Geographic variation in fruit colour is associated with contrasting seed disperser assemblages in a south‐Andean mistletoe

Fruit colour influences fruit choice by seed dispersers. The mistletoe Tristerix corymbosus (Loranthaceae) produces mature fruits of two different colours in two different biomes: yellow in the Chilean matorral and green in the temperate forest of southern South America. We conducted field surveys to establish the association between fruit colour and disperser identity throughout the entire geographical range of T. corymbosus. We selected 22 populations, eight of which were located in the Chilean matorral and 14 in the temperate forest south of the matorral. To identify the seed dispersers of the mistletoe we used direct observation, camera traps, and live‐trapping of small mammals. We also report experiments to assess fruit selection by seed dispersers based on differences in colour. The assemblages of dispersers of T. corymbosus differ between the two biomes: yellow fruits in Chilean matorral are exclusively dispersed by three bird species while green fruits in the temperate forest are exclusively dispersed by a marsupial. The differences in the assemblages of seed dispersers can be explained by differences in food‐finding strategies between the two assemblages. Green fruits in temperate forest are not easily detected by birds, while colour might not be an important cue for the marsupial because it is nocturnal and uses other senses to locate food. We propose that the association between the marsupial and the green‐fruited mistletoe constitutes an ecological fitting rather than the outcome of a co‐evolutionary process. The marsupial might have allowed the mistletoe T. corymbosus to retain green coloration in mature fruit, a condition to which it is preadapted by a slower ripening process in temperate forest populations.     

Energetics and torpor of a South American “living fossil”, the microbiotheriid<Emphasis Type="Italic"> Dromiciops gliroides</Emphasis>

We examined the energetics of the living fossil microbiotheriid Dromiciops gliroides, a nocturnal and rare small marsupial, endemic to the northern portion of the temperate forest of southern South America. We investigated the effects of changes at ambient temperature and food restriction on the energetics and patterns of torpor. We determined whether they exhibit shallow daily torpor or deep prolonged torpor like some Australian marsupials. Thermal conductance was 92.5% of the expected value for a similarly sized eutherian and basal metabolic rate was 82.9 and 58.6% of the predicted value for standard metatherians and eutherians, respectively. Euthermic D. gliroides showed daily fluctuations in body temperature, being significantly higher during the night. Dromiciops gliroides entered torpor and aroused spontaneously. The duration of torpor bouts increased in response to decreasing ambient temperature; torpor bout duration ranged from 10 h at 20 °C to 120 h at 12.5 °C. This study is the first record of deep torpor or hibernation for a South American mammal. Torpor in this species as well as in marsupials in general appears to be an opportunistic response to unpredictable biotic and abiotic conditions.Abbreviations VO₂ metabolic rate - Tb body temperature - Ta ambient temperature - BMR basal metabolic rate - C thermal conductance - T_m temperature differentialCommunicated by I.D. Hume     

Host spatial structure and disperser activity determine mistletoe infection patterns

What processes and factors are responsible for species distribution are long-standing questions in ecology and a key element for conservation and management. Mistletoes provide the opportunity to study a forest species whose occurrence is expected to be constrained by multiple factors as a consequence of their life form. We studied the mistletoe Tristerix corymbosus (Loranthaceae) on its most common hosts species in northwest Patagonia. The seeds of this mistletoe are almost exclusively dispersed by the small arboreal and endemic marsupial Dromiciops gliroides (Microbiotheridae). We assessed the underlying causes of plant spatial patterns through point pattern analysis and we used different variables that characterize the neighborhood around each host to analyze the relative effect of host availability, potential for disperser movement and canopy light conditions. We found that potential hosts were strongly aggregated and that the three most common host species were distributed independent of each other. Considering all host species together, infected and non-infected host were individually aggregated but segregated from each other. The aggregated pattern of infected hosts could be explained in part by the template of potential hosts distribution, but was subsequently modulated by the activity of the mistletoe disperser. Potential for disperser movement, the proximity to reproductive mistletoes and habitat complexity, increased mistletoe infection probability. However, neighboring host availability decreased mistletoe infection probability, and tree DBH (used as surrogate for light conditions) had no detectable effect. Our results suggested that the distribution of mistletoe infection was determined by the structure of potential host populations and by the marsupial disperser activity. Compared to bird dispersed mistletoes, the scale of the infection was smaller and the proximity to reproductive mistletoes and habitat complexity were important for seed arrival and infection. The interplay between landscape structure and disperser activity determine the spatial structure of mistletoe future generations.     

