution model performed with MaxEnt. We evaluate the importance of the National System of Protected Areas (SNAP) in Colombia and Ecuador, under scenarios of climate change and habitat loss. We predicted a restricted environmental suitability area from 48,509 Km² to 65,147 Km² along western Ecuador and adjacent Colombia; ∼8% of the potential distribution occurs within SNAP. We examined four aspects of C. mache ecology: (1) ecological data suggests a strong correlation between relative abundance and rainfall, with a high probability to observe frogs through rainy months (February–May); (2) habitat use and the species distribution model suggest that this canopy dweller is restricted to small streams and rivulets in primary and old secondary forest in evergreen lowland and piedmont forest of western Ecuador, with predictions of suitability areas in adjacent southern Colombia; (3) the SNAP of Colombia and Ecuador harbor a minimum portion of the predicted model of distribution (<10%); and (4) synergetic effects of habitat loss and climate change reduces in about 95% the suitability areas for this endangered frog along its distributional range in Protected Areas. The resulting model allows the recognition of areas to undertake conservation efforts and plan future field surveys, as well as forecasting regions with high probability of C. mache occurrence in western Ecuador and southern Colombia. Further research is required to assess population tendencies, habitat fragmentation and target survey zones to accelerate the discovery of unknown populations in unexplored areas with high probability of suitability. We recommend that Cochranella mache must be re-categorized as “Critically Endangered” species in national and global status, according with criteria and sub-criteria A4, B1ab(i,ii,iii,iv),E.     

The Impact of Forest Disturbance on the Seasonal Foraging Ecology of a Critically Endangered African Primate

Forest loss and fragmentation threaten many primates globally, and often leads to a reduction in food resources. During a 22 ‐ mo period, the foraging ecology of the critically endangered kipunji Rungwecebus kipunji was studied in the heterogeneous Rungwe–Livingstone forests, southwest Tanzania, to identify periods of possible ecological stress, fallback foods used by the species, and the impact of forest disturbance on feeding resources. The studied group had a wide diet and was predominantly frugivorous. Fruit consumption was driven by fruit availability which peaked during the wet season, and dipped during the driest months. During this period, two fallback foods: mature leaves and pith were widely consumed, with Macaranga capensis an essential fallback species. α diversity and evenness of diet was remarkably similar across months, but there was high β diversity in diets at the cusp of wet and dry seasons, and during periods of low fruit availability. This suggests considerable dietary adaptability to fluctuating resources, which may act to buffer against further forest disturbance. Tree species associated with relatively undisturbed forest were significantly more important in the diet, especially in the dry season, than those of disturbed forests. Regeneration of key trees (determined through counting of seedlings and saplings in plots) appeared healthy except in two important Ficus species. Conservation management, while focusing on promoting old growth forest, should also consider populations of some important pioneer tree species such as Macaranga capensis both inside the forest and in any reforestation schemes outside the species’ current area of occupancy.     

Tourism and the Conservation of Critically Endangered Frogs

Protected areas are critical for the conservation of many threatened species. Despite this, many protected areas are acutely underfunded, which reduces their effectiveness significantly. Tourism is one mechanism to promote and fund conservation in protected areas, but there are few studies analyzing its tangible conservation outcomes for threatened species. This study uses the 415 IUCN critically endangered frog species to evaluate the contribution of protected area tourism revenue to conservation. Contributions were calculated for each species as the proportion of geographic range inside protected areas multiplied by the proportion of protected area revenues derived from tourism. Geographic ranges were determined from IUCN Extent of Occurrence maps. Almost 60% (239) of critically endangered frog species occur in protected areas. Higher proportions of total range are protected in Nearctic, Australasian and Afrotopical regions. Tourism contributions to protected area budgets ranged from 5–100%. These financial contributions are highest for developing countries in the Afrotropical, Indomalayan and Neotropical regions. Data for both geographic range and budget are available for 201 critically endangered frog species with proportional contributions from tourism to species protection ranging from 0.8–99%. Tourism''s financial contributions to critically endangered frog species protection are highest in the Afrotropical region. This study uses a coarse measure but at the global scale it demonstrates that tourism has significant potential to contribute to global frog conservation efforts.