2024-04-20 2024, Volume 19 Issue 4

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  • ORIGINAL ARTICLE
    Maya L. MAURER , José F. GOYCO-BLAS , Kevin D. KOHL

    Research has shown that leached plant toxins negatively impact the growth and development of larval amphibians. However, tadpoles may encounter these same toxins in food material, and differential exposure routes and distribution of toxic chemicals can yield variable downstream effects on animals. To date, most research understanding the interactions between dietary plant toxins and herbivores has been conducted in terrestrial systems. Despite the abundance of plant toxins in food and water sources, the effects of dietary plant toxins on larval amphibians have not been studied, and tannins could negatively affect these species. Here, green frog tadpoles (Lithobates clamitans) were fed diets with or without 2% tannic acid to test how their growth, development, behavior, and gut microbiome respond to dietary tannins. At the end of the trial, we conducted a behavioral assay to measure tadpole activity and boldness and inventoried the gut microbiome using 16S rRNA sequencing. Dietary tannins significantly decreased body mass by 66% and length by 28%, without influencing tadpole developmental stage. We found significant differences in exploratory behavior and boldness during the first minute of our behavioral assay, demonstrating that tannins have the potential to influence behavior during novel or stressful events. Finally, tannins significantly sculpted the gut microbiome, with an increase in the measurement of Shannon entropy. We observed 7 microbial phyla and 153 microbial genera that exhibited significantly differential abundances differences between control and tannic acid-fed tadpoles. Collectively, our results demonstrate that dietary tannins have the potential to alter amphibian growth, behavior, and microbiome.

  • ORIGINAL ARTICLE
    Xinyu BO , Jialing CHEN , Jinzhan MU , Xianggui DONG , Zhanjun REN , Jinyao LIU , Shuhui WANG

    Musk is a scarce and precious medical resource secreted by male forest musk deer (FMD). Current research to promote musk secretion in FMD has used almost exclusively hormone injections, but this approach can be detrimental to the health of FMD. In order to conserve this endangered species as much as possible while increasing the production of musk, this study first used bioinformatics methods to predict the function of quercetin, a flavonoid that promotes testosterone (T) production and prevents late-onset male hypogonadism. On the basis of good prediction effect, different concentrations of quercetin were added to the diet of FMD. The results showed that quercetin could change the levels of T, luteinizing hormone releasing hormone, luteinizing hormone, and estradiol, and regulate the structure of intestinal microorganisms and musk microorganisms of FMD. Moreover, there is a correlation among musk components, hormones, intestinal microorganisms, and musk microorganisms, which indicates that the production of musk may be regulated by these three at the same time, and the addition of quercetin with 800 mg per kg diet could significantly increase the yield of muscone (P < 0.05), the most effective ingredient in musk. In addition, quercetin decreased the high level of cortisol during musk secretion, which may relieve the stress on FMD in this process. This may help to protect the health of FMD. Combined with the results of software prediction, we finally proposed a possible mechanism for the complex process of musk secretion in FMD with a view to providing ideas for further studies.

  • ORIGINAL ARTICLE
    Hanwen CAO , Yongpeng SHI , Ji WANG , Zhanyu NIU , Li WEI , Huabing TIAN , Feifei YU , Lan GAO

    The intestinal microbiota help regulate hibernation in vertebrates. However, it needs to be established how hibernation modulates the gut microbiome and intestinal metabolism. In the present study, we used an artificial hibernation model to examine the responses of the gut microbiota of the Strauchbufo raddei to the environmental changes associated with this behavior. Hibernation significantly lowered the diversity of the microbiota and altered the microbial community of the gut. Proteobacteria, Firmicutes, and Bacteroidota were the major bacterial phyla in the intestines of S. raddei. However, Firmicutes and Proteobacteria predominated in the gut of active and hibernating S. raddei, respectively. Certain bacterial genera such as Pseudomonas,Vibrio,Ralstonia, and Rhodococcus could serve as biomarkers distinguishing hibernating and non-hibernating S. raddei. The gut microbiota was more resistant to environmental stress in hibernating than active S. raddei. Moreover, metabolomics revealed that metabolites implicated in fatty acid biosynthesis were highly upregulated in the intestines of hibernating S. raddei. The metabolites that were enriched during hibernation enabled S. raddei to adapt to the low temperatures and the lack of exogenous food that are characteristic of hibernation. A correlation analysis of the intestinal microbiota and their metabolites revealed that the gut microbiota might participate in the metabolic regulation of hibernating S. raddei. The present study clarified the modifications that occur in the intestinal bacteria and their symbiotic relationship with their host during hibernation. These findings are indicative of the adaptive changes in the metabolism of amphibians under different environmental conditions.

