Convergence in tent architecture and tent-making behavior among neotropical and paleotropical bats

Fifteen species of neotropical and three species of paleotropical bats are known either to roost in or to make tents in over 80 species of vascular plants. We summarize the current knowledge of bat-tent architecture, report two new styles of tents (conical and apical) from the Paleotropics, compare the similarity in tents constructed, or used, by neotropical and paleotropical bats, and consider possible functions of tents. Seven styles of tents are known from the Neotropics, three (conical, palmate umbrella, and apical tents) are known from both the Neo- and the Paleotropics, and one (stem tent) is unique to the Paleotropics. In the Neotropics tent-roosting and/or tent-making appears to be a behavior unique to the diverse microchiropteran family Phyllostomidae (subfamily Phyllostomatinae: tribe Stenodermatini), and in the Paleotropics two members of the megachiropteran family Pteropodidae and one member of the microchiropteran family Vespertilionidae are known to construct or roost in tents. Despite the variety of plant taxa used by bats in tent construction, there appears to be a limited number of different leaf forms that can be altered by bats and used as tents. We suggest that the similarity in tent architecture observed among the neotropical and paleotropical bats is a consequence of convergence in leaf morphology among forest understory plants. The congruence in tent-making/roosting behavior observed in members of the Stenodermatini and the Pteropodidae (genusCynopterus) suggests a phylogenetic influence on these behaviors. The similarity in tent-making and/or tent-roosting behavior and life-history traits (small, <70 g, mostly foliage-roosting frugivores) among these divergent neotropical and paleotropical taxa supports a convergence hypothesis in which members of these groups have become ecological equivalents. Although actual tent-making has been observed in only one bat species to date, we suggest that the principal selective force leading to the evolution of tent-making is a polygynous mating system whereby males construct tents to gain access to females. Tents in turn provide resources that offer protection from predators and inclement weather.     

Roosting ecology of Stenodermatinae bats (Phyllostomidae): evolution of foliage roosting and correlated phenotypes

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Molecular evolution of bat color vision genes

The two suborders of bats, Megachiroptera (megabats) and Microchiroptera(microbats), use different sensory modalities for perceivingtheir environment. Megabats are crepuscular and rely on a well-developedeyes and visual pathway, whereas microbats occupy a nocturnalniche and use acoustic orientation or echolocation more thanvision as the major means of perceiving their environment. Inview of the differences associated with their sensory systems,we decided to investigate the function and evolution of colorvision (opsin genes) in these two suborders of bats. The middle/longwavelength (M/L) and short wavelength (S) opsin genes were sequencedfrom two frugivorous species of megabats, Haplonycteris fischeriand Pteropus dasymallus formosus, and one insectivorous speciesof microbat, Myotis velifer. Contrary to the situation in primates,where many nocturnal species have lost the functional S opsingene, both crepuscular and strictly nocturnal species of batsthat we examined have functional M/L and S opsin genes. Surprisingly,the S opsin in these bats may be sensitive to UV light, whichis relatively more abundant at dawn and at dusk. The M/L opsinin these bats appears to be the L type, which is sensitive tored and may be helpful for identifying fruits among leaves orfor other purposes. Most interestingly, H. fischeri has a recentduplication of the M/L opsin gene, representing to date theonly known case of opsin gene duplication in non-primate mammals.Some of these observations are unexpected and may provide insightsinto the effect of nocturnal life on the evolution of opsingenes in mammals and the evolution of the life history traitsof bats in general.     