Consequences of disperser behaviour for seedling establishment of a mistletoe species

The dispersal process in plants links adults and their offspring. For frugivore‐dispersed plants, animal behaviour can have a strong effect on plant fitness. Many mistletoes are totally dependent on animals that deposit seeds on suitable hosts and particular branch diameters. We characterised the seed dispersal and seedling establishment of the mistletoe Tristerix corymbosus, which at our study site, is exclusively dispersed by the marsupial Dromiciops gliroides. Mistletoes’ fruits have a viscous pulp that remains in the seed even after dispersal. This substance adheres the seed to the host branch. We estimated host branch availability in the forest and seed deposition (faeces) by the marsupial in the study area. Specifically, the branch suitability factors we assessed were host identity, branch status (alive or dead), branch diameter, height, and canopy cover. Lodged faeces were individually marked and the number of seed deposited within these droppings was counted, and we recorded the number of seedlings with true leaves that had established after 1 year to estimate the probability of seedling establishment. Branch diameter and canopy cover had a significant positive effect on seed deposition probability. Seedling establishment probability decreased with the number of seeds deposited per faeces and with canopy cover. In general, the marsupial deposited mistletoe seeds in microsites that increase the chance of seedling establishment. Thus, the movement behaviour of the marsupial has a positive effect on the regeneration process of this mistletoe species.     

The ecology and evolution of the monito del monte,a relict species from the southern South America temperate forests

The arboreal marsupial monito del monte (genus Dromiciops, with two recognized species) is a paradigmatic mammal. It is the sole living representative of the order Microbiotheria, the ancestor lineage of Australian marsupials. Also, this marsupial is the unique frugivorous mammal in the temperate rainforest, being the main seed disperser of several endemic plants of this ecosystem, thus acting as keystone species. Dromiciops is also one of the few hibernating mammals in South America, spending half of the year in a physiological dormancy where metabolism is reduced to 10% of normal levels. This capacity to reduce energy expenditure in winter contrasts with the enormous energy turnover rate they experience in spring and summer. The unique life history strategies of this living Microbiotheria, characterized by an alternation of life in the slow and fast lanes, putatively represent ancestral traits that permitted these cold‐adapted mammals to survive in this environment. Here, we describe the ecological role of this emblematic marsupial, summarizing the ecophysiology of hibernation and sociality, updated phylogeographic relationships, reproductive cycle, trophic relationships, mutualisms, conservation, and threats. This marsupial shows high densities, despite presenting slow reproductive rates, a paradox explained by the unique characteristics of its three‐dimensional habitat. We finally suggest immediate actions to protect these species that may be threatened in the near future due to habitat destruction and climate change.     

<Emphasis Type="Italic">Allassogonoporus dromiciops</Emphasis> n. sp. (Digenea: Allassogonoporidae) from <Emphasis Type="Italic">Dromiciops gliroides</Emphasis> (Marsupialia: Microbiotheriidae) in Patagonia,Argentina

A new species of Allassogonoporus Olivier, 1938, from a naturally infected specimen of Dromiciops gliroides, is described. Adults of A. dromiciops n. sp. were recovered from the small intestine. This new species can be distinguished from all other species of the genus by having: the largest body and eggs, a lobed testes and ovary, a Y-shaped excretory vesicle and vitelline follicles beginning at the level of the posterior margin of the oral sucker. This is the first record of a species of Allassogonoporus in South America and the first record of a digenean parasitising D. gliroides.     

