ArticleLiterature Review

Coprophagy in animals: A review

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Abstract

Coprophagy is performed by rodents and lagomorphs and to a lesser degree by piglets, foals, dogs and nonhuman primates. Due to the construction of the digestive system of rodents and rabbits, coprophagy is necessary to supply many essential nutrients. Bacterial synthesis of nutrients occurs in the lower gastrointestinal tract in these animals where little absorption is realized. The eating of their feces provides a method for obtaining these nutrients.

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... Coprophagy is the habit of eating or feeding on one's own (autocoprophagy) or other individual's (or species) excrement (allocoprophagy) (Galef 1979). This phenomenon was first reported in 1882 in rabbits (Morat 1882) which form excreta (that are later ingested later) in the cecum, and the term cecotrophy refers to coprophagy practiced by rabbits and sometimes rodents (Soave and Brand 1991). Coprophagy is a normal phenomenon observed in a variety of invertebrate (Silverman et al. 1991) and vertebrate groups including mammals such as rodents and lagomorphs (Soave and Brand 1991). ...
... This phenomenon was first reported in 1882 in rabbits (Morat 1882) which form excreta (that are later ingested later) in the cecum, and the term cecotrophy refers to coprophagy practiced by rabbits and sometimes rodents (Soave and Brand 1991). Coprophagy is a normal phenomenon observed in a variety of invertebrate (Silverman et al. 1991) and vertebrate groups including mammals such as rodents and lagomorphs (Soave and Brand 1991). In humans, auto-and allocoprophagy, or coprophilia (playing with the feces) are abnormal phenomena and practiced by those deemed mentally impaired and psychiatrically disordered, or even by normal people as a protest behavior (Zeitlin and Polivy 1995;Mason 1996;Giacometti et al. 1997). ...
... As a normal phenomenon, coprophagy has nutritional importance in the provision of vitamins (mainly B-complex), proteins, amino acids, minerals (e.g., iron), and trace elements, which are excreted in the feces having not been effectively absorbed by the lower intestinal tract (Soave and Brand 1991). It aids in acquiring sufficient amounts of these nutrients in the diet of herbivorous animals, i.e., ruminants and monogastric herbivores, as plant food provides much less protein and amino acids than animal tissue (Casimir 1975). ...
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The Central American squirrel monkey, Saimiri oerstedii citrinellus is endemic to Costa Rica and listed by IUCN (2002) as Critically Endangered. The last optimistic estimate of the population of S. o. citrinellus was of 1,500 individuals. According to The second Squirrel Monkey Population and Habitat Viability Assessment Workshop (PHVA) took place in Costa Rica in June 1995 and Boinski and Sirot (1997), the principal recommendation was to verify in situ the localities where S. oerstedii has been recorded, to obtain counts of the number of troops and individuals, along with data on forest size, its characteristics and status. Following these recommendations, we carried out an intensive survey to assess the presence of the subspecies, number of monkeys, troop size and composition in every forest fragment in the central area of the squirrel monkey’s total distribution range. The study area was in the Costa Rican Central and South Pacific lowlands, from 0 to 350 m above sea level, between the western margins of Ríos Parrita and Naranjo. Within our study area, we identified every forest fragment below 350 m above sea level detectable on 1:35.000 and 1:60.000 aerial photographs. During April 1995 our team of 14 biologists divided into four to five subgroups to carry out surveys and interviews which totaled 1220 hoursperson effort, and a 400 hours-team effort. Forest fragments, African oil palm, fruit and silviculture plantations were surveyed. Each forest fragment identified was traversed along a line as close to its center as possible. Whenever we found squirrel monkeys we registered troop size, sex and age composition. We interviewed local farmers and ranch owners near every fragment, totaling 124 interviews. The foothill forests were not considered as a fragment because of their extent, covering 30 km² rising from 400 m and reaching 1000 m above sea level. We surveyed these foothills and conducted interviews below 700 m above sea level. We surveyed 45 fragments that ranged from 10 to 200 ha, with a mean of 60 ha. The total number of squirrel monkeys sighted was 445. Troop sizes ranged from 15 to 80 individuals, with a mean of 32. We recorded 48 infants with an average of three infants per troop, ranging from 9% to 25% of infants per troop. We saw squirrel monkeys in 13 fragments (at six locations the presence of squirrel monkeys had never been reported before) and another 17 fragments (12 unreported locations) were considered to hold troops after interviews. This gives a total of 18 new locations for S. o. citrinellus. Two of these locations were in the foothills where we saw squirrel monkeys. We found troops with 34, 55 and 58 monkeys in 14, 20 and 33 ha forest fragments, connected with other fragments by fruit plantations or creeks. Fifty six percent of the fragments located between the Ríos Parrita and Naranjo were connected by riparian forests, fruit, silvicultural, and African oil palm plantations. During our field work we saw troops traveling along hedgerows, plantations, and electric wires which were rarely insulated, and we also obtained reports of squirrel monkeys crossing highways and pastures between forest strips. We observed troops feeding in natural forests, fruit plantations of guava (Inga sp.), banana (Musa acuminata), and pink apple (Eugenia jambos), and on the outskirts of villages. Surprisingly one of the palm plantations where we saw them (Finca Cerros) had no forest in the immediate vicinity. The squirrel monkey was known by 98% of the interviewees who informed that it is common in the region. Interviews confirm that squirrel monkeys move through African oil palm, fruit and wood plantations. Those carried out in the foothills also confirmed the monkey’s presence in the area. There were no reports of squirrel monkeys above 400 m above sea level. The study area has three zones containing squirrel monkeys: the foothills, the forest fragments and Manual Antonio National Park (MANP). In the foothill forests, we estimated around 750 individuals (based on the lowest density estimate of 25 individuals/km²). In the forest fragments we saw 445 individuals. There are two population estimates for the MANP based on different methodologies: 1) 105 individuals after a brief survey by Boinski et al. (1998) and 2) 581 individuals after a nine-month census (Wong 1990). With this information and not including the 12 new localities where the monkey’s presence was confirmed through interviews, we conservatively estimate that there are at least 1300-1780 squirrel monkeys living in the study area. These numbers surpass those reported for the subspecies within its entire distribution (Boinski et al. 1998). Taking into account that some areas such as Tulín (Arauz 1993), Londres and Ventana de Osa (Arauz 1993, Boinski et al. 1998) where the monkey occurs have not been included in our study and not included in our estimate, we indicate that the total population size reported for S. o. citrinellus is significantly larger than has been previously estimated
... Coprophagy is defined as the consumption of one's own faeces (autocoprophagy) or the faeces of other individuals of the same or other species (allocoprophagy) (Soave & Brand, 1991). Coprophagy has been described for a wide range of species and usually serves as an additional source of nutrients or as a means to acquire intestinal bacterial microflora (Graczyk & Cranfield, 2003;Soave & Brand, 1991). ...
... Coprophagy is defined as the consumption of one's own faeces (autocoprophagy) or the faeces of other individuals of the same or other species (allocoprophagy) (Soave & Brand, 1991). Coprophagy has been described for a wide range of species and usually serves as an additional source of nutrients or as a means to acquire intestinal bacterial microflora (Graczyk & Cranfield, 2003;Soave & Brand, 1991). ...
... In captive and domesticated animals, coprophagy has also been associated with mental stress, anxiety and boredom (Boze, 2010). The consumption of one's own faeces or faeces of conspecifics (intraspecific coprophagy) is common, in particular for rodents and lagomorphs (Soave & Brand, 1991). However, among vertebrates, the consumption of faeces of another species (interspecific coprophagy) is relatively rare (Fish et al., 2007;Reading et al., 2017). ...
Article
Coprophagy is defined as the consumption of one’s own faeces (autocoprophagy) or the faeces of other individuals of the same or other species (allocoprophagy). The consumption of one’s own faeces or the faeces of conspecifics is common, in particular for rodents and lagomorphs. However, the consumption of faeces of individuals of another species has rarely been described for vertebrates. In this study, we describe occurrence of coprophagy of African wild dog faeces by hooded vultures and spotted hyaenas in Mana Pools National Park, Zimbabwe. Between September 2017 and November 2020, we radio-tracked six collared African wild dog packs and recorded interactions with spotted hyaenas and hooded vultures. When spotted hyaenas and/or hooded vultures were present, they engaged in coprophagy of African wild dog faeces in 38.5% and 65.5% of the cases respectively. For both species coprophagy was not related to season, drought, time of day or size of the African wild dog pack. Hooded vultures especially, often engaged in coprophagy when they accompanied African wild dogs while they were resting, suggesting such an association may be intended to have access to faeces. Allocoprophagy in wild vertebrates usually serves as an additional source of energy and/or nutrients. Further research is required to determine the content of African wild dog faeces and the potential nutritional benefits for spotted hyaenas and hooded vultures. However, it is clear from our and other studies that the critically endangered hooded vulture forms close associations with the endangered African wild dog. Such associations may play a role in the hooded vulture's survival and should therefore be considered in the conservation strategy of this species.