Colour also matters for nocturnal birds: owlet bill coloration advertises quality and influences parental feeding behaviour in little owls

Chromatic signals of offspring quality have been shown to play a role in parent–offspring communication in diurnal birds, but are assumed to be useless in dim light conditions because colour-based discrimination probably requires more light. A major ecological and evolutionary conundrum in this scenario is why the nestlings of some nocturnal owls display colourful beaks. Here, we test the hypothesis that yellow bill coloration of owlets of the nocturnal little owl Athene noctua may function as a chromatic signal revealing to parents aspects of quality of their offspring. In a first step, we examined physical variation in bill coloration and its covariation with owlet quality. Secondly, we studied parental provisioning in relation to an experimental manipulation of bill coloration of owlets. Bills of owlets showed higher within-nest variation in yellow–red chroma than in brightness. Plasma carotenoid concentration and nestling immunological status were not associated with chromatic or achromatic features of the bill. Interestingly, however, heavier owlets displayed more yellow bills than lighter ones. The effect of bill coloration on parental favouritism changed with brood size. Parents holding large broods preferentially fed owlets with enhanced over reduced yellow bill coloration, whereas those with small broods did not significantly bias feeding in relation to owlet bill coloration. Our results, based on integration of objective spectrophotometric assessment of colour and experimental procedures, confirm that parent little owls use bill coloration to reveal information on owlet body mass to adjust their feeding strategies, thus highlighting the importance of considering potential chromatic signals for a full comprehension of parent–offspring communication processes in nocturnal bird species.     

The dynamics of tent‐roosts in the palm Sabal mauritiiformis and their use by bats in a montane dry forest

Tent‐making bats modify leaves to build refuges. Leaf modification involves energetic and defense costs that should be balanced by the benefits of tent‐roosting. The alteration of the leaf's vascular system reduces the tent's life expectancy, so to obtain a benefit, bats are expected to use tents regularly as long as they remain functional and not modify more leaves than necessary. Over 2 yr, we documented the dynamics of tent construction and use by Uroderma convexum and other bat species in the palm Sabal mauritiiformis in a Colombian transitional dry forest. We also assessed tent condition and compared it to nonmodified leaves of approximately the same age in focal palms. Probability of tent use by U. convexum varied between 57 percent during a reproductive period and 4 percent outside of this period. Bats cut the main vein of folioles, partially affecting water transport in the leaf. However, there were no differences between tents and nonmodified leaves in deterioration scores or deterioration rates over 1 yr. During 2 yr, 48 tents were lost for different causes, but this loss was balanced by the construction of 51 new tents. Thus, bats maintained an excess of usable tents. Palm leaves are long‐lived and seem preadapted to sustain damage and remain viable, particularly in species growing in dry environments. We present several hypotheses to explain the advantage of maintaining a tent surplus.     

Roosting Ecology of the Tent‐Roosting Bat Artibeus watsoni (Chiroptera: Phyllostomidae) in Southwestern Costa Rica1

We described the plants used as roost resources by Artibeus watsoni in southwestern Costa Rica, assessed roost fidelity, and compared roosting ecology between two sites, Golfito and Corcovado, which vary in the degree of human influence. A total of 349 tents from 25 different plant species were used by A. watsoni as roosts; some plant species (e.g., Carludovica palmata, Asplundia alata, Heliconia imbricata and Calathea lutea) were modified into tents with significantly higher frequency than others. The highest tents above the ground were observed in Philodendron popenoei and Rhodospatha wendlandii, whereas tents in Philodendron grandipes and A. alata were significantly lower than any other species. Asplundia alata and R. wendlandii also had the highest frequency of leaves modified per plant. Fidelity of bats to tents was low, although bats used several tents intermittently within a restricted area. Males generally were more faithful to tents than females, although not significantly so. This observation, along with indirect evidence of leaf modification, suggests that males are primarily responsible for tent construction. The two study sites differed in the plants used for roosting and in tent fidelity. Bats in Corcovado used a greater variety of plant species for tent roosting, whereas bats in Golfito were more faithful, suggesting that roosting resources were scarcer at the latter site.     