  • ORIGINAL ARTICLE
    Jun-Kyu PARK , Yuno DO

    The hibernation of amphibians can offer a unique window into overwintering adaptation processes and host–gut microbiota interactions through changes in metabolic availability and homeostasis. We attempted to identify differences in the physiology and gut microbiome during and after hibernation in Japanese wrinkled frogs (Glandirana rugosa), an aquatic overwintering amphibian. After hibernation, the high alpha and beta diversity of the gut bacterial community appears to reflect the more diverse and complex environmental conditions. During winter, Proteobacteria dominated the majority of the gut bacterial community, likely due to high oxygen saturation. After hibernation, Firmicutes and Bacteroidetes increased, which are supportive of host metabolism by gut microbiota. Corticosterone also showed high values and variances after hibernation, presumably allowing the population to remain adaptable across a broad range of environmental gradients. Innate immunity was high after hibernation but exhibited low variation among populations, which supports the idea of a prioritized investment in immunity after hibernation. Blood biochemistry suggests that aquatic overwintering frogs have a mechanism to adapt through overhydration and regulate homeostasis through water excretion associated with the kidney and urine after hibernation. Frog populations exhibit variations and adaptability in gut microbiota and physiology during and after hibernation: Through this, they may demonstrate an adaptive response that regulates metabolic availability in preparation for unpredictable environmental changes. We also propose that the maintenance of Proteobacteria during hibernation can support the colonization of Firmicutes and Bacteroidetes after hibernation, underscoring the need to study the complex effects of gut microbiota across multiple life stages.

  • ORIGINAL ARTICLE
    Jidong ZHAO , Tuo FENG , Xiaolei AN , Xiaoning CHEN , Ning HAN , Jing WANG , Gang CHANG , Xiang HOU

    With the overuse of antibiotics in health care and animal husbandry, antibiotic resistance becomes a serious threat to public health. Antibiotic residues from veterinary medicine have increased the dissemination of antibiotic resistance genes (ARGs) by horizontal gene transfer globally, leading to the enrichment of ARGs in wildlife. Plateau pika (Ochotona curzoniae) is a small herbivore endemic to the Qinghai–Tibetan Plateau. Previous studies reveal that pika evolves a coprophagy behavior toward cohabitated yak, which makes the pika population a potential reservoir of ARGs. Yet, little is known about the resistome of pika under different grazing intensities. Here, we sampled the cecum content of pika from three different grazing intensity areas in the Qinghai–Tibetan Plateau to evaluate the effect of grazing on its gut microbiota and resistome. By using the 16S full-length amplicon and metagenomic sequencing, our study revealed that livestock grazing significantly altered the gut microbial community of plateau pika as compared to prohibited grazing areas. We found bacterial lineage Prevotellaceae, Lachnospirales, and RF39 increased in grazing areas. Analysis of the resistome revealed that pika from continuous grazing areas enriched a higher abundance of colistin (MCR) and streptogramin (vat) resistance genes. Moreover, we observed significant correlations between the gut microbial community, ARGs, and mobile genetic element profiles, hinting that pika gut microbiota was an important shaping force of the resistome. In future studies, the continuous monitoring of wildlife gut resistome and environmental antibiotic residues is imperative for a better understanding and for tackling the horizontal gene transfer of ARGs across the wildlife–livestock interface.