... Interestingly, coprophagy is found in many animal species including pigs (Orland and Brand, 1991), rabbits (Combes et al., 2014), termites (Rosenberg and Zilber-Rosenberg, 2011), horses and rats (Galef, 1979;Crowelldavis and Houpt, 1985). For example, piglets reportedly ingest 20 g of their mother's feces daily (Orland and Brand, 1991). ...
... Interestingly, coprophagy is found in many animal species including pigs (Orland and Brand, 1991), rabbits (Combes et al., 2014), termites (Rosenberg and Zilber-Rosenberg, 2011), horses and rats (Galef, 1979;Crowelldavis and Houpt, 1985). For example, piglets reportedly ingest 20 g of their mother's feces daily (Orland and Brand, 1991). Regarding rabbits, the doe defecates in the nest (Kovacs et al., 2006), and the fecal pellets that the kits ingest when they are between 8 and 20 days old change their microbiota at weaning (Combes et al., 2014). ...
Article
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Reducing antibiotic use is a necessary step toward less antibiotic resistance in livestock, but many antibiotic resistance genes can persist for years, even in an antibiotic-free environment. In this study, we investigated the potential of three fecal complex microbial communities from antibiotic-naive does to drive the microbiota of kits from antibiotic-exposed dams and outcompete bacteria-carrying antibiotic-resistant genes. The fecal complex microbial communities were either orally delivered or simply added as fresh fecal pellets in four to five nests that were kept clean from maternal feces. Additionally, four nests were cleaned for the maternal feces and five nests were handled according to the common farm practice (i.e., cleaning once a week) as controls. At weaning, we measured the relative abundance of 26 antibiotic resistance genes, the proportion of Enterobacteriaceae resistant to tetracycline and sulfonamide antibiotics, and the taxonomic composition of the microbiota by sequencing the 16S rRNA genes of one kit per nest. Changing the surrounding microbes of the kits can hinder the transmission of antibiotic resistance genes from one generation to the next, but the three communities widely differed in their ability to orient gut microbes and in their impact on antibiotic resistance genes. The most efficient delivery of the microbial community reduced the proportion of resistant Enterobacteria from 93 to 9%, decreased the relative abundance of eight antibiotic resistance genes, and changed the gut microbes of the kits at weaning. The least efficient did not reduce any ARG or modify the bacterial community. In addition, adding fecal pellets was more efficient than the oral inoculation of the anaerobic suspension derived from these fecal pellets. However, we were unable to predict the outcome of the exclusion from the data of the donor does (species composition and abundance of antibiotic resistance genes). In conclusion, we revealed major differences between microbial communities regarding their ability to exclude antibiotic resistance genes, but more work is needed to understand the components leading to the successful exclusion of antibiotic resistance genes from the gut. As a consequence, studies about the impact of competitive exclusion should use several microbial communities in order to draw general conclusions.
... Moreover, further work is needed to identify in what stages developmental effects on cognition can or cannot be reversed by, for example, newly colonized microbiota through natural transmission from the environment, or by targeted experimental approaches such as faecal transplantation. Indeed many animals engage in coprophagy by eating their own or conspecifics' faeces (reviewed in [61]). This behaviour is typically observed during periods when microbiome enhancement may be most critical, such as during early development (by eating mother or sibling excretions (e.g. ...
... Dietary manipulation has also led to impaired or enhanced cognition in mice models [7,9,21], and in one case has been shown to be independent of nutritional value [7]. Diet varies between and within species along spatial and temporal scales, which can cause shifts in gut microbiota as demonstrated in animals that engage in coprophagy [61], migratory birds during stopovers [84], wild mice across seasons [85] and animals brought into captivity [73], and therefore could impact cognition as a result. Microbiome shifts may also arise in the opposite causal direction when cognition directly affects an individual's dietary preferences or capacity to gain access to food, resulting in feedback loops between cognition and the microbiome via diet (figure 2). ...
Article
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Research into proximate and ultimate mechanisms of individual cognitive variation in animal populations is a rapidly growing field that incorporates physiological, behavioural and evolutionary investigations. Recent studies in humans and laboratory animals have shown that the enteric microbial community plays a central role in brain function and development. The ‘gut–brain axis’ represents a multi-directional signalling system that encompasses neurological, immunological and hormonal pathways. In particular it is tightly linked with the hypothalamic–pituitary–adrenal axis (HPA), a system that regulates stress hormone release and influences brain development and function. Experimental examination of the microbiome through manipulation of diet, infection, stress and exercise, suggests direct effects on cognition, including learning and memory. However, our understanding of these processes in natural populations is extremely limited. Here, we outline how recent advances in predominantly laboratory-based microbiome research can be applied to understanding individual differences in cognition. Experimental manipulation of the microbiome across natal and adult environments will help to unravel the interplay between cognitive variation and the gut microbial community. Focus on individual variation in the gut microbiome and cognition in natural populations will reveal new insight into the environmental and evolutionary constraints that drive individual cognitive variation. This article is part of the theme issue ‘Causes and consequences of individual differences in cognitive abilities’.
... Hence, we used paper strips stained with carminic acid that were not consumed by the control mice ( Figure 5A) because almost all the faeces collected from this group were brown, not pink. When faeces are collected from cages for evaluation, it is important to avoid coprophagia, which is often seen in mice (34). Thus, cages with wire mesh floors were used. ...
... Thus, cages with wire mesh floors were used. Prior to using these specialized cages, we found that less faeces were collected from mice treated with INH and fed a low-niacin diet compared with those that did not receive INH because undernourished mice tend to eat faeces to obtain vitamins (34). Furthermore, while rodents such as mice are typically nocturnal in nature (35)(36)(37), a diurnal pattern of activity is rare in experimental environments, and mice therefore eat and drink freely throughout the day and night (38). ...
Article
Niacin deficiency causes pellagra, the symptoms of which include dermatitis, diarrhoea and dementia. Investigating the mechanism underlying these phenotypes has been challenging due to the lack of an appropriate animal model. Here, we report a mouse model of pellagra-related nausea induced by feeding mice a low-niacin diet and administering isoniazid (INH), which is thought to induce pellagra. Mice fed a normal or low-niacin diet received INH (0.3 or 1.0 mg/mg/animal, twice daily, 5 days), and nausea was evaluated based on pica behaviour, which is considered the rodent equivalent of the emetic reflex. Furthermore, the effect of therapeutic niacin administration on nausea was evaluated in this model. Urinary and hepatic metabolite levels were analysed by liquid chromatography coupled with mass spectrometry. INH-induced pica was observed in mice fed a low-niacin diet but not in those fed a normal diet. Levels of urinary metabolites, such as 1-methyl-2-pyridone-5-carboxamide, kynurenic acid and xanthurenic acid, were significantly reduced in the mice treated with INH compared with those that did not receive INH. Furthermore, niacin supplementation prevented pica and restored the levels of some metabolites in this mouse model. Our findings suggest that INH-related nausea is pellagra-like. We also believe that our newly established method for quantifying pica is a useful tool for investigating the mechanisms of pellagra-related nausea.
... KEY WORDS: coprophagy, gut microbiome development, herbivorous bird, microbiome transmission Coprophagy, which is the consumption of feces, includes the consumption of feces from other species (heterospecific coprophagy), from other individuals of the same species (allocoprophagy), or from one's self (autocoprophagy) [22] and has been observed in a variety of animal groups, including vertebrates [14,23,44]. In herbivorous mammals, such as rodents, autocoprophagy is considered an adaptive behavior for recycling vitamins, minerals, amino acids, trace elements, and other nutrients that are excreted in the feces. ...
... In herbivorous mammals, such as rodents, autocoprophagy is considered an adaptive behavior for recycling vitamins, minerals, amino acids, trace elements, and other nutrients that are excreted in the feces. However, heterospecific coprophagy and allocoprophagy are sometimes considered non-feeding behaviors that inoculate the gut with the bacteria and protozoa of other individuals [11,13], even if these types of coprophagy also have nutritional significance [22,36,44]. Feeding the feces of older individuals to juvenile conspecifics is, in fact, a kind of fecal transplantation that facilitates the coevolution between host species and symbiotic gut bacteria by continuously transmitting the bacteria to subsequent generations. ...
Article
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The transgenerational maintenance of symbiotic microbes that benefit host nutrition and health is evolutionarily advantageous. In some vertebrate lineages, coprophagy is used as a strategy for effectively transmitting microbes across generations. However, this strategy has still not been studied in birds. Accordingly, the aim of the present study was to evaluate the role of maternal cecal feces consumption by Japanese rock ptarmigan (Lagopus muta japonica) chicks as a strategy for acquiring essential gut microbes. Both the duration of coprophagy behavior by the chicks and the development process of the chick cecal microbiome (n=20 one- to three-week-old chicks, from three broods) were investigated. In all three broods, coprophagy behavior was only observed from 3 to 18 days of age. Furthermore, there was no significant difference in the number of bacterial operational taxonomic units (OTUs) in 1-week-old chicks (n=651) and adults (n=609), and most of the main OTUs observed in the adults were already present in the 1-week-old chicks. These results indicate that, in this precocial bird species, coprophagy may contribute to the early establishment of cecal bacteria that are essential for food digestion and, thus, chick survival. In fact, Japanese rock ptarmigan chicks consume the same food as their hens from the time of hatching. This behavior may have applications to ex-situ conservation.