The Evolution of Group Stability and Roost Lifespan: Perspectives from Tent‐Roosting Bats

Although multiple hypotheses have been proposed to explain group formation, few fully explain the diversity of social interactions found in foliage‐roosting bats. Among these bats, tent‐roosting species are capable of constructing their own shelters. Although many bats utilize tents previously constructed by other species, it has been suggested that a particular subset of tent‐roosting bats specialize on making tents from particular plant species. Tents provide protection from weather and often a place to roost close to foraging sites. Moreover, tent lifespan is plant species specific and may last from a few weeks to more than a year. To better understand effects that roosts have on social bonds of tent‐roosting bats, we conducted a literature review to collect information on social systems and tent lifespan. We tested correlated evolution of group stability and group longevity with tent lifespan using Pagel's method for discrete characters. We found that group stability and group longevity are correlated with tent lifespan. That there is correlated evolution between these characters contributes to our understanding of how different mechanisms interact to produce a variety of social systems in mammals.     

Predation by squirrel monkeys and double-toothed kites on tent-making bats

Central American squirrel monkeys (Saimiri oerstedi) appear to recognize the modified leaves that phyllostomid bats utilize for diurnal roost sites. The monkeys visually and manually search these bat tents for both bats and insects. Adult males are the most successful at capturing bats. Nonvolant juvenile bats are more vulnerable to monkey predation than are adults. Bats that escape monkey predation frequently are captured by doubletoothed kites (Harpagus bidentatus) that tend foraging troops of monkeys. Predation by squirrel monkeys, coupled with that of double-toothed kites, may be a significant source of mortality for tent-making bats.     

Comparative analysis of the male reproductive accessory glands of bat species from the five Brazilian Subfamilies of the family Phyllostomidae (Chiroptera)

This study aimed to morphologically characterize and compare the male reproductive accessory glands (RAGs) of bats belonging to the five Brazilian subfamilies of the family Phyllostomidae (Carollia perspicillata—Carollinae; Desmodus rotundus—Desmodontinae; Glossophaga soricina—Glossophaginae; Phyllostomus discolor—Phyllostominae and Platyrrhinus lineatus—Stenodermatinae). The study demonstrated that the RAGs of phyllostomid bats were comprised of a pair of extra‐abdominal bulbourethral glands and an intra‐abdominal complex, composed of paraurethral glands and a prostate with two (Desmodontinae and Stenodermatinae) or three (Carollinae, Glossophaginae and Phyllostominae) different regions, with the absence of the seminal vesicles; this pattern possibly evolved from a process of compaction of the prostatic regions from an ancestor with three regions. J. Morphol. 276:470–480, 2015. © 2014 Wiley Periodicals, Inc.     

Association of red coloration with senescence of sugar maple leaves in autumn

We evaluated the association of red coloration with senescence in sugar maple (Acer saccharum Marsh.) leaves by assessing differences in leaf retention strength and the progression of the abscission layer through the vascular bundle of green, yellow, and red leaves of 14 mature open-grown trees in October 2002. Computer image analysis confirmed visual categorization of leaves as predominantly green, yellow or red, and chemical quantification of leaf pigment concentrations verified that leaf color reflected underlying differences in leaf biochemistry. Significantly lower chlorophyll concentrations within red and yellow leaves indicated that senescence was more advanced in leaves from these color categories relative to green leaves. Among leaf types, only red leaves contained high concentrations of anthocyanins. There were significant differences in leaf retention capacity among color categories, with the petioles of green leaves being the most firmly attached to twigs, followed by red and then yellow leaves. Microscopic analysis indicated that yellow leaves had the most advanced extension of the abscission layer through the vasculature, with green and red leaves having significantly less abscission layer progression than yellow. A more limited progression of the abscission layer through vascular bundles may be evidence of delayed leaf senescence that could extend resorption of mobile leaf constituents. Together, results from this study suggest an association between leaf anthocyanin content and functional delays in senescence.     