Spatial ecology of monito del monte (Dromiciops gliroides) in a fragmented landscape of southern Chile

Habitat loss is one of the most important causes of biodiversity loss in South American temperate rainforests, where many endemic species exist. Among these is the monito del monte (Dromiciops gliroides), an arboreal marsupial with restricted distribution, and the only extant species of the order Microbiotheria. Current knowledge about monito del monte habitat use and its responses to human disturbances is scarce. To help fill this gap we investigated its habitat use and selection patterns in a fragmented landscape in southern Chile. Monito del monte individuals were abundant in a large and a small fragment, but rare or undetected in forest strips. Using telemetry data from 12 neighboring individuals in a large fragment and 2 individuals in a small fragment, we estimated their mean home range size of 1.6 ha±0.6 (1SD). Monitos del monte had a spatial overlap among individuals of 50±4%. Tracked individuals used old- and second-growth habitats as available, did not use the prairie habitats, and strongly avoided the scrublands. In the large fragment we estimated a relative population density of 21±5 individuals/ha (mean±1SD), whereas in the small fragment it was of 19±6 individuals/ha. This is, to our knowledge, the first study of the spatial ecology of the monito del monte based on telemetry data, and evidence presented here could have conservation and planning implications, not only for the target species but also its habitat.     

Elevation has contrasting effects on avian and mammalian nest traits in the Andean temperate mountains

Nest building is a widespread breeding strategy across taxa. Nest composition and structure can play a critical role in the breeding success and/or adult survival of nest‐building vertebrates. Although nest traits are expected to vary adaptively across elevational gradients, few studies address this relationship. We studied the variation in nest traits (composition and structure) across elevation for two taxa with two different functions in the Andean temperate forests of southern Chile: a bird (Aphrastura spinicauda, Furnariidae, 170 breeding nests) and a marsupial mammal (Dromiciops gliroides, Microbiotheriidae, 91 winter torpor nests). For A. spinicauda, we further assessed how nest traits influenced clutch size and hatching success. Both species used fewer types of nest materials (items) with increasing elevation, and a greater proportion of leaves were used in highland compared to lowland forests. Aphrastura spinicauda used feathers and hair, and D. gliroides used bryophytes more frequently in lowland forests. The mass and volume of nests decreased with increasing elevation for A. spinicauda and increased for D. gliroides. Nest traits had subsequent fitness consequences for A. spinicauda, such that: (i) greater cup volume and depth were associated with larger clutch sizes, (ii) more items used during nest building were linked to improved clutch size at high elevation only, and (iii) nest wall thickness was negatively associated with hatching success. Thus, in temperate mountain ecosystems, elevation may be an important factor influencing nest‐building behaviour for cavity‐using vertebrates. However, the direction of the elevational effects may vary among taxa and nest functions in these ecosystems.     

Historical biogeography and post-glacial recolonization of South American temperate rain forest by the relictual marsupial Dromiciops gliroides

Aim Long‐term climatic variation has generated historical expansions and contractions of species ranges, with accompanying fragmentation and population bottlenecks, which are evidenced by spatial variation in genetic structure of populations. We examine here hypotheses concerning dispersal and vicariance in response to historical geoclimatic change and potential isolation produced by mountains and water barriers. Location The temperate rain forest of southern South America, which is distributed from coastal Chile, including the large continental island of Chiloé, across the Andes into Argentina. Methods We investigated our hypotheses in the phylogenetically and biogeographically relictual marsupial Dromiciops gliroides. We examined 56 specimens, which resulted from field samples and museum study skins from 21 localities. We evaluated the influence of two major barriers, the Andean cordillera and the waterway between the mainland and the large island of Chiloé, by performing Bayesian and maximum‐likelihood phylogenetic analyses on sequences of 877 base pairs of mitochondrial DNA. We further tested the contribution of the proposed geographical barriers using analysis of molecular variance (amova ). We also evaluated the responses of populations to historical north–south shifts of habitat associated with glacial history and sea‐level change. Results Our analyses revealed a phylogeny with three clades, two of which are widespread and contain nearly all the haplotypes: a northern clade (36–39° S) and a southern clade (40–43° S). These two clades contain forms from both sides of the Andes. Within the southern clade, island and mainland forms were not significantly differentiated. Tests of recent demographic change revealed that southern populations have experienced recent expansion, whereas northern populations exhibit long‐term stability. The direction of recent gene flow and range expansion is predominantly from Chile to Argentina, with a modest reciprocal exchange across the Andes. Recent gene flow from the island of Chiloé to the mainland is also supported. Main conclusions The genetic structure of contemporary D. gliroides populations suggests recent gene flow across the Andes and between the mainland and the island of Chiloé. Differences in demographic history that we detected between northern and southern populations have resulted from historical southward shifts of habitat associated with glacial recession in South America. Our results add to a growing literature that demonstrates the value of genetic data to illuminate how environmental history shapes species range and population structure.     