... Once again, this might appear to be an unlikely strategy, but given the perplexing constellation of data we possess on the diet and masticatory adaptations of P. boisei, should we be expecting the unexpected? Others have asked about the possibility that P. boisei practiced coprophagy to maximize assimilation of complex carbohydrates with the added benefit of providing vitamins, minerals, and amino acids (see Soave and Brand, 1991). Coprophagy is practiced by hominoids in the wild, although it is mostly focused on the consumption of seeds ostensibly softened by passage through the digestive tract and never represents more than a small fraction of the diet (Harcourt and Stewart, 1978;Krief et al., 2004;Sakamaki, 2010). ...
Article
Carbon isotopic analysis has been challenging our ideas about hominin diet for nearly 30 years. The first study in 1994 revealed that Paranthropus robustus from South Africa consumed principally C3 foods (e.g., tree fruits and leaves) but also about 25% C4/CAM resources (e.g., tropical grasses and sedges). This result was largely consistent with morphological and dental microwear evidence suggesting P. robustus had a diet which included hard objects like nuts and seeds. Decades later, however, P. boisei from eastern Africa was shown to have eaten nearly 80% C4/CAM plants like the contemporaneous grass-eating primate Theropithecus. Moreover, dental microwear revealed no evidence of hard object consumption in P. boisei, suggesting a diet of tough foods such as grass or sedge leaf and stem. So Paranthropus presents us with two central problems: 1) Why do dietary proxies suggest different diets for the two robust australopiths despite their morphological congruity; and 2) How could P. boisei have consumed tough foods with teeth that seem unsuited to the task. Here we review these questions and more with a particular focus on new isotopic data from the Omo and insights that can be gleaned from mammals outside the haplorrhine primates. We argue that extant Primates do not capture the ecomorphological diversity of P. boisei and other extinct primates and should not narrowly circumscribe the behaviors we ascribe to extinct taxa. We also discuss possible digestive strategies for P. boisei in light of its morphology, dietary proxy data, food mechanical properties, and comparative data on mammalian digestive kinetics.
... bacteria, viruses, parasitic protozoa and helminths) thrive in animal excreta. Other animal species, however, such as pigs, dogs and rabbits exhibit coprophagy to acquire certain digestive enzymes lacking in their diet, obtain nutrients that were unabsorbed by the gastrointestinal tract during the first passage, and/or to develop their microbiome (Soave and Brand, 1991). However, it was only very recently that scientists started testing whether feces or other fecally-contaminated substrates elicit avoidance in non-human primates (Chapters 2, 5, 6; ...
Thesis
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Threats from parasites are ubiquitous. Infectious agents come in myriad forms and often use transmission pathways that exploit host trophic interactions. Because they can have serious fitness impacts on those they infect, host organisms have evolved a behavioral immune system to facilitate contamination-risk assessment and avoidance of sources of infection. Here, I investigated mechanisms and potential consequences of avoidance using food-choice experiments and foraging observations in non-human primates. Parasite avoidance strategies have been studied only rarely and mostly anecdotally in this taxonomic group. Three main questions guided my research: (1) which biological contaminants elicit avoidance in a foraging context? (2) which sensory cues are employed to assess contamination-risk? and, (3) what are the consequences of parasite avoidance? To address these questions, I conducted a series of field experiments, behavioral observations and parasitological investigations on 5 species of Papionini and Hominini: Japanese macaques (Macaca fuscata), long-tailed macaques (Macaca fascicularis), mandrills (Mandrillus sphinx), chimpanzees (Pan troglodytes), and bonobos (Pan paniscus) in Japan, Gabon, and the Democratic Republic of the Congo between January 2014 and July 2016. I first tested whether biological contaminants such as bodily fluids and rotten food, which are known to be universal disgust elicitors in humans, would trigger aversion in these primates in feeding experiments. Food items were presented to subjects uncontaminated (control condition) versus in association with feces (real or replica), blood, semen or rotten food through visual, olfactory or tactile stimuli, or multiple sensory modalities simultaneously. Individuals demonstrated risk-sensitivity when confronted with ‘contaminated’ food items, manifest as increased latencies to consuming food rewards, maintenance of greater distances from contaminants, increased olfactory investigations and food manipulation behaviors, reduced engagement during certain experiments, and/or outright refusals to consume food in test versus control conditions. In addition, as observed in bonobos, risk-sensitivity seemed to increase along a contamination probability gradient. Across experiments, all species appeared to use multiple sensory modalities (i.e. visual, olfactory, tactile, gustatory) to inform their feeding decisions. Studies on the sensory ecology of parasite avoidance are now needed to link the proximate and ultimate mechanisms of parasite avoidance behavior and relate them further to the epidemiology of infectious disease. In parallel to behavioral experiments and observations, I also collected fecal samples from Japanese macaques to test whether behavioral tendencies toward contaminant avoidance correlated with levels of gastrointestinal parasite infection. I showed that such ‘hygienic tendencies’ are good predictors of geohelminth infection intensity, as measured via fecal egg output. Future work must determine whether these results are generalizable, i.e. the extent to which risk-proneness in the face of contaminant exposure increases parasite acquisition and the progression of infectious disease across individuals and species. Taken together, this research allows us a better understanding of how non-human primates might avoid the acquisition of parasites. My results are consistent with other recent findings in the blossoming field of parasite avoidance behaviors in animals. My results are also consistent with what we would expect if the behaviors observed were governed by an adaptive system of disgust, which has been proposed as an evolutionary mechanism that protects organisms from infectious disease threats. Finally, I propose new avenues of research that may move us closer toward determining whether disgust mediates animal behavior as it does for human behavior. Future studies are also needed to explore the health and fitness benefits that a stronger behavioral immune system might confer.
... It comprises the consumption of faeces by animals. Many domestic species such as horses, pigs, and dogs either regularly or occasionally practise coprophagia (Soave and Brand 1991). In contrast, some species including goats (at least in an unconfined grazing system) will almost always reject any plants contaminated with the scent of their own species' urine or faeces. ...
... Rodent models also have several well-recognized limitations associated with their genetic, anatomical, and physiological differences with humans [13,14]. Among these limitations is the persistent tendency of rodents to practice gastrointestinal auto-and allo-reinoculation with large intestine microbiota (via fecal ingestion, or coprophagy) in laboratory settings [15][16][17]. This pervasive behavior has been documented in classical studies using observational techniques in both conventional and GF mice [18], in conventional mice maintained on standard and fortified diets [19], in animals with and without access to food [20], and across different mouse strains [16,21]. ...
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Background: The upper gastrointestinal tract plays a prominent role in human physiology as the primary site for enzymatic digestion and nutrient absorption, immune sampling, and drug uptake. Alterations to the small intestine microbiome have been implicated in various human diseases, such as non-alcoholic steatohepatitis and inflammatory bowel conditions. Yet, the physiological and functional roles of the small intestine microbiota in humans remain poorly characterized because of the complexities associated with its sampling. Rodent models are used extensively in microbiome research and enable the spatial, temporal, compositional, and functional interrogation of the gastrointestinal microbiota and its effects on the host physiology and disease phenotype. Classical, culture-based studies have documented that fecal microbial self-reinoculation (via coprophagy) affects the composition and abundance of microbes in the murine proximal gastrointestinal tract. This pervasive self-reinoculation behavior could be a particularly relevant study factor when investigating small intestine microbiota. Modern microbiome studies either do not take self-reinoculation into account, or assume that approaches such as single housing mice or housing on wire mesh floors eliminate it. These assumptions have not been rigorously tested with modern tools. Here, we used quantitative 16S rRNA gene amplicon sequencing, quantitative microbial functional gene content inference, and metabolomic analyses of bile acids to evaluate the effects of self-reinoculation on microbial loads, composition, and function in the murine upper gastrointestinal tract. Results: In coprophagic mice, continuous self-exposure to the fecal flora had substantial quantitative and qualitative effects on the upper gastrointestinal microbiome. These differences in microbial abundance and community composition were associated with an altered profile of the small intestine bile acid pool, and, importantly, could not be inferred from analyzing large intestine or stool samples. Overall, the patterns observed in the small intestine of non-coprophagic mice (reduced total microbial load, low abundance of anaerobic microbiota, and bile acids predominantly in the conjugated form) resemble those typically seen in the human small intestine. Conclusions: Future studies need to take self-reinoculation into account when using mouse models to evaluate gastrointestinal microbial colonization and function in relation to xenobiotic transformation and pharmacokinetics or in the context of physiological states and diseases linked to small intestine microbiome and to small intestine dysbiosis. Video abstract.
... More possibly, an individual could be infected with two closely related AstV strains, which may recombine and provide the chance for interspecies transmission with the emergence of a novel or more virulent human strains (Wohlgemuth et al., 2019). More importantly, coprophagous animals like pigs might directly get infected via ingestion of contaminated feces from other infected animals, including humans, which could then provide the opportunity for the coinfection and recombination of AstVs (Soave and Brand, 1991). The subsequent shedding of the new virus in their feces could result in an environmental risk as well as public health concern. ...
