| The survival of animals is affected by both external and internal factors,and food is an important external ecological factor.Taihangshan macaques(Macaca mulatta.tcheliensis)living in temperate regions face seasonal fluctuations in food availability,as well as increased pressure for food shortages and energy costs due to low temperatures in winter.To estimate the nutritional strategeies of Taihangshan macaques,from March 2013 to July 2017,a systematic study on the nutritional ecology of Taihangshan macaques were conducted at Taihangshan Macaque National Nature Reserve including a long-term behavior observation,collection of food and faeces samples,determination of nutrition and secondary substances.Using the highthroughput 16 S r RNA sequencing technology,integrated food choices,nutrition,reproductive output and parental investment data,the structure and function of the Taihangshan macaques gut microbiota in terms of nutritional ecology was studied systematically.This study aims to reveal the nutritional strategies of Taihangshan macaques under harsh environment,and to interpret the mechanism of the exceptionally wide distribution of the generalist species as per the structure and distribution of nutrition.The main contents and results are as follows:1.Food selection patterns of Taihangshan macaquesIn this study,the food selection patterns of Taihangshan macaques in Taihang mountain area were studied by focus animal sampling,continuous tracking record and field survey.The result shows that 1)Taihangshan macaques subsisted on a relatively small range of foods(57 different foods items from 33 plant species in 8 categories including seeds,fruits,buds,flowers,leaves,herbs,young bark,and twigs).2)However,macaques faced considerable variation in food selection in different seasons.In spring and summer,when seeds were scarce,leaves accounted for 60.3 ± 13.8% of their diet(dry matter [DM]%),and herbs contributed 31.7 ± 22.2%.However,in autumn and winter,when seeds were abundant,they contributed 68.5 ± 22.7% of the diet while herbs accounted for 18.9 ± 12.9% on a DM.Although young bark and twigs were available in all seasons,the macaques only fed on them in winter,and 3)Electivity indexes(Ei)reflects the relationship between food availability and consumption.In autumn,the Ei for seeds was positive(Ei=0.3),compared with the negative value for herbs(Ei=-0.35).In winter,the Ei for seeds was approximately 0.In contrast,both herbaceous plants and fruits had almost maximal Ei(Ei=1).In spring,as that in winter,the Ei for seeds was approximately 0,while fruits had almost maximal Ei.In summer,rhesus monkeys selected more herbaceous plants(EI=0.8)and leaves(EI=0.85).2.Nutritional regulation patterns of Taihangshan macaquesIn this study,Taihangshan macaques with their habitat were selected as the target system,and the data during 4 years,were obtained through behavioral observation,sample survey and other methods.Nutritional geometry framework was used to analyze the nutritional regulation patterns of Taihangshan macaques.The result shows that 1)there were significant seasonal differences in available protein(AP),nonprotein(NP)and total energy intake(TE)(Linear Mixed Models: AP: F=13.113,df=3,P=0.001;NP: F=56.003,df=3,P<0.001;TE: F=132.608,df=3,P<0.001).2)The available protein(One-way ANOVA: spring: F=134.486,df=3,179,P<0.001;winter: F=20.725,df=3,76,P<0.001)and non-protein intake(One-way ANOVA: spring: F=11.638,df=3,179,P<0.001;winter:F=9.250,df=3,76,P<0.001)of Taihangshan macaques in spring and winter showed significant inter-annual changes,while there was no significant interannual difference in the available protein(One-way ANOVA: summer: F=1.305,df=3,72,P=0.279;autumn: F=0.181,df=3,97,P=0.909)and non-protein(One-way ANOVA: summer: F=0.244,df=3,72,P=0.865;autumn: F=0.101,df=3,97,P=0.959)intake in summer and autumn.However,total energy intake of Taihangshan macaques remained constant across the years(One-way ANOVA: spring: F=0.161,df=3,179,P=0.922;summer: F=0.158,df=3,72,P=0.924;autumn: F=0.058,df=3,97,P=0.982;winter: F=2.541,df=3,76,P=0.063),whatever in spring,summer,autumn or winter.3)The lactating group consumed more energy(Linear Mixed Models: F = 231.200,df = 1,110,P<0.001)than the non-lactating group(adult males and non-lactating females).There was no significant difference(Linear Mixed Models: F = 0.276,df = 1,110,P=0.600)in the nutrient ratio(AP/NP)of food intake.4)The 4-year energy intake of macaques in the mammalian group was on average 413 k J/d·BWKg,while the 4-year energy intake in the non-mammalian group was on average 318 k J/d·BWKg.The tannin intake of lactating group was significantly higher than that of non-lactating group(Linear Mixed Models: F = 358.436,df = 1,184,P<0.001).Similarly,the indigestible fiber intake of lactating group was significantly higher than that of non-lactating group(Linear Mixed Models: F = 295.188,df = 1,192,P<0.001).3.Effects of interannual changes in seeds availability on the reproductive output of Taihangshan macaquesData in 3 years,including food availability,diet,nutrient intake,reproductive output,and maternal investment,were recorded using