Geographic patterns in fruit colour diversity: do leaves constrain the colour of fleshy fruits?

We tested for geographic patterns in fruit colour diversity. Fruit colours are thought to promote detection by seed dispersers. Because seed dispersers differ in their spectral sensitivities, we predicted that fruit colour diversity would be higher in regions with higher seed disperser diversity (i.e. the tropics). We collected reflectance data on 232 fruiting plant species and their natural backgrounds in seven localities in Europe, North and South America, and analysed fruit colour diversity according to the visual system of birds—the primary consumer types of these fruits. We found no evidence that fruit colours are either more conspicuous or more diverse in tropical areas characterised by higher seed disperser diversity. Instead, fruit colour diversity was lowest in central Brazil, suggesting that fruit colours may be more diverse in temperate regions. Although we found little evidence for geographic variation in fruit hues, the spectral properties of fruits were positively associated with the spectral properties of backgrounds. This result implies that fruit colours may be influenced by selection on the reflectance properties of leaves, thus constraining the evolution of fruit colour. Overall, the results suggest that fruit colours in the tropics are neither more diverse nor more conspicuous than temperate fruits, and that fruit colours may be influenced by correlated selection on leaf reflectance properties. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Cranial morphological variation of Dromiciops gliroides (Microbiotheria) along its geographical distribution in south-central Chile: A three-dimensional analysis

We analyzed the variation in cranial morphology of the marsupial Dromiciops gliroides along its distribution in south-central Chile. We evaluated whether the cranial morphological variation is congruent with the phylogeographic structure previously observed in this species. We built three-dimensional models of 69 crania on which we digitized 30 landmarks. We used standard geometric morphometric methods to extract and analyze the shape and size components of the crania. Our data showed a subtle but consistent cranial size and shape variation along the studied distributional range, suggesting a geographic variation pattern rather than a phylogeographic structuring. Indeed, our multivariate analyses recovered a subtle morphological differentiation between island and mainland populations, contrary to what is suggested by a former phylogeographic study. We detected that either the cranial size variation, as well as the insularity and the latitude could be important factors underlying the cranial shape changes. We suggest that an interplay of historical and contemporary processes could be shaping the morphological pattern observed in this marsupial.     

A methodological approach to assess the small mammal community diversity in the temperate rainforest of Patagonia

Assessing small mammal diversity is a common procedure, which usually employs widespread standard techniques, for gathering information for a wide range of studies. Traditional methods, however, may be biased against capturing arboreal marsupials, such as Dromiciops gliroides, an endemic marsupial currently considered a rare species in the Patagonian temperate rainforest due to the low abundances reported previously. I tested a new capturing methodology to assess the small mammal diversity of an old-growth forest in Patagonia, based on a randomized and balanced design, which incorporated a combination of different trap types, bait types, and placement heights. The proposed methodology included four trap types (two for live-capturing: wire-mesh and Sherman traps, and two sign-recording traps for tracks and hair), two types of bait (banana and rolled oats), and two trap placements (ground level and 1.5–2.5 m above the ground). Trap type, bait type, and height of placement all had significantly different effects on capturing and detecting rodents or marsupials; environmental variables at the trap location also affected the ability to detect rodents and marsupials. Traditional methods used for sampling small mammals performed well for rodents but are not effective for capturing marsupials and vice versa, showing species-specific sampling protocols. There is no single combination of trap-bait-height capable to assess the entire small mammal community, but the combination of the most effective protocol for rodents and the most effective protocol for marsupials guarantee better results.     