Article
Swine could serve as a natural reservoir for a large variety of viruses, including potential zoonotic enteric viruses. The presence of viruses with high genetic similarity between porcine and human strains may result in the emergence of zoonotic or xenozoonotic infections. Furthermore, the globalization and intensification of swine industries exacerbate the transmission and evolution of zoonotic viruses among swine herds and individuals working in swine-related occupations. To effectively prevent the public health risks posed by zoonotic swine enteric viruses, designing, and implementing a comprehensive measure for early diagnosis, prevention, and mitigation, requires interdisciplinary a collaborative ‘‘One Health" approach from veterinarians, environmental and public health professionals, and the swine industry. In this paper, we reviewed the current knowledge of selected potential zoonotic swine enteric viruses and explored swine intensive production and its associated public health risks.
... Since WT and KO mice did not exhibit differences in circulating LPS, and glandular saliva can be considered sterile (Schroder et al., 2017), we reasoned that salivary LPS was derived from oral bacteria in anesthetized mice. When awake, mice also may ingest LPS from food and coprophagy (Soave and Brand, 1991). To directly test the effect of swallowed LPS on the GI tract, mice were fed LPS in their drinking water and the effect on intestinal motility was determined (Anitha et al., 2012). ...
Preprint
Saliva plays important roles in the mastication, swallowing and digestion of food, speech and lubrication of oral mucosa, antimicrobial and anti-inflammatory activity and control of body temperature in grooming animals. The salivary protein BPIFA2 (BPI fold containing family A member 2; former names: Parotid Secretory Protein, PSP, SPLUNC2, C20orf70) is related to lipid-binding and LPS-binding proteins expressed in mucosa. Indeed, BPIFA2 binds LPS but the physiological role of BPIFA2 remains to be determined. To address this question, Bpifa2 knockout (Bpifa2[tm1(KOMP)Vlcg]) (KO) mice were phenotyped with a special emphasis on saliva and salivary glands. Saliva collected from KO mice was less able to spread on a hydrophobic surface than wild-type saliva and the surface tension of KO saliva was close to that of water. These data suggest that BPIFA2 is a salivary surfactant that is mainly responsible for the low surface tension of mouse saliva. The reduced surfactant activity of KO saliva did not affect consumption of dry food or grooming, but saliva from KO mice contained less LPS than wild-type saliva. Indeed, mice lacking BPIFA2 responded to ingested LPS with an increased stool frequency, suggesting that BPIFA2 plays a role in the solubilization and activity of ingested LPS. Consistent with these findings, BPIFA2-depleted mice also showed increased insulin secretion and metabolomic changes that were consistent with a mild endotoxemia. These results support the distal physiological function of a salivary protein and reinforce the connection between oral biology and systemic disease.
... In pigs, during the suckling period up to day 14, the nursing dam influences the fecal bacterial community which shows progressive changes, with specific bacteria taxa associated with the nursing sow (Bian et al., 2016). Besides parent/nurse-offspring contact, in some species such as pigs (Soave and Brand, 1991), rabbits , horses (Crowell-Davis and Houpt, 1985), and rats (Galef, 1979), early coprophagia behavior is also likely to play an important role in parent/nurse-to-offspring transmission of the microbiota. It has been demonstrated that, in rabbits, preventing coprophagia delays microbiota maturation . ...
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Evolutionary biologists studying wild species have demonstrated that genetic and non-genetic sources of information are inherited across generations and are therefore responsible for phenotypic resemblance between relatives. Although it has been postulated that non-genetic sources of inheritance are important in natural selection, they are not taken into account for livestock selection that is based on genetic inheritance only. According to the natural selection theory, the contribution of non-genetic inheritance may be significant for the transmission of characters. If this theory is confirmed in livestock, not considering non-genetic means of transmission in selection schemes might prevent achieving maximum progress in the livestock populations being selected. The present discussion paper reviews the different mechanisms of genetic and non-genetic inheritance reported in the literature as occurring in livestock species. Non-genetic sources of inheritance comprise information transmitted via physical means, such as epigenetic and microbiota inheritance, and those transmitted via learning mechanisms: behavioral, cultural and ecological inheritance. In the first part of this paper we review the evidence that suggests that both genetic and non-genetic information contribute to inheritance in livestock (i.e. transmitted from one generation to the next and causing phenotypic differences between individuals) and discuss how the environment may influence non-genetic inherited factors. Then, in a second step, we consider methods for favoring the transmission of non-genetic inherited factors by estimating and selecting animals on their extended transmissible value and/or introducing favorable non-genetic factors via the animals’ environment.
... E) Morder madeira: o animal morde a madeira como portas e baias(Mills & Nankervis, 2005). F) Coprofagia: o equino ingere as suas fezes ou de outro animal(Soave & Brand, 1991).G) Lambedura de cocho: o animal lambe repetitivamente o cocho após ingerido o alimento. H) Bater na porta da baia: bater com os membros anteriores na porta da baia (Cooper et al., 2005). ...
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Buscando avaliar o comportamento e as condições de bem-estar dos cavalos utilizados no Centro de Equoterapia do IF Goiano Ceres, GO, foram realizadas avaliações entre março e agosto de 2018, quanto ao temperamento, estado de saúde e comportamentos normais e estereotipados expressos antes, durante e após as sessões equoterápicas, turnos das sessões e diferenças individuais de cada animal. Não houve diferença para o temperamento quanto tempo de serviço semanal, idade do animal e condição física (p > 0,05). Os animais avaliados demonstraram temperamento adequados a cavalos utilizados para a finalidade equoterápica. As frequências cardíacas foram maiores antes das sessões, as frequências respiratórias foram maiores antes e até 15 minutos após o início das sessões (p < 0,05). Estação distraído foi o comportamento mais observado (63%) que ocorreu com animais antes e após as sessões e a estação alerta (36%) foi expressa com maior frequência durante as sessões (p < 0,05). Os comportamentos estereotipados foram pouco frequentes, sendo expressado em apenas um animal antes das sessões equoterápicas. Os indicadores de saúde, de condição corporal e parâmetros comportamentais avaliados estavam de acordo com os comportamentos da espécie, mostrando que os animais do Centro de Equoterapia do IF Goiano Ceres apresentam um bem-estar adequado.
... Coprophagy is common in many animal species, including turkeys (87)(88)(89) and it is common to see turkeys consuming cecal drops of their cage mates. This innate behavior in turkeys may have evolved to enable bird-to-bird spread of beneficial microbiota within a flock. ...
Preprint
Turkeys ( Meleagris gallopavo ) provide a globally important source of protein and constitute the second most important source of poultry meat in the world. Bacterial diseases are common in commercial poultry production causing significant production losses for farmers. Due to the increasingly recognized problems associated with large-scale/indiscriminant antibiotic use in agricultural settings, poultry producers need alternative methods to control common bacterial pathogens. In this study we compared the cecal microbiota of wild and domestic turkeys, hypothesizing that environmental pressures faced by wild birds may select for a disease-resistant microbial community. Sequence analysis of 16S rRNA genes amplified from cecal samples indicate that free-roaming wild turkeys carry a rich and variable microbiota compared to domestic turkeys raised on large-scale poultry farms. Wild turkeys also had very low levels of Staphylococcus, Salmonella and E. coli when compared to domestic turkeys. E. coli strains isolated from wild or domestic turkey cecal samples also belong to distinct phylogenetic backgrounds and differ in their propensity to carry virulence genes. E. coli strains isolated from factory-raised turkeys were far more likely to carry genes for capsule ( kpsII , kpsIII ) or siderophore ( iroN , fyuA ) synthesis than those isolated from wild turkeys. These results suggest that the microbiota of wild turkeys may provide colonization resistance against common poultry pathogens. Importance Due to the increasingly recognized problems associated with antibiotic use in agricultural settings, poultry producers need alternative methods to control common bacterial pathogens. In this study we compare the microbiota of wild and domestic turkeys. Results suggest that free ranging wild turkeys carry a distinct microbiome when compared to farm raised turkeys. The microbiome of wild birds contains very low levels of poultry pathogens compared to farm raised birds. The microbiomes of wild turkeys may be used to guide development of new ways to control disease in large scale poultry production.
... Because the dentalite morphology found on the Nanjemoy coprolites is congruent with specimens from different units worldwide (Godfrey & Smith 2010;Eriksson et al. 2011;Milàn et al. 2012;Godfrey & Palmer 2015;Dentzien-Dias et al. 2018), we believe that some Nanjemoy coprolites were intentionally mouthed by exploring or foraging animals and that these bites were not accidental. Nowadays, several vertebrates and invertebrates are known to be facultatively coprophagous (Frankenberg & Smith 1967;Robertson 1982;Cambefort 1991;Soave & Brand 1991). ...