  • ORIGINAL ARTICLE
    Yunwei LU , Liang ZHANG , Xu LIU , Yue LAN , Lixia WU , Jiao WANG , Kongju WU , Chaojie YANG , Ruiqing LV , Dejiao YI , Guifu ZHUO , Yan LI , Fujun SHEN , Rong HOU , Bisong YUE , Zhenxin FAN

    The red panda (Ailurus fulgens) is a distinctive mammal known for its reliance on a diet primarily consisting of bamboo. The gut microbiota and overall health of animals are strongly influenced by diets and environments. Therefore, conducting research to explore the taxonomical and functional variances within the gut microbiota of red pandas exposed to various dietary and environmental conditions could shed light on the dynamic complexities of their microbial communities. In this study, normal fecal samples were obtained from red pandas residing in captive and semi-free environments under different dietary regimes and used for metabolomic, 16S rRNA, and metagenomic sequencing analysis, with the pandas classified into four distinct cohorts according to diet and environment. In addition, metagenomic sequencing was conducted on mucus fecal samples to elucidate potential etiological agents of disease. Results revealed an increased risk of gastrointestinal diseases in red pandas consuming bamboo shoots due to the heightened presence of pathogenic bacteria, although an increased presence of microbiota-derived tryptophan metabolites appeared to facilitate intestinal balance. The red pandas fed bamboo leaves also exhibited a decrease in gut microbial diversity, which may be attributed to the antibacterial flavonoids and lower protein levels in leaves. Notably, red pandas residing in semi-free environments demonstrated an enriched gut microbial diversity. Moreover, the occurrence of mucus secretion may be due to an increased presence of species associated with diarrhea and a reduced level of microbiota-derived tryptophan metabolites. In summary, our findings substantiate the influential role of diet and environment in modulating the gut microbiota of red pandas, offering potential implications for improved captive breeding practices.

  • ORIGINAL ARTICLE
    Joanna T. BIALAS , Łukasz DYLEWSKI , Marcin TOBOLKA

    The brain size of vertebrates represents a trade-off between natural selection for enhanced cognitive abilities and the energetic constraints of brain tissue production. Processing information efficiently can confer benefits, but it also entails time costs. Breeding strategies, encompassing timing of breeding onset and nest-site selection, may be related to brain size. In this study, we aim to elucidate the relationship between brain size, breeding timing, nest-site choice, and breeding success in the red-backed shrike Lanius collurio. Our findings revealed that the timing of the first egg-laying date was associated with female head size, with larger-headed females tending to lay eggs later in the breeding season. Additionally, we observed that breeding success was positively correlated with increased nest concealment. However, this relationship was stronger in males with smaller heads. In turn, nest concealment was not related to head size but primarily influenced breeding onset. These results suggest that the choice of breeding strategy may be moderated by brain size, with differences between sexes. Larger-headed females may invest more time in selecting nesting sites, leading to delayed breeding onset, while larger-headed males may compensate for suboptimal nest concealment. Our study sheds light on the intricate interplay between brain size, breeding timing, nest-site preferences, and breeding success in passerine birds, underscoring the potential role of cognitive capacity in shaping individual decision-making processes.

  • ORIGINAL ARTICLE
    Weichao WANG , Jingru GE , Yaohua ZHANG , Jianxu ZHANG

    Pheromones and olfactory communication play vital roles in sex recognition and mate choice in rodents. Asian house rats (Rattus tanezumi) (RT) often startle easily, making behavioral measurements difficult to carry out accurately in the laboratory. Here, the behavioral and olfactory preferences of the female RT between males and females were not observed using a conventional two-choice device; we then explored the neuro-immunohistochemical evidence in the brains of RT females. We found that male urine elicited significantly higher c-fos expression in the accessory olfactory system and sex-related brain regions in females than female urine did. On the other hand, the differences of volatile compounds and major urinary proteins (MUPs) in both voided urine and preputial glands (PGs) of the RT were detected using gas chromatography–mass spectrometer, sodium dodecyl sulfate-polyacrylamide gel electrophoresis, isoelectric focusing electrophoresis, and liquid chromatography–electrospray ionization mass spectrometry. We found that PG-derived 1-(4, 5-dihydro-2-thiazolyl)-ethanone and total MUPs were more abundant in males versus females, suggesting these sexually divergent components might activate the female’s accessory olfactory system. In conclusion, the neuro-immunohistochemical evidence indicated that potential sex pheromones might exist in RT; however, the strength of the chemical signal might be too weak to cause behavioral responses in females.