Ultrastructure and distribution of chromatophores in the skin of the leopard gecko (Eublepharis macularius)

The aim of this study was to describe the ultrastructure and arrangement of pigment cells in the leopard gecko (Eublepharis macularius) skin to explain how wild‐type coloration is formed. The study also attempted to explain, on a morphological level, how skin colour changes occur. Samples of leopard gecko skin were collected from wild‐type coloration adult specimens. The morphology of pigmented cells was determined using light microscopy on haematoxylin and eosin (H&E) stained sections and in transmission electron microscopy. These studies indicate that skin of E. macularis contains xanthophores and melanophores but lacks iridophores and that this is probably related to nocturnal activity. The number and distribution of xanthophores and melanophores determines the skin colour and pigmentation pattern. The colour changes depend on the arrangement of characteristic protrusions of melanophores and the degree of filling them with melanosomes.     

Rhodopsin Molecular Evolution in Mammals Inhabiting Low Light Environments

The ecological radiation of mammals to inhabit a variety of light environments is largely attributed to adaptive changes in their visual systems. Visual capabilities are conferred by anatomical features of the eyes as well as the combination and properties of their constituent light sensitive pigments. To test whether evolutionary switches to different niches characterized by dim-light conditions coincided with molecular adaptation of the rod pigment rhodopsin, we sequenced the rhodopsin gene in twenty-two mammals including several bats and subterranean mole-rats. We compared these to thirty-seven published mammal rhodopsin sequences, from species with divergent visual ecologies, including nocturnal, diurnal and aquatic groups. All taxa possessed an intact functional rhodopsin; however, phylogenetic tree reconstruction recovered a gene tree in which rodents were not monophyletic, and also in which echolocating bats formed a monophyletic group. These conflicts with the species tree appear to stem from accelerated evolution in these groups, both of which inhabit low light environments. Selection tests confirmed divergent selection pressures in the clades of subterranean rodents and bats, as well as in marine mammals that live in turbid conditions. We also found evidence of divergent selection pressures among groups of bats with different sensory modalities based on vision and echolocation. Sliding window analyses suggest most changes occur in transmembrane domains, particularly obvious within the pinnipeds; however, we found no obvious pattern between photopic niche and predicted spectral sensitivity based on known critical amino acids. This study indicates that the independent evolution of rhodopsin vision in ecologically specialised groups of mammals has involved molecular evolution at the sequence level, though such changes might not mediate spectral sensitivity directly.     

基于类胡萝卜素着色的鸟类羽色多样性形成机制

人们对动物体色的研究由来已久。作为一类让生物呈现出多变色彩的重要色素, 类胡萝卜素可以在鸟类的羽毛、鸟喙和皮肤等体表组织中沉积, 产生红、橙、黄、粉、紫等颜色。类胡萝卜素不能在鸟类体内合成, 需从食物中摄取, 进而在体内完成吸收、运输、代谢和沉积等一系列过程, 才能用于羽毛着色。与类胡萝卜素着色相关的生理及遗传调控机制一直备受关注, BCO2、SCARB1和CYP2J19等影响类胡萝卜素在鸟类羽毛中着色的关键基因, 推动了对羽色遗传调控机制的深入认识。本文介绍了鸟类可利用类胡萝卜素的主要类型和基本特征, 综述了类胡萝卜素着色相关的生理过程以及调控基因研究的最新进展, 旨在增加对鸟类羽毛中类胡萝卜素着色过程和相关遗传机制的理解。     