Article
The Eocene Nanjemoy Formation crops out on the Maryland and Virginia Coastal Plain, along the eastern coast of the United States. This formation is composed of sands, silts and clays and is divided into the Potapaco and Woodstock members. Remains of fishes, reptiles, birds, mammals, molluscs, fruits and seeds are common in the Potapaco Member, in addition to vertebrate coprolites. Here, we present an analysis of more than 2000 coprolites from the Fisher/Sullivan Site in Virginia. The chemical composition (phosphatic) and the type of inclusions (fish bones) indicate that only scats of carnivorous animals were preserved. The analysed specimens were grouped into six morphotypes: (1) the cylindrical morphotype is a cylinder with rounded ends; (2) the segmented morphotype is a cylinder segmented with rounded ends, and occasionally one end is concave; (3) the oval morphotype represents a bean‐shaped coprolite; (4) the scroll morphotype is cylindrical to conical in lateral view and has coils seen only at the ends; (5) the folded morphotype is a spiral that is concentrically folded; and (6) the sinuous morphotype is serpentine, with rounded ends. Coprophagy‐related scrape traces occur in different morphotypes and represent both invertebrate burrows and bite traces made by fishes. The mineralogical and chemical analyses indicate an early precipitation of phosphate and pyrite minerals, probably induced by the microbial community. All coprolites at the Fisher/Sullivan Site were produced by fishes: carcharhiniform sharks for the scroll morphotype and lamniform sharks, probably the genus Carcharias, for the folded morphotype; the oval, cylindrical and segmented morphotypes were likely produced by actinopterygian fishes.
... bacteria, viruses, parasitic protozoa and helminths) abound in animal excreta. Other animal species, however, such as pigs, dogs and rabbits exhibit coprophagy to acquire certain digestive enzymes lacking in their diet, obtain nutrients that were unabsorbed in the gastrointestinal tract during the first passage and/or to develop their microbiome [13]. However, it was only very recently that scientists started testing whether faeces or other faecally contaminated substrates elicit avoidance in non-human primates [14][15][16][17][18][19]. ...
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Parasites constitute a major selective pressure which has shaped animal behaviour through evolutionary time. One adaption to parasites consists of recognizing and avoiding substrates or cues that indicate their presence. Among substrates harbouring infectious agents, faeces are known to elicit avoidance behaviour in numerous animal species. However, the function and mechanisms of faeces avoidance in non-human primates has been largely overlooked by scientists. In this study, we used an experimental approach to investigate whether aversion to faeces in a foraging context is mediated by visual and olfactory cues in two cercopithecoid primates: mandrills (Mandrillus sphinx) and long-tailed macaques (Macaca fascicularis). Visual and olfactory cues of faeces elicited lower food consumption rates in mandrills and higher food manipulation rates in long-tailed macaques. Both results support the infection-avoidance hypothesis and confirm similar tendencies observed in other primate species. More studies are now needed to investigate the divergence of avoidance strategies observed in non-human primates regarding food contamination.
... Coprophagy is a feeding strategy commonly found in invertebrates (Weiss 2006), but much less so in vertebrates. Coprophagy sometimes exists in mammals such as rodents and lagomorphs, and to a lesser degree in pigs, horses, dogs and nonhuman primates (Thacker and Brandt 1955;Soave and Brand 1991;Marinier and Alexander 1995;Aitken 2003;Krief and Hladik 2004). In amphibians, coprophagy is rare but when present may influence larval development of some species with herbivorous larvae. ...
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The transition from carnivory to omnivory is poorly understood. The ability to feed at more than one trophic level theoretically increases an animals fitness in a novel environment. Because of the absence of light and photosynthesis, most subterranean ecosystems are characterized by very few trophic levels, such that food scarcity is a challenge in many subterranean habitats. One strategy against starvation is to expand diet breadth. Grotto salamanders ( Eurycea spelaea ) are known to ingest bat guano deliberately, challenging the general understanding that salamanders are strictly carnivorous. Here we tested the hypothesis that grotto salamanders have broadened their diet related to cave adaptation and found that, although coprophagous behavior is present, salamanders are unable to acquire sufficient nutrition from bat guano alone. Our results suggest that the coprophagic behavior has emerged prior to physiological or gut biome adaptations.
... Because of its high environmental stability and prevalence in numerous animal species, opportunities for spillover are abundant. Coprophagous animals such as pigs and wild boars could become directly infected though ingestion of feces from another infected species (Soave and Brand, 1991). Additionally, bats roosting in barns and other agricultural dwellings can defecate on and infect livestock, especially cattle and pigs (Fischer et al., 2017) (Fig. 3). ...
Article
Astroviruses are small, non-enveloped, positive-sense, single-stranded RNA viruses that belong to the Astroviridae family. Astroviruses infect diverse hosts and are typically associated with gastrointestinal illness; although disease can range from asymptomatic to encephalitis depending on the host and viral genotype. Astroviruses have high genetic variability due to an error prone polymerase and frequent recombination events between strains. Once thought to be species specific, recent evidence suggests astroviruses can spread between different host species, although the frequency with which this occurs and the restrictions that regulate the process are unknown. Recombination events can lead to drastic evolutionary changes and contribute to cross-species transmission events. This work reviews the current state of research on astrovirus evolution and emergence, especially as it relates to cross-species transmission and recombination of astroviruses.
... Rabbit coprophagy was first reported in the scientific literature in 1882 [41]. Rabbits produced 2 types of feces, soft mucous-covered feces during the night and hard dry pellet-like feces in the daytime; and rabbits took soft feces directly from their anus and swallowed them like pills [41,42]. Coprophagy is of significance in rabbits because soft-feces consumption is conducive to the establishment of a nutritious intestinal microflora in rabbits and the soft feces supply rabbits with nitrogen, protein, sulfur and vitamins. ...
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Background Rabbit can produce meat, fur and leather, and serves as an important biomedical animal model. Understanding the microbial community of rabbits helps to raise rabbits healthily and better support their application as animal models. Results In this study, we selected 4 healthy Belgium gray rabbits to collect the microbial samples from 12 body sites, including skin, lung, uterus, mouth, stomach, duodenum, ileum, jejunum, colon, cecum, cecal appendix and rectum. The microbiota across rabbit whole body was investigated via 16S rRNA gene amplicon sequencing. After quality control, 46 samples were retained, and 3,148 qualified ASVs were obtained, representing 23 phyla and 264 genera. Based on the weighted UniFrac distances, these samples were divided into the large intestine (Lin), stomach and small intestine (SSin), uterus (Uter), and skin, mouth and lung (SML) groups. The diversity of Lin microbiota was the highest, followed by those of the SSin, Uter and SML groups. In the whole body, Firmicutes (62.37%), Proteobacteria (13.44%) and Bacteroidota (11.84%) were the most predominant phyla. The relative abundance of Firmicutes in the intestinal tract was significantly higher than that in the non-intestinal site, while Proteobacteria was significantly higher in the non-intestinal site. Among the 264 genera, 35 were the core microbiota distributed in all body sites. Sixty-one genera were specific in the SML group, while 13, 8 and 1 were specifically found in the Lin, SSin and Uter groups, respectively. The Lin group had the most difference with other groups, there were average 72 differential genera between the Lin and other groups. The functional prediction analysis showed that microbial function within each group was similar, but there was a big difference between the intestinal tracts and the non-intestinal group. Notably, the function of microorganism in uterus and mouth were the most different from those in the gastrointestinal sites; rabbit’s coprophagy of consuming soft feces possibly resulted in little differences of microbial function between stomach and large intestinal sites. Conclusion Our findings improve the knowledge about rabbit microbial communities throughout whole body and give insights into the relationship of microbial communities among different body sites in health rabbits.
... These microorganisms decompose cellulose and produce volatile fatty acids(VFA) for rabbits to use [23]. In addition, due to the coprophagy of rabbits, microorganisms can provide certain bacterial proteins for domestic rabbits [24]. The transparent circle on the CMC-Congo Red plate indicates that the bacterium can decompose cellulose, it means that C. sartagoforme XN-T4 has the potential to improve the digestibility of cellulose for herbivores as a microbial feed additive. ...
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In order to develop microbial additives for rabbit feed, a spore-forming bacteria was isolated from the feces of Hyla rabbit using reinforced clostridium medium (RCM). The 16S rDNA sequence of the bacterium was subjected to pairwise sequence alignment using BLAST; the colony morphology, and physiological, biochemical, and stress resistance were studied. The results showed that the bacterium was Clostridium sartagoforme , a gram positive anaerobe, which can produce spores. The colony diameter was 0.5 mm—2.5 mm, the diameter of the bacteria was 0.5 μm—1.0 μm × 2.0 μm—6.3 μm, and the spore diameter was 1 μm—1.2 μm × 1 μm—1.2 μm. C . sartagoforme can utilize various sugars and alcohols such as fructose, galactose, sorbitol, and inositol. It secreted cellulase into the extracellular environment to form a transparent hydrolysis circle in Congo red medium, it could not liquify gelatin, and the lysine decarboxylase reaction was positive. In liquid medium it entered the stable growth period after 9 h of inoculation. Additionally, it had good stress resistance with a survival rate that exceeded 53% after gastric juice (pH 2.5) treatment for 3 h, it grew in a medium with a bile salt concentration of 0.3%, and the survival rate exceeded 85% after 10 minutes at 80°C. Moreover, animal testing indicated that this strain has no adverse effects on the morbidity and mortality of rabbits. In summary, C . sartagoforme XN-T4 was isolated from rabbit feces. This bacterium has good resistance to stress, can decompose a variety of monosaccharides and polysaccharides including cellulose, which is relatively harmless for animal health.