  • ORIGINAL ARTICLE
    Wenyu ZOU , Pan WU , Xinyi WEI , Daying ZHOU , Yingchun DENG , Yunke JIANG , Bo LUO , Wenqin LIU , Jiaxin HUO , Shichen PENG , Jiang FENG

    Artificial light at night has been considered an emerging threat to global biodiversity. However, the impacts of artificial light on foraging behavior in most wild animals remain largely unclear. Here, we aimed to assess whether artificial light affects foraging behavior in Asian parti-colored bats (Vespertilio sinensis). We manipulated the spectra of light-emitting diode (LED) lighting in a laboratory. Using video and audio recording, we monitored foraging onset, total foraging time, food consumption, freezing behavior (temporary cessation of body movement), and echolocation vocalizations in triads of bats under each lighting condition. Analyses showed that the foraging activities of experimental bats were reduced under LED light. Green, yellow, and red light had greater negative effects on bats’ foraging onset, total foraging time, and food consumption than white and blue light. LED light of different spectra induced increased freezing time and echolocation vocalizations in captive bats, except for the white light. The peak wavelength of light emission correlated positively with freezing time, estimated echolocation pulse rate (the number of echolocation pulses per minute), and foraging onset, but negatively with total foraging time and food consumption. These results demonstrate that artificial light disturbs foraging behavior in Asian parti-colored bats. Our findings have implications for understanding the influencing mechanism of light pollution on bat foraging.

  • LETTER TO THE EDITOR
    Wuxin LI , Changxuan YU , Shijian FU , Shaun S. KILLEN , Lingqing ZENG
  • BOOK REVIEW
    Guy SION
  • ORIGINAL ARTICLE
    Nan WU , Yao WANG , Jie WANG , Yaqian ZHANG , Baoshuang HU , Jinyu GUO , Zhenfei ZHENG , Youbing ZHOU

    Mining can significantly alter landscapes, impacting wildlife and ecosystem functionality. Natural recovery in open-pit mines is vital for habitat restoration and ecosystem re-establishment, although few empirical studies have examined this process. Here, we assessed temporal and spatial responses of small rodents at the community, population, and individual levels during natural mine recovery. We examined the abundance, reproductive potential, and individual health of small rodents at active mines and at former mine sites left to recover naturally for approx. 10 and 20 years. We also assessed the effects of disturbance on rodent recovery processes at three distances from the mine boundary. Rodent numbers peaked after 10–13 years of recovery and exhibited the strongest male bias in the sex ratio. The Chinese white-bellied rat (Niviventer confucianus) was the most abundant species, achieving its highest population abundance at sites abandoned for 10–13 years and thriving at locations closer to the mine boundary. Only Chevrier’s field mouse exhibited morphological responses to the mine recovery category. Ectoparasite load was unaffected by mine or distance-disturbance categories. Both Chevrier’s field mouse (Apodemus chevrieri) and the South China field mouse (Apodemus draco) were affected significantly by vegetation layer cover during recovery succession. Our study highlights the complexities of ecological succession, with a peak in abundance as pioneer communities transition toward a climax seral stage. Careful prior planning and active site management are necessary to optimize abandoned mine recovery. Efforts to accelerate mine recovery through technical restoration should promote conditions that initiate and perpetuate the establishment and succession of wildlife assemblages.

  • ORIGINAL ARTICLE
    Huanhuan GUAN , Shangyun ZHANG , Nan YANG , Yifei HUANGPU , Bin LAN , Karl J. NIKAS , Xinwei WU , Shucun SUN