Seasonal Shifts in Nocturnal Habitat Use by Coastal Bat Species

Sensitivity of bats to land use change depends on their foraging ecology, which varies among species based on ecomorphological traits. Additionally, because prey availability, vegetative clutter, and temperature change throughout the year, some species may display seasonal shifts in their nocturnal habitat use. In the Coastal Plain of South Carolina, USA, the northern long-eared bat (Myotis septentrionalis), southeastern myotis (Myotis austroriparius), tri-colored bat (Perimyotis subflavus), and northern yellow bat (Lasiurus intermedius) are species of conservation concern that are threatened by habitat loss. Our objective was to identify characteristics of habitat used by these species during their nightly active period and compare use between summer and winter. We conducted acoustic surveys at 125 sites during May–August and at 121 of the same 125 sites December–March 2018 and 2019 in upland forests, bottomland forests, fields, ponds, and salt marsh and used occupancy models to assess habitat use. The northern long-eared bat and southeastern myotis (i.e., myotis bats) used sites that were closer to hardwood stands, pine stands, and fresh water year-round. We did not identify any strong predictors of tri-colored bat habitat use in summer, but during winter they used bottomland forests, fields, and ponds more than salt marsh and upland forests. During summer and winter, northern yellow bats used sites close to fresh water and salt marsh. Additionally, during summer they used fields, ponds, and salt marsh more than upland and bottomland forests, but in winter they used bottomland forests, fields, and ponds more than upland forest and salt marsh. Our results highlight important land cover types for bats in this area (e.g., bottomland forests, ponds, and salt marsh), and that habitat use changes between seasons. Accounting for and understanding how habitat use changes throughout the year will inform managers about how critical habitat features may vary in their importance to bats throughout the year. © 2021 The Wildlife Society.     

Parallel and Convergent Evolution of the Dim-Light Vision Gene RH1 in Bats (Order: Chiroptera)

Rhodopsin, encoded by the gene Rhodopsin (RH1), is extremely sensitive to light, and is responsible for dim-light vision. Bats are nocturnal mammals that inhabit poor light environments. Megabats (Old-World fruit bats) generally have well-developed eyes, while microbats (insectivorous bats) have developed echolocation and in general their eyes were degraded, however, dramatic differences in the eyes, and their reliance on vision, exist in this group. In this study, we examined the rod opsin gene (RH1), and compared its evolution to that of two cone opsin genes (SWS1 and M/LWS). While phylogenetic reconstruction with the cone opsin genes SWS1 and M/LWS generated a species tree in accord with expectations, the RH1 gene tree united Pteropodidae (Old-World fruit bats) and Yangochiroptera, with very high bootstrap values, suggesting the possibility of convergent evolution. The hypothesis of convergent evolution was further supported when nonsynonymous sites or amino acid sequences were used to construct phylogenies. Reconstructed RH1 sequences at internal nodes of the bat species phylogeny showed that: (1) Old-World fruit bats share an amino acid change (S270G) with the tomb bat; (2) Miniopterus share two amino acid changes (V104I, M183L) with Rhinolophoidea; (3) the amino acid replacement I123V occurred independently on four branches, and the replacements L99M, L266V and I286V occurred each on two branches. The multiple parallel amino acid replacements that occurred in the evolution of bat RH1 suggest the possibility of multiple convergences of their ecological specialization (i.e., various photic environments) during adaptation for the nocturnal lifestyle, and suggest that further attention is needed on the study of the ecology and behavior of bats.     

不同叶色三叶海棠叶片成色色素分析

结合民族植物学和药理学的研究方法,对西双版纳地区傣族、哈尼族和基诺族等3个少数民族民间利用番石榴（Psidium guajava）、余甘子（Phyllanthus emblica）和水柳（Homonoia riparia）的传统知识进行调查研究及体外抗菌活性实验。结果表明：番石榴和余甘子在村寨中较为常见,当地少数民族将其种植于庭院中,常作为果蔬食用,食用番石榴嫩叶可缓解拉肚子的症状,治疗腹痛、腹泻。水柳生长在水边,傣族会将其叶作为腌酸鱼的配料之一。根据文献记载,番石榴、余甘子和水柳的叶部位作为药使用时,常煎水外洗,治疗皮肤瘙痒。对这3种药用植物叶部位采用80%乙醇浸泡制备的提取物进行体外抗菌实验,结果显示番石榴、余甘子和水柳3种药用植物对金黄色葡萄球菌和大肠埃希菌均有较好的抑菌和杀菌活性,其最小抑菌浓度MIC在98~390 μg·mL 1之间,最小杀菌浓度MBC在98~781 μg·mL 1之间。番石榴和水柳叶对铜绿假单胞菌有一定抑菌和杀菌活性,其MIC和MBC范围均为6 250~12 500 μg·mL 1。由此可见,这3种药用植物的民间利用具有一定的合理性和药用开发价值。     