... As a result, a wide variety of host adaptations have evolved to optimize the digestive efficiency of symbiotic gut microbiota, including sacculated stomachs, enlarged ceca and colons, and rumination 4,5 in ungulates and coprophagous mammals. 6 Among primates, lineages have evolved either a large, multi-chambered foregut (stomach) 7 or a voluminous hindgut (cecum-colon), 8 in which high volumes of fiber are fermented by symbiotic microorganisms. Colobine primates have a sacculated foregut and a relatively small hindgut compared with hindgut-fermenting primates. ...
Article
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In mammal herbivores, fiber digestion usually occurs predominantly in either the foregut or the hindgut. Reports of mechanisms showing synergistic function in both gut regions for the digestion of fiber and other nutrients in wild mammals are rare since it requires integrative study of anatomy, physiology and gut microbiome. Colobine monkeys (Colobinae) are folivorous, with high-fiber foods fermented primarily in their foreguts. A few colobine species live in temperate regions so obtaining energy from fiber during the winter is essential. However, the mechanisms enabling this remain largely unknown. We hypothesized that such species possess specialized mechanisms to enhance fiber digestion in the hindgut and studied microbial and morphological digestive adaptations of golden snub-nosed monkeys (GSMs), Rhinopithecus roxellana. Which is a temperate forest colobine from central China that experiences high thermal energy demands while restricted to a fibrous, low-energy winter diet. We tested for synergistic foregut and hindgut fiber digestion using comparisons of morphology, microbiome composition and function, and digestive efficiency. We found that the GSM’s colon has a significantly greater volume than that of other foregut-fermenting colobines. The microbiomes of the foregut and hindgut differed significantly in composition and abundance. However, while digestive efficiency and the expression of microbial gene functions for fiber digestion were higher in the foregut than in the hindgut, both gut regions were dominated by microbial taxa producing enzymes to enable active digestion of complex carbohydrates. Our data suggest that both the GSM foregut and hindgut facilitate fiber digestion, and that an enlarged colon is likely an adaptation to accommodate high throughput of fiber-rich food during winter.
... The transfer of maternal microbes to the mammalian young begins during the birthing process and continues through nursing and social interactions (74,75). Coprophagy is common in many animal species, including turkeys (76)(77)(78), and it is common to see turkeys consuming cecal drops of their cage mates. This innate behavior in turkeys may have evolved to enable the bird-to-bird spread of beneficial microbiota within a flock. ...
Article
Full-text available
Turkeys ( Meleagris gallopavo ) provide a globally important source of protein and constitute the second most important source of poultry meat in the world. Bacterial diseases are common in commercial poultry production causing significant production losses for farmers. Due to the increasingly recognized problems associated with large-scale/indiscriminant antibiotic use in agricultural settings, poultry producers need alternative methods to control common bacterial pathogens. In this study we compared the cecal microbiota of wild and domestic turkeys, hypothesizing that environmental pressures faced by wild birds may select for a disease-resistant microbial community. Sequence analysis of 16S rRNA genes amplified from cecal samples indicate that free-roaming wild turkeys carry a rich and variable microbiota compared to domestic turkeys raised on large-scale poultry farms. Wild turkeys also had very low levels of Staphylococcus, Salmonella and E. coli when compared to domestic turkeys. E. coli strains isolated from wild or domestic turkey cecal samples also belong to distinct phylogenetic backgrounds and differ in their propensity to carry virulence genes. E. coli strains isolated from factory-raised turkeys were far more likely to carry genes for capsule ( kpsII , kpsIII ) or siderophore ( iroN , fyuA ) synthesis than those isolated from wild turkeys. These results suggest that the microbiota of wild turkeys may provide colonization resistance against common poultry pathogens. Importance Due to the increasingly recognized problems associated with antibiotic use in agricultural settings, poultry producers need alternative methods to control common bacterial pathogens. In this study we compare the microbiota of wild and domestic turkeys. Results suggest that free ranging wild turkeys carry a distinct microbiome when compared to farm raised turkeys. The microbiome of wild birds contains very low levels of poultry pathogens compared to farm raised birds. The microbiomes of wild turkeys may be used to guide development of new ways to control disease in large scale poultry production.
... However, there has been surprisingly little research documenting the role of coprophagy in the foraging dynamics of these fishes. Coprophagy has clear documentation and significance in terrestrial ecosystems (e.g., Soave and Brand 1991;Hirakawa 2001;Nalepa et al. 2001). It may also play an important role in nutrient transfer in marine ecosystems, such as providing a source of iron in the mesopelagic (Le Mézo and Galbraith 2021), nitrogen and phosphorus in temperate littoral systems (Pinnegar and Polunin 2006), carbon and nitrogen for marine invertebrates (Frankenberg and Smith 1967), and as a possible source of detrital organic matter for marine zooplankton recycling (Turner and Ferrante 1979). ...
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Parrotfishes and surgeonfishes are major Caribbean herbivores that primarily graze reef algae and thereby play an important functional role in indirectly promoting coral recruitment and growth. Yet, an emerging body of research suggests that these nominal herbivores graze on a diverse array of other food sources and researchers have questioned whether they may target more nutrient-dense foods growing within or upon algae, such as cyanobacteria. In this study, we investigated the species-specific foraging rates of parrotfishes and surgeonfishes on Brown Chromis (Chromis multilineata) fecal pellets compared to other major dietary items. We found that almost 85% of observed fecal pellets were ingested by fishes and that over 90% of ingested fecal pellets were consumed by parrotfishes and surgeonfishes alone. While there were species-specific differences in the levels of feces consumption (coprophagy), we found that all three surgeonfishes (Acanthurus chirurgus, A. coeruleus, and A. tractus) and six of the nine of parrotfish species surveyed (Scarus coeruleus, S. iseri, S. taeniopterus, S. vetula, Sparisoma aurofrenatum, and S. viride) consumed C. multilineata feces. To better understand the nutritional value of this behavior, we analyzed the composition of proteins, lipids, carbohydrates, total calories, and micronutrients in C. multilineata fecal pellets and compared these to published values for other food sources targeted by these fishes. Our findings suggest that these fecal pellets may have higher values of proteins, carbohydrates, total calories, and important micronutrients, such as phosphorus, compared to various macroalgae and the epilithic algae matrix, though comparable or lower values compared to cyanobacteria. To our knowledge, this is the first study to document coprophagy by tropical herbivorous fishes in the Caribbean region. This research advances our understanding of the foraging ecology of nominally herbivorous fishes and highlights the importance of fish feces as a nutritional resource on coral reefs. Graphical abstract
... Intrinsic environmental factors, such as the interaction of mice with their cage mates, are known to influence the composition of gut microbiomes (Deloris Alexander et al., 2006;Kovacs et al., 2011;Hildebrand et al., 2013). Mice are known to ingest feces excreted by their co-housed mates either through direct consumption or through grooming (Soave and Brand, 1991). This practice, called coprophagy, is likely the primary driver of gut microbiota convergence or synchronization in co-housed mice (Deloris Alexander et al., 2006;Hildebrand et al., 2013;Nguyen et al., 2015). ...
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Murine models have become essential tools for understanding the complex interactions between gut microbes, their hosts, and disease. While many intra-facility factors are known to influence the structure of mouse microbiomes, the contribution of inter-facility variation to mouse microbiome composition, especially in the context of disease, remains under-investigated. We replicated microbiome experiments using identical mouse lines housed in two separate animal facilities and report drastic differences in composition of microbiomes based upon animal facility of origin. We observed facility-specific microbiome signatures in the context of a disease model [the Ednrb (endothelin receptor type B) Hirschsprung disease mouse] and in normal C57BL/6J mice. Importantly, these facility differences were independent of cage, sex, or sequencing-related influence. In addition, we investigated the reproducibility of microbiome dysbiosis previously associated with Ednrb-/- (knock-out; KO) mice. While we observed genotype-based differences in composition between wild-type (WT) and KO mice, these differences were inconsistent with the previously reported conclusions. Furthermore, the genotype-based differences were not identical across animal facilities. Despite this, through differential abundance testing, we identified several conserved candidate taxa and candidate operational taxonomic units that may play a role in disease promotion or protection. Overall, our findings raise the possibility that previously reported microbiome-disease associations from murine studies conducted in a single facility may be heavily influenced by facility-specific effects. More generally, these results provide a strong rationale for replication of mouse microbiome studies at multiple facilities, and for the meticulous collection of metadata that will allow the confounding effects of facility to be more specifically identified.
... Coprophagy is the behavior of eating feces to help establish the intestinal microbiota, and to acquire protein and micronutrients, which is common in lagomorphs, rodents and other species (Soave and Brand, 1991). The term caecotrophy refers specially to soft faeces ingestion practiced by rabbits and small herbivores (small hindgut fermenters) (Hoernicke, 1981). ...