Gibbons (Nomascus gabriellae) provide key seed dispersal for the Pacific walnut (Dracontomelon dao), in Asia's lowland tropical forest

Understanding the mutualisms between frugivores and plants is essential for developing successful forest management and conservation strategies, especially in tropical rainforests where the majority of plants are dispersed by animals. Gibbons are among the most effective seed dispersers in South East Asia's tropical forests, but are also one of the highly threatened arboreal mammals in the region. Here we studied the seed dispersal of the Pacific walnut (Dracontomelon dao), a canopy tree which produces fruit that are common in the diet of the endangered southern yellow-cheeked crested gibbon (Nomascus gabriellae). We found that gibbons were the most effective disperser for this species; they consumed approximately 45% of the fruit crop, which was four times more than that consumed by macaques – the only other legitimate disperser. Gibbons tracked the temporal (but not spatial) abundance of ripe fruits, indicating this fruit was a preferred species for the gibbon. Both gibbons and macaques dispersed the majority (>90%) of the seeds at least 20 m away from parent crowns, with mean dispersal distances by gibbons measuring 179.3 ± 98.0 m (range: 4–425 m). Seeds defecated by gibbons germinated quicker and at greater rates than seeds spat by macaques, or in undispersed fruits. Gibbon-dispersed seeds were also more likely to be removed by unknown seed predators or unknown secondary dispersers. Overall, gibbons play a key role in the regeneration of the Pacific walnut. Our findings have significant implications both for the management of the Pacific walnut tree dominating tropical rainforest as well as the reintroduction program of the Southern yellow-cheeked crested gibbon.     

Phenology of fleshy fruits in a wet sclerophyll forest in southeastern Australia: are birds an important influence?

Summary The hypothesis that seasonality in the production of fleshy fruits in temperate regions is the result of selection by avian seed dispersal agents or avian seed predators was tested in a temperate wet sclerophyll forest in south-eastern Australia. I determined whether ten common fleshy-fruited species produced fruits when potential avian seed dispersers were most abundant or avian seed predators were least abundant. The season of fruit production was not correlated with avian disperser abundance nor with seasonal changes in avian seed predators. Peak fruiting occurred during autumn but fruit-eating birds were equally abundant from spring through to autumn. Avian seed predators (parrots) did not show any seasonal variation in abundance. If dispersers are influencing fruiting seasonality in wet sclerophyll forest, it is likely that changes in social behaviour and feeding patterns of dispersers during autumn, rather than increases in abundance, will be an important influence on fruiting patterns in wet sclerophyll forest. However, environmental and life history factors may also influence phenology.     

Seed dispersal by carnivores in temperate and tropical dry forests

The seed dispersal mechanisms and regeneration of various forest ecosystems can benefit from the actions of carnivores via endozoochory. This study was aimed to evaluate the role of carnivores in endozoochory and diploendozoochory, as well as their effect on seed viability, scarification, and germination in two forest ecosystems: temperate and tropical dry forest. We collected carnivore scat in the Protected Natural Area of Sierra Fría in Aguascalientes, Mexico, for 2 years to determine the abundance and richness of seeds dispersed by each carnivore species, through scat analysis. We assessed seed viability through optical densitometry using X‐rays, analyzed seed scarification by measuring seed coat thickness using a scanning electron microscope, and evaluated seed germination in an experiment as the percentage of seeds germinated per carnivore disperser, plant species, and forest type. In the temperate forest, four plant species (but mainly Arctostaphylos pungens) were dispersed by four mammal species. The gray fox dispersed the highest average number of seeds per scat (66.8 seeds). Bobcat dispersed seeds through diploendozoochory, which was inferred from rabbit (Sylvilagus floridanus) hair detected in their scats. The tropical dry forest presented higher abundance of seeds and richness of dispersed plant species (four species) than in the temperate forest, and the coati dispersed the highest number of seeds (8,639 seeds). Endozoochory and diploendozoochory did not affect viability in thick‐testa seeds (1,480 µm) in temperate forest and thin‐testa seeds (281 µm) in tropical dry forest. Endozoochory improved the selective germination of seeds. Nine plant species were dispersed by endozoochory, but only one species (Juniperus sp.) by diploendozoochory. These results suggest that carnivores can perform an important ecological function by dispersing a great abundance of seeds, scarifying these seeds causing the formation of holes and cracks in the testas without affecting viability, and promoting the selective germination of seeds.     