    Parasitism is known to affect the behavior of host species to enhance parasite dispersal and transmission. However, host behavioral responses to parasitism unrelated to parasite dispersal and transmission have been much less studied. The objective of this study was to determine whether grasshopper hosts infected and uninfected with a parasitic fly (Blaesoxipha sp.) differ in terms of the nutrient content of the diet they consume. We investigated the dietary preferences of two grasshopper species (i.e. Asulconotus chinghaiensis and Chorthippus fallax) in terms of the C/N composition of plant species consumed, and determined whether this affected the egg production of unparasitized and parasitized grasshoppers by flies in a Tibetan alpine meadow. The composition of plants consumed differed significantly between the unparasitized and parasitized grasshoppers. Specifically, the abundance of N-rich legumes was lower and that of high C/N grasses was higher in the diet of the parasitized compared to the unparasitized grasshoppers. Diet N content was higher and C/N was lower in the diet of unparasitized grasshoppers, and parasitized females produced fewer eggs than their unparasitized conspecifics. Future enquiries are needed to understand the specific mechanisms underlying these dietary differences. The effects of parasites on the fitness–associated behavior of hosts should be studied more broadly to better understand parasite evolution and adaptation.

  • ORIGINAL ARTICLE
    Zheng WANG , Wei TAI , Xuan ZHANG , Shouguo LIU , Yixing NIU , Wenwen CHEN , Ning LI

    Species functional traits can influence seed dispersal processes and consequently affect species’ role in the mutualistic network. Although the effect of animal traits on the structure of the seed dispersal network is well explored, it remains poorly understood how plant and fruit traits contribute to the structure. We here studied the effects of plant and fruit traits on the structure of bird seed dispersal networks across different disturbed habitats in the Meihua Mountain National Nature Reserve, Southeastern China. During the study period, 16, 20, 13, and 15 bird species were recorded foraging on 10, 11, 12, and 8 plant species, resulting in 511, 312, 265, and 201 foraging events in the protected forest, natural forest, village, and bamboo forest, respectively. The composition of these seed dispersal networks is not primarily influenced by a specific group of bulbul species, but rather by the presence of an endangered plant species,Taxus chinensis. As we expected, the structure of the four networks was different among the four disturbed habitats. Furthermore, our results also showed tree height and canopy density were the most important plant traits for structuring the seed dispersal network, while sugar, amylase, dry matter, and alkaloids were identified as significant fruit traits. Overall, our findings highlight the value of integrating trait-based ecology into the framework of the seed dispersal network and provide new insights for mutualistic network conservation in disturbed habitats.

  • ORIGINAL ARTICLE
    Xiangping WANG , Xiao FU , Miaomiao SHI , Chunquan XUE , Jiazhi YANG , Zhongtao ZHAO , Shijin LI , Tieyao TU

    Plant–Lepidoptera interactions are often studied using the pollination or herbivore networks only. Lepidoptera species are involved in two types of plant–insect interactions because they are herbivores as larvae and pollinators as adults. The study of entangled networks is critical, since the interaction of different networks can affect the overall network and community stability. Here, we studied the interaction of plants and Lepidoptera on the Yongxing Island, South China Sea. A plant–lepidopteran pollination network and a plant–lepidopteran herbivore network were built by using data from flower–pollinator and leaf–herbivore interactions. We then combined the two networks into a single network. We measured plant composition similarity within each sub-network and across sub-networks for Lepidoptera species. Our findings indicate that the plant–Lepidoptera pollination network and the herbivory network share significant proportions of Lepidoptera but small proportions of plant assemblages. The pollination network had higher nestedness and connectance than the herbivore network. Agrius convolvuli was the most specialized species, while Zizina otis had the highest species strength in the pollination network. Most Lepidoptera species were highly specialized in the herbivore network and their importance positively correlated across the two networks. Furthermore, there was no dietary composition similarity between the two networks for most Lepidoptera species. Our findings highlight the visible structural difference between the pollination and the herbivore networks. Adult Lepidoptera selects different plants for oviposition and feeding, a strategy that may benefit their reproduction and survival by sustaining adequate resources for their two life stages and the diversity of both plants and insects in oceanic island communities.

  • LETTER TO THE EDITOR
    Georgette Paola ANCAJIMA , Maicon ALICRIN DA SILVA , Paulo Eduardo DE OLIVEIRA , Marcelo DUARTE
  • LETTER TO THE EDITOR
    Bin LI , Fengjie LIU , Xin HE , Xiaolong LIU , Min LU
  • CORRECTION