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The endotherms, particularly the small mammals living in the polar region and temperate zone, are faced with extreme challenges for maintaining stable core body temperatures in harsh cold winter. The non-hibernating small mammals increase metabolic rate including obligatory thermogenesis (basal/resting metabolic rate, BMR/RMR) and regulatory thermogenesis (mainly nonshivering thermogenesis, NST, in brown adipose tissue and skeletal muscle) to maintain thermal homeostasis in cold conditions. A substantial amount of evidence indicates that the symbiotic gut microbiota are sensitive to air temperature, and play an important function in cold-induced thermoregulation, via bacterial metabolites and byproducts such as short-chain fatty acids and secondary bile acids. Cold signal is sensed by specific thermosensitive transient receptor potential channels (thermo-TRPs), and then norepinephrine (NE) is released from sympathetic nervous system (SNS) and thyroid hormones also increase to induce NST. Meanwhile, these neurotransmitters and hormones can regulate the diversity and compositions of the gut microbiota. Therefore, cold-induced NST is controlled by both Thermo-TRPs—SNS—gut microbiota axis and thyroid—gut microbiota axis. Besides physiological thermoregulation, small mammals also rely on behavioral regulation, such as huddling and coprophagy, to maintain energy and thermal homeostasis, and the gut microbial community is involved in these processes. The present review summarized the recent progress in the gut microbiota and host physiological and behavioral thermoregulation in small mammals for better understanding the evolution and adaption of holobionts (host and symbiotic microorganism). The coevolution of host-microorganism symbionts promotes individual survival, population maintenance, and species coexistence in the ecosystems with complicated, variable environments.
Article
This study was conducted to elucidate the intestinal dysmotility during coccidiosis. C57BL/6 male mice at seven weeks of age were inoculated with Eimeria pragensis sporulated oocysts (100 to 1,000 oocysts). The intestinal motility was evaluated by observing discharging time of barium sulfate (Ba2SO4) after oral administration (WITT: the whole intestinal transit time). The exact location of the dysmotility was analyzed by intermittent barium gastrography. Upper intestinal dysmotility was evaluated by charcoal propulsion study. Additionally, the occurrence of dysmotility was observed at different post-infection times (4, 7, and 14 days post-infection (d.p.i.)) and in infection-dose dependent manner (100, 300, and 1,000 oocysts). As the E. pragensis infected mice had significantly lower feed intake compared to the control group, we designed a feed apprehension study to evaluate the effect of low feed intake on the intestinal dysmotility. The WITT of infected mice at 7 d.p.i. was significantly longer (6 hr) than the uninfected mice (2.5 hr). Intestinal dysmotility was observed in the small intestine, caecum, and colorectum in the infected mice. Charcoal propulsion was slower in infected group (reaching to 40.4% of the whole small intestine) compared to control group (68.0%). The dysmotility was observed at the beginning of the patent period (7 d.p.i.) and subsided as the patency ended (14 d.p.i.). Mice with lower feed intake appeared to have similar intestinal motility as control mice. In summary, this study revealed the evidence of intestinal hypomotility during E. pragensis infection.
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Commercial mouse chow is designed to provide a complete, nutrient-rich diet, and it can contain upwards of 100 mg/kg manganese, an essential mineral. Manganese acts as a relaxation time-shortening contrast agent for both T 1 and T 2 , and where standard chow is hydrated in the gastrointestinal tract, bright signals are produced when using T 1 -weighted imaging (T 1 WI). As a result of peristalsis, gastrointestinal hyperintensities result in temporally unstable signals, leading to image ghosting and decreased resolution from that prescribed. To avoid the problem, various methods of gastrointestinal tract modulation, including the use of intestinal cleansing with laxatives and dietary modulation, have been reported. Here, dietary modulation has been extended to the use of a biologically innocuous, long-term change of diet. In this study, we report on the use of a commercially available manganese-free chow to improve the image quality of the gastrointestinal tract. This manganese-free chow, apart from the omitted manganese which is available in tap water, is a complete diet and readily available. We investigated the time-dependent, diet-related gastrointestinal intensities on short-TR T 1 WI magnetic resonance imaging; monitored body mass, food and water consumption and standard blood biochemistry analysis following diet change; and determined manganese concentration in blood plasma following a five-day change to manganese-free chow. We show that the manganese-free chow presents a refinement to other gastrointestinal tract modulation, as it avoids the need for invasive procedures for gut voiding and can be provided ad libitum so that animals can be maintained with no need for prescribed diet change before imaging.
Article
Lagidium viscacia is considered as a fragile species with patchy distribution, a strict habitat specialist and an obligatory diet specialist. The Southern Andean Precordillera constitutes an interesting environment to analyze the species’ presence across the altitudinal gradient. Diet selection and habitat use were studied in the summit plateau, characterized by rigorous conditions and vegetation representative of the Southern Puna. Pellet groups were counted in transects perpendicular to rock formations, and diet and vegetation were seasonally analyzed using microhistological analysis and point-quadrat transects. Vizcachas were strictly associated with rock formations at middle and high altitudes, with higher occurrence on the mountain summit where grasslands surrounded the rock formations. Vizcachas avoided shrubs associated with rock formations and preferred grasses on sandy soils. Phenological changes slightly affected the selective diet that involves a considerable search effort and risky feeding activity. Puna grasslands constituted attractive feeding places where L. viscacia ’s activity decreased with distance from rock shelters as expected for a central-place forager. Habitat partitioning allows coexistence with Ctenomys mendocinus , despite the high dietary overlap between these central-place species. The high mobility and broad diet of Lama guanicoe reduce the competition risk. Lepus europaeus preferred shrubs and forbs, determining a discrete dietary overlap with vizcachas.
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Medication-related osteonecrosis of the jaw (MRONJ) is a rare intraoral lesion that occurs in patients undergoing long-term and/or high-dose therapy with nitrogen-containing bisphosphonates, a RANKL inhibitor, antiangiogenic agents, or mTOR inhibitors. The presence of pathogenic bacteria is highly associated with advanced stages of MRONJ lesions; however, the exact role of indigenous microbes in MRONJ development is unknown. Here, we report that the normal oral flora in mice protects against inflammation-induced osteonecrosis. In mice that developed osteonecrosis following tooth extraction, there was increased bacterial infiltration when compared with healed controls. Antibiotic-mediated oral dysbiosis led to a local inhibition of bone resorption in the presence of ligature-induced periodontitis (LIP). There was no significant difference in empty lacunae, necrotic bone formation, osteoclast number, and surface area in antibiotic-treated as compared with conventionally colonized mice following extraction of healthy teeth after zoledronic acid infusions. However, extraction of LIP teeth led to increased empty lacunae, necrotic bone, and osteoclast surface area in antibiotic- and zoledronic acid–treated mice as compared with conventionally colonized mice. Our findings suggest that the presence of the indigenous microbiota protects against LIP-induced osteonecrosis.
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Coprophagy has been described in piglets although its importance has not been fully assessed. This study aimed to evaluate how deprivation of maternal feces influenced piglet physiology, behavior, and performance. Eight litters were randomly assigned to one of two treatments. Control (CON) litters had access to maternal feces while deprived (DEP) litters were deprived of maternal feces for the first 7 d post-partum. Piglet behavior was quantified for 24 h at 7 d of age. Blood samples were collected from one male and female from each litter at 0, 7, and 21 d for hematological analyses and post-weaning performance was assessed until 123 d post-weaning. No treatment effects were observed on piglet behavior. DEP piglets had 25% lower leukocyte counts (p < 0.01). Relative to DEP litters, CON litters had increased post-weaning feed intake (0.998 vs 0.901 kg/d; p = 0.02) and weight gain (0.536 vs 0.483 kg/d; p < 0.01). At 123 d post-weaning, CON pigs were 9.3 � 2.3 kg heavier than treatment pigs (p < 0.01). These results suggest that access to maternal feces improves immunocompetence and growth performance. Further studies are needed to explore the physiological mechanisms through which maternal feces improve growth performance, including nutritional and microbial factors, or the presence of maternal semiochemicals.
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The reinstatement and revision of abandoned therapeutic ventures of the past has been an integral part of medical research and advancement. In psychiatry, much interest was generated recently by emerging data on the use of faecal supplements for restoring the neurochemical balance in the brain, and on the ingestion of placenta to stabilize neural circuits disrupted by childbirth-related hormonal changes. Herein, we consider the emerging scientific evidence and socio-cultural prerequisites favouring the re-entry of these heterodox customs, which are reminiscent of widespread instinctive behaviours in wildlife, into modern healthcare. We explore their evolutionary background and adaptive significance, and consider mechanisms of therapeutic benefits. Finally, we reflect on emerging opportunities and challenges, which present clues towards better prevention and treatment of major neuropsychiatric disorders.
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Microbiomes are transmitted between generations by a variety of different vertical and/or horizontal modes, including vegetative reproduction (vertical), via female germ cells (vertical), coprophagy and regurgitation (vertical and horizontal), physical contact starting at birth (vertical and horizontal), breast-feeding (vertical), and via the environment (horizontal). Analyses of vertical transmission can result in false negatives (failure to detect rare microbes) and false positives (strain variants). In humans, offspring receive most of their initial gut microbiota vertically from mothers during birth, via breast-feeding and close contact. Horizontal transmission is common in marine organisms and involves selectivity in determining which environmental microbes can colonize the organism’s microbiome. The following arguments are put forth concerning accurate microbial transmission: First, the transmission may be of functions, not necessarily of species; second, horizontal transmission may be as accurate as vertical transmission; third, detection techniques may fail to detect rare microbes; lastly, microbiomes develop and reach maturity with their hosts. In spite of the great variation in means of transmission discussed in this paper, microbiomes and their functions are transferred from one generation of holobionts to the next with fidelity. This provides a strong basis for each holobiont to be considered a unique biological entity and a level of selection in evolution, largely maintaining the uniqueness of the entity and conserving the species from one generation to the next.