Avian frugivory and seed dispersal of a large fruited tree in an Indian moist deciduous forest

Seed dispersal systems in degraded areas can be compromised following the decline of large-bodied frugivore populations responsible for their dispersal. In this context we examined the seed dispersal ecology of a large fruited deciduous tree (Dillenia pentagyna) along a forest degradation gradient in India. We examined the effect of structural components of vegetation and frugivore foraging behavior on D. pentagyna seed dispersal. Depauperate mammalian community and declined large avian frugivores e.g. hornbills in our study site make this system a specialized one and currently dependent on only two large bodied avian frugivores. Seed dispersal followed an overall leptokurtic pattern and the seed dispersal kernels were best explained by an inverse power function. Seed dispersal kernels in dense forest indicated longer dispersal distances than moderately dense forest and degraded forest. In degraded areas, no dispersal away from the crown was recorded for D. pentagyna and it occurred at low density. Canopy foliage abundance of the surrounding vegetation of the focal trees was best explained by quantity of seed dispersal by large avian frugivores. The number of avian frugivore species those are effective disperser of D. pentagyna decreased along the degradation gradient. Avian frugivore behavior in terms of visitation and seed swallowed is a determining factor that controls quantity of seed dispersal. Our study underscores deleterious impact of forest degradation on avian disperser community which in turn would affect regeneration capacity of degraded forest.     

Different nest predator guild associated with egg size in the Patagonian temperate forest

Capsule: Studies of nest predation using artificial nests need to consider the effect of egg size on the types of predator that are detected.

Aims: To estimate the nest predation rate in the Patagonian temperate forest and evaluate the influence of egg size on predator guild.

Methods: On different plant species, we placed 108 nests each containing eggs of either Atlantic Canary Serinus canaria or Common Quail Coturnix coturnix, and a model clay egg of equal size to the real egg. Nest predators were identified from the marks left on the clay eggs or by videos recorded using camera traps.

Results: 86% of the nests were predated. Birds, mainly Chimango Caracara Milvago chimango, were the main nest predators. A marsupial, the Monito del Monte Dromiciops gliroides, and rodents also contributed to nest predation. Nest predation rates were similar for both egg sizes but the nest predator guild was different. Birds and rodents preyed on both eggs but the Monito del Monte consumed mainly small eggs.

Conclusion: Egg size did not influence the rate of nest predation but, instead, affected the nest predator guild. Consequently, in order to avoid underestimating the impacts of small predators, egg size should be considered in studies of nest predation.     

Radiation of extant marsupials after the K/T boundary: evidence from complete mitochondrial genomes

The complete mitochondrial (mt) genomes of five marsupial species have been sequenced. The species represent all three South American orders (Didelphimorphia, Paucituberculata, and Microbiotheria). Phylogenetic analysis of this data set indicates that Didelphimorphia is a basal marsupial lineage followed by Paucituberculata. The South American microbiotherid Dromiciops gliroides (monito del monte) groups with Australian marsupials, suggesting a marsupial colonization of Australia on two occasions or, alternatively, a migration of an Australian marsupial lineage to South America. Molecular estimates suggest that the deepest marsupial divergences took place 64-62 million years before present (MYBP), implying that the radiation of recent marsupials took place after the K/T (Cretaceous/Tertiary) boundary. The South American marsupial lineages are all characterized by a putatively non-functional tRNA for lysine, a potential RNA editing of the tRNA for asparagine, and a rearrangement of tRNA genes at the origin of light strand replication.     

Spatial Scales of Pollen and Seed-Mediated Gene Flow in Tropical Rain Forest Trees

Gene flow via seed and pollen is a primary determinant of genetic and species diversity in plant communities at different spatial scales. This paper reviews studies of gene flow and population genetic structure in tropical rain forest trees and places them in ecological and biogeographic context. Although much pollination is among nearest neighbors, an increasing number of genetic studies report pollination ranging from 0.5–14 km for canopy tree species, resulting in extensive breeding areas in disturbed and undisturbed rain forest. Direct genetic measures of seed dispersal are still rare; however, studies of fine scale spatial genetic structure (SGS) indicate that the bulk of effective seed dispersal occurs at local scales, and we found no difference in SGS (Sp statistic) between temperate (N?=?24 species) and tropical forest trees (N?=?15). Our analysis did find significantly higher genetic differentiation in tropical trees (F _ST?=?0.177; N?=?42) than in temperate forest trees (F _ST?=?0.116; N?=?82). This may be due to the fact that tropical trees experience low but significant rates of self-fertilization and bi-parental inbreeding, whereas half of the temperate tree species in our survey are wind pollinated and are more strictly allogamous. Genetic drift may also be more pronounced in tropical trees due to the low population densities of most species.