focus animal sampling,continuous recording,and nutritional measurements.The relationship between the energy and nutrient intake of the Taihangshan macaque with seasonal reproduction states was analyzed using the geometric model of nutrition.The result shows that 1)the availability of Quercus(the main source of fats and carbohydrates)varies greatly across the years.The contribution of seeds to total energy,carbohydrates,available protein and fat varies across the years.2)AP and NPE ratios in pregnant and lactating macaques did not change significantly over the years(Mann-Whitney U-test: Z1,18=-0.634,P=0.526,2013;Z1,16=-1.659,P=0.097,2014;Z1,17=-0.089,P=0.929,2015).However,there were significant interannual differences in AP/NPE values between pregnant and lactating macaques(Kruskal-Wallis test: chi-squared= 44.949,df=2,53,P<0.001).3)There was no significant interannual change in total energy intake in pregnant macaques(Kruskal-Wallis test: chi-squared=2.898,df=2,26,P=0.235),however,the total energy intake in lactating female macaques was lower in years with seed deficiency than that in other years(Kruskal-Wallis test: chi-squared= 7.249,df=2,26,P=0.027).In addition,lactating macaques consumed more calories per day than pregnant macaques(P<0.001).4).The reproductive success rate in 2014(48%)was lower than in 2013(95%)and 2015(82%).5)In 2014,females in lactation had greater weight loss(drew on body reserves)(Mann-Whitney U test: Z1,26=-3.49,P<0.001),moved less(Mann-Whitney U test: Z1,26=-2.770,P=0.006),and spent more time nursing their offspring(Mann-Whitney U test: Z1,26=-2.436,P=0.015)than those in 2013 and 2015.4.The composition and function of intestinal microbial community of macaques in response to the dynamics of food resourcesIn this study,the 16 S r RNA of gut microbiota in 12 adult macaques(6 females and 6 males)were sequenced,analyzed using high-throughput sequencing technology.Combined with the diet and nutrition data,the dynamics of gut microbiota and its response to food and nutrient intake in four seasons were analyzed.The results show that: 1)The diets of Taihangshan macaques mainly consisted of leaves,seeds,flowers,buds,young bark and twigs.In summer(2016),they mainly fed on herbs and leaves,accounting for 51.60% and 48.40% respectively.In autumn(2016),it mainly fed on seeds,accounting for 89.16% of food composition,in which Quercus seeds accounted for 64.13%.In winter(2016),they fed on seeds(47.94%)and herbs(25.76%).In spring of 2017,macaques mainly fed on leaves(accounting for 72.27% of the diet).2)The intake of protein and non-protein energy of Taihangshan macaques showed significant seasonal differences(PERMANOVA: F=261.77,df =169,P<0.001).For each season,the nutrient compositions in autumn and winter were very similar.That was greatly different from other seasons in summer,and the nutrient intake in spring was moderate.3)Firmicutes(56.14 ± 6.46%)and Bacteroides(36.57 ± 6.80%)in the gut microbiota of Taihangshan macaques accounted for more than 90%relative abundance.The dominant genera were Prevotella(17.67 ± 8.62%),Treponema(1.73 ± 1.31%),Faecalibacterium(1.45 ± 1.33%),Ruminococcus(1.41 ± 0.99%),Alloprevotella(0.81 ± 1.05%),Succinivibrio(0.61% ± 1.10%),and Roseburia(0.56 ± 0.60%).3)There were significant seasonal differences in Alpha diversity(ANOVA: P = 0.042)and Beta diversity over the seasons(PERMANOVA: F = 8.288,df =47,P < 0.001).4)There was no significant difference in gut microbiota between individuals of Taihangshan macaques,while significant differences between seasons were observed.5)the functional prediction of the metagenomic data identified 329 metabolic pathways at level 3 within 40 metabolic pathways at level 2.Among them,amino acid metabolism pathway,carbohydrate metabolism pathway,energy metabolism,coenzyme factor and vitamin metabolism pathway were highly abundant,ranking 2nd,4th,6th and 10 th respectively.Conclusions1)Variations in food availability affect the food intake of Taihangshan macaque.The diversity of their food intake is low.Nutritional complementarity and nutritional supplementary are the main reasons leading to the seasonal differences in compositions of the diet.2)This study for the first time verifies the "equal distance" nutritional regulation model with constant total energy intake in vertebrates(Taihangshan macaques in this study).This model indicates that Taihangshan macaques is a subspecies with macronutrient generalization.3)Taihangshan macaques maintain the ability to reproduce successfully under different nutritional conditions.It suggests that Taihangshan macaques have evolved a compensatory mechanism that matches the number of births with their ability to rear offspring.4)The main gut microbiota of Taihangshan macaques always have the correlation between protein and non-protein energy intake,which reflects an adaptive response to nutrients intake.The genus level characteristics of gut microbiota and the enrichment of metabolic pathways related to macronutrients and energy indicate that the gut microbes of Taihangshan macaques are highly adaptable to herbivores. |
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