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Background: Microbial colonization and immune cell maturation coincide at mucosal sites and are decisive for postnatal lung development. How external factors influence neonatal pulmonary immune development is poorly understood. Objective: To elucidate the impact of key determinants in early life, nutrition, and maternal bonding, on postnatal lung maturation in a human-relevant animal model. To investigate the underlying immunological changes of impaired lung maturation and study the mechanisms of conversion. Methods: Newborn piglets were kept with or without isolation from their mothers and fed bovine milk-based infant formula or received milk of sow. Lung growth, histomorphology, respiratory immune responses, and lung microbiota were analyzed. Mother- and sow-milk-deprived piglets received maternal material or were reintroduced to the maternal environment at varying intervals to study options for reversal. Results: Formula feeding combined with isolation of newborn piglets resulted in disturbed postnatal lung maturation. Reduced lung growth correlated with dampened IL-33 expression, impaired lung myeloid cell activation, and decreased Th1 differentiation, along with diminished richness and diversity of the lung microbiota. Transfer of bacteria-enriched maternal material reversed the negative effects on pulmonary immune maturation. Early (within 3 days) but not late (within 7 days) reintroduction to the mother allowed restoration of normal lung development. Conclusion: Our findings reveal that lung growth, respiratory immunity, and microbial lung colonization in newborns depend on postnatal diet and maternal contact, and targeting these key regulators could promote lung development during this critical life stage. Summary: Disturbances in natural diet and reduced maternal contact during the neonatal period impair postnatal lung maturation. In pediatrics, timely breast milk feeding and intensive maternal bonding represent valuable intervention measures to promote early postnatal lung development.
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Objectives Parasite selection pressures have driven the evolution of numerous behavioral defenses in host species, but recent studies revealed individual variation in their expression. As little is known about the factors causing heterogeneity among individuals in infection-avoidance behaviors, we investigated in woolly monkeys (Lagothrix lagotricha poeppigii) the influence of several environmental and individual characteristics on the tendency to avoid food contaminated by soil and by their own and conspecifics' feces. Materials and methods We conducted feeding tests on 40 semi-free ranging individuals rescued from the pet trade. Using generalized linear mixed models, we investigated the effect of season, sex, age, dominance rank, and exposure to non-natural living conditions on feeding decisions. Results Woolly monkeys did not avoid soil-contaminated food and equally avoided food contaminated by their own and conspecifics' feces. Individuals varied greatly in their level of fecal avoidance. Only females exhibited strong avoidance of fecally contaminated food, but adapted their behavior to food availability, highlighting the trade-off between nutritional intake and parasite avoidance. Additionally, low-ranking females, less competitive over food resources, exhibited lower avoidance than dominant ones. Juveniles were more cautious than adults, possibly to compensate for a higher parasite susceptibility. Finally, we reported an unknown effect of exposure to non-natural living conditions on behavioral defenses, as animals kept as household pets for an extended period apparently lost their ability to avoid fecally contaminated food. Conclusion We argue that striving to understand variation in infection-avoidance behaviors in natural populations is crucial to predict disease spread and inform conservation policies.
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The perinatal period is a sensitive time in mammalian development that can have long-lasting consequences on offspring phenotype via maternal effects. Maternal effects have been most intensively studied with respect to two major conditions: maternal diet and maternal stress. In this review, we shift the focus by discussing five major additional maternal cues and their influence on offspring phenotype: maternal androgen levels, photoperiod (melatonin), microbiome, immune regulation, and milk composition. We present the key findings for each of these topics in mammals, their mechanisms of action, and how they interact with each other and with the maternal influences of diet and stress. We explore their impacts in the contexts of both predictive adaptive responses and the developmental origins of disease, identify knowledge gaps and research opportunities in the field, and place a particular emphasis on the application and consideration of these effects in non-model species and natural ecological systems.
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Background: In mammal herbivores, the digestion of fiber usually occurs predominantly in either the foregut or in the hindgut. However, how both gut regions function synergistically in the digestion of fiber and other nutrients has rarely been reported in wild mammals. This requires an integrative study of host anatomy, physiology and gut microbiome. Colobine monkeys (Colobinae) are folivorous, with fiber fermentation primarily occurring in the foregut, with residual fermentation in the hindgut. For the few colobine species that live in temperate regions obtaining energy from fiber during winter is critical but the mechanisms enabling this remain unclear. Results: We studied microbial and morphological digestive adaptations of golden snub-nosed monkeys (GSMs), Rhinopithecus roxellana, a temperate forest colobine from central China. We tested for synergistic foregut and hindgut fiber digestion in a species that experiences high thermal energy demands while restricted to a fibrous, low-energy winter diet. We found that the GSM’s colon has a significantly greater volume than that of other foregut fermenting colobines, and both gut regions of GSMs are dominated by microbial taxa producing enzymes to enable active digestion of complex carbohydrates. The microbiomes of the fore- and hindgut differed significantly in composition and abundance. Although the expression of microbial gene functions for fiber digestion were higher in the foregut than in the hindgut, our microbiome analysis in conjunction with that for morphology, enzyme activity and fiber-protein digestion, suggests complementary fiber and protein metabolism in both gut regions. Conclusions: Our results support that both the GSM fore- and hindgut facilitate fiber digestion, with an enlarged colon consistent as an adaptation to accommodate high throughput of fiber-rich food during winter.
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To consider holobionts with their hologenomes as levels of selection in evolution, there must be a continuity of partnerships between holobiont throughout generations. Microbiotas are transmitted from parent to offspring by a variety of methods, including cytoplasmic inheritance, via eggs and seeds, coprophagy (consumption of feces), close contact during and after birth, via insect vectors, and via the environment. Vertical transmission is defined as the movement of microbiota from parent to offspring without mixing with microbes in the environment. In humans, colonization of the newborn gut occurs initially via inoculation with maternal vaginal and fecal microbes when the baby transits the birth channel (vertical transmission). Breastfeeding provides an additional route of maternal vertical microbial transmission. Individuals can acquire and transfer symbionts throughout their lives, and not just during their reproductive phase. Using animal systems, including humans, it has been shown that a large fraction of bacterial species and specific strains in the microbiome are transmitted to offspring over short and long periods. It has been suggested that transmission of mutualistic symbionts and group living (animal sociality) coevolved. The large varieties in modes of transmission have an interesting implication: The fidelity of transmission of the microbiome lends a strong basis for each holobiont to be a unique biological entity, largely maintaining the uniqueness of the entity and conserving the species, from one generation to the next.
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In people, fecal microbiota transplantation is recognized as the best treatment modality for recurrent Clostridioides difficile infection in people, and its value is currently investigated in the treatment of other diseases associated with an abnormal gut microbiome. In dogs, intestinal dysbiosis has been documented in many acute and chronic digestive diseases as well as in diseases of other organ systems. There are only few published studies evaluating the benefits of fecal microbiota transplantation (FMT) in canine gastrointestinal disorders. They provide evidence that FMT may be beneficial in the treatment of acute intestinal diseases and hope that the technique might also be useful for the management of chronic enteropathies.
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Diversion colitis (DC) is a frequent clinical condition occurring in patients with bowel segments excluded from the fecal stream as a result of a diverting enterostomy. The etiology of this disease remains ill-defined but appears to differ from that of classical inflammatory bowel diseases such as Crohn's disease and ulcerative colitis. Research aimed to decipher the pathophysiological mechanisms leading to the development of this disease has been severely hampered by the lack of an appropriate murine model. This protocol generates a murine model of DC that facilitates the study of the immune system's role and its interaction with the microbiome in the development of DC. In this model using C57BL/6 animals, distal parts of the colon are excluded from the fecal stream by creating a distal colostomy, triggering the development of mild to moderate inflammation in the excluded bowel segments and reproducing the hallmark lesions of human DC with a moderate systemic inflammatory response. In contrast to the rat model, a large number of genetically-modified murine models on the C57BL/6 background are available. The combination of these animals with our model allows the potential roles of individual cytokines, chemokines, or receptors of bioactive molecules (e.g., interleukin (IL)-17; IL-10, chemokine CXCL13, chemokine receptors CXCR5 and CCR7, and the sphingosine-1-phosphate receptor 4) to be assessed in the pathogenesis of DC. The availability of congenic mouse strains on the C57BL/6 background largely facilitates transfer experiments to establish the roles of distinct cell types involved in the etiology of DC. Finally, the model offers the opportunity to assess the influences of local interventions (e.g., modification of the local microbiome or local anti-inflammatory therapy) on mucosal immunity in affected and non-affected bowel segments and the on systemic immune homeostasis.
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