Abundance responses of frugivorous bats (Stenodermatinae) to coffee cultivation and selective logging practices in mountainous central Veracruz,Mexico

Shifting and permanent cultivation, selective logging, cattle production and coffee plantations are among the most important factors in montane cloud forest conversion and disturbance. Although shaded-coffee plantations can contribute to the preservation of local species richness, abundance of organisms could be determined by habitat resource availability in agricultural landscapes. We compared abundance of Sturnira and Artibeus bats (Phyllostomidae, Stenodermatinae), in shade coffee plantations and disturbed cloud forest fragments, which represent habitats with different chiropterochorous plant density. We also investigated the relationship between bat species abundance and food plant richness, abundance and diversity. We captured 956 bats, 76% in cloud forest fragments and 24% in shaded coffee plantations. Abundance of Sturnira spp. (small bats) was greater in cloud forest than in coffee plantations, but Artibeus spp. (large bats) abundance was similar in both habitats. Chiropterochorous plant abundance was positively related with bat abundance for Sturnira spp., while chiropterochorous plant richness and diversity were negatively related for Artibeus spp. This suggests that frugivorous bats with different morphological and ecological characteristics respond differentially to anthropogenic activities. For landscape management purposes, the maintenance and augmentation of diverse food resources, for frugivorous bats with different foraging requirements in coffee plantations, will benefit the resilience of bats to modification of their natural habitat.     

Small Tent-Roosting Bats Promote Dispersal of Large-Seeded Plants in a Neotropical Forest

In Neotropical regions, fruit bats are among the most important components of the remaining fauna in disturbed landscapes. These relatively small-bodied bats are well-known dispersal agents for many small-seeded plant species, but are assumed to play a negligible role in the dispersal of large-seeded plants. We investigated the importance of the small tent-roosting bat Artibeus watsoni for dispersal of large seeds in the Sarapiquí Basin, Costa Rica. We registered at least 43 seed species > 8 mm beneath bat roosts, but a species accumulation curve suggests that this number would increase with further sampling. Samples collected beneath bat feeding roosts had, on average, 10 times more seeds and species than samples collected 5 m away from bat feeding roosts. This difference was generally smaller in small, disturbed forest patches. Species-specific abundance of seeds found beneath bat roosts was positively correlated with abundance of seedlings, suggesting that bat dispersal may influence seedling recruitment. Our study demonstrates a greater role of small frugivorous bats as dispersers of large seeds than previously thought, particularly in regions where populations of large-bodied seed dispersers have been reduced or extirpated by hunting.     

Discrete evolutionary color changes in caciques suggest different modes of carotenoid evolution between closely related taxa

Carotenoid‐based colors have signaling roles in a range of animal taxa, yet little is known about how carotenoids vary across species or whether overall patterns may vary across genera. The caciques (Cacicus, Clypicterus and Ocyalus; family Icteridae), a group of passerine birds from Central and South America, appear to visually divide into discrete yellow and red color groups. Reflectance spectrometry supported this observation, showing widely separated short and long‐wavelength groups corresponding with yellow and red‐feathered taxa. Ancestral state reconstructions inferred a yellow ancestral state with two independent changes to red, and no reversals back to yellow. This pattern contrasts with that of another closely related icterid clade, the New World orioles (Icterus), which exhibit a full range of carotenoid colors and have a pattern of evolution that is continuous and extremely labile. To our knowledge, this study is the first to highlight the possibility of different modes of color evolution even among closely related clades. This study also emphasizes the importance of the methods and assumptions of ancestral state reconstruction. In particular, although coloration and other characters can be measured along a continuous scale, they should be reconstructed using discrete methods when data from extant taxa and underlying mechanisms suggest discrete changes.