Abstract
Although all hystricomorph rodents have the colonic furrow or groove that is the anatomical prerequisite for a ‘mucous trap’ colonic separation mechanism linked to coprophagy or cecotrophy, the taxon that gives this group its name, the porcupines, have been claimed to not practice coprophagy. Absence of coprophagy has repeatedly been claimed for hystricomorph species in which it was later confirmed. Here, we report the observation of a characteristic posture—sitting on one hindleg, with the other hindleg lifted and the snout covering the anogenital region—that is the typical posture during coprophagy in other large hystricomorph rodents, in two zoo-managed Indian crested porcupines (Hystrix indica). Together with other circumstantial evidence, these observations are suggestive of coprophagy in porcupines, and support claims that it may be wise to assume all hystricomorph rodents can use this strategy.
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The hystricomorph rodents are characterized by a groove in their proximal colon (Gorgas 1967; Langer 2017) that is an integral part of a so-called ‘colonic separation mechanism’ (Björnhag and Snipes 1999). Its major function is to trap microbes from the colonic digesta and transport them backwards into the caecum (Takahashi and Sakaguchi 2000). Hence, the regular, so-called ‘hard’ faeces are somewhat depleted of microbial material (Takahashi and Sakaguchi 1998). In the caecum, the microbes are collected and form a major part of the so-called ‘soft’ faeces that are re-ingested in the act of ‘coprophagy’ or ‘caecotrophy’.
Ingestion takes place directly as the soft faeces exit the anus, so that the behaviour might be interpreted as auto-grooming or cleaning. In some species, the typical posture is a sagittal bending of the body, while squatting on both hindlegs, so that the snout reaches the anus—as depicted for nutrias (Myocastor coypus) (Gosling 1979) or viscachas (Lagostomus maximus) (Hagen et al. 2015). In larger species, the typical posture is sitting on one hindleg, while the other is slightly lifted and the body bends back sideways, with the snout reaching towards the anus underneath the lifter leg—as depicted for capybaras (Hydrochoerus hydrochaeris) (Mendes and Nogueira-Filho 2013) or pacas (Cuniculus paca) (Guerra Aldrigui et al. 2018a).
It has been suggested that all hystricomorph rodents should be considered coprophagic based on the ubiquitous presence of the colonic groove (Clauss et al. 2007). Apart from the species mentioned above, coprophagy has been demonstrated in many other hystricomorph rodent species: in the guinea pig (Cavia porcellus) and the chinchilla (Chinchilla laniger) (Holtenius and Björnhag 1985), the greater cane rat (Thryonomys swinderianus) (Holzer et al. 1986), the punare (Thrichomys apereoides) (Roberts et al. 1988), the naked mole rat (Heterocephalus glaber) (Sherman et al. 1992), the degu (Octodon degus) (Kenagy et al. 1999), the dassie rat (Pteromus typicus) (Mess and Ade 2005), the tuco-tucos (Ctenomys pearsoni, C. talarium) (Martino et al. 2007), the agouti (Dasyprocta leporina) (Brown-Uddenberg 2008), the cavy (Microcavia australis) (Sassi et al. 2010), the hutia (Capromys pilorides) (Valdés and Álvarez 2015), or the mara (Dolichotis patagonum) (Clauss et al. 2019).
However, for the taxon that gives the hystricomorph rodents their name—the porcupines—it has been claimed vigorously that they do not practice coprophagy (Johnson and McBee 1967; van Jaarsveld and Knight-Eloff 1984; Björnhag 1987; Vispo and Hume 1995; Giné et al. 2020). This assumption is so firmly anchored in the concept of porcupine function that even when in a study of Felicetti et al. (2000) on digesta passage in Erethizon dorsatum, markers showed secondary excretion peaks, this was not interpreted as a reflection of coprophagy. To our knowledge, only a personal communication cited in Dyer (1998) mentions that North American porcupines may practice coprophagy regularly. Hagen et al. (2019) reported passage marker excretion patterns in Hystrix indica that were suggestive of coprophagy, but not as distinct as similar peaks reported in viscachas (Clauss et al. 2007), guinea pigs (Franz et al. 2011), chinchillas (Hagen et al. 2016), pacas (Guerra Aldrigui et al. 2018b) or maras (Clauss et al. 2019). Hence, whether porcupines practice coprophagy might still be considered unresolved.
Coprophagy is a behavioural and digestive strategy intuitively shunned by humans (Karasov and Martínez del Rio 2007). The history of an initial denial of coprophagy in a hystricomorph species followed by a gradual admission and finally acceptance can be traced in nutria (Kirner 1931; Otto 1954; Gosling 1979; Takahashi and Sakaguchi 1998, 2000), paca (Kraus et al. 1970; Matamoros 1982; Pérez 1992; Sabatini and Paranhos De Costa 2001; Guerra Aldrigui et al. 2018a), or capybara (Mendes et al. 2000; Hirakawa 2001, 2002). And although coprophagy had been described repeatedly in guinea pigs (Harder 1950; Hintz 1969; Björnhag and Sjöblom 1977; Hörnicke and Björnhag 1980; Holtenius and Björnhag 1985), Prieur and Froseth (1986) specifically selected the guinea pig as a species ‘in which cecotrophy does not occur’ for an experiment. Hence, science history seems to advise treating the claim that a hystricomorph rodent does not practice coprophagy with caution.
Based on the presence of a colonic groove in porcupines as well as the passage marker excretion patterns mentioned above, we hypothesized that these animals should practice coprophagy. Consequently, we predicted that a behaviour in the typical sideway posture as reported for pacas or capybaras (Fig. 1) should be observable in this group. In order to test whether corresponding visual observations could be made, we applied video surveillance to a pair of zoo-managed Hystrix indica.
A female and a male adult Indian crested porcupine (Hystrix indica) were observed over a period of 7 weeks by using video recording in their enclosure in the Zoo Cleves, Germany. The enclosure is 50 m2 in size (14 × 3.6 m) and consists of a larger open area and a sheltered place (2.3 × 1.3 m) filled with straw, which the animals use as a retreat and for sleeping. Due to the enclosure’s structure, it was not possible to record the entire area with the single video camera available. Therefore, initially, the larger outside area was surveyed from 27 April 2023–30 May2023 (except 29 April 2023–08 May 2023). Following this period, we suspected that the behaviour might occur more reliably in the retreat shelter, which was then surveilled from 30 May 2023–25 June 2023. Recordings were made with a Reolink Argus Eco 1080P (Reolink, Hong Kong, People’s Republic of China), which was triggered by motion for 40 s of video recording. This resulted in a total of 4626 video sequences, of which approximately 10% were not triggered by the porcupines but by insects or birds.
Due to the logistical options available at this zoo, no 24 h activity budget, and no budget of a certain continuous shorter observation period, could be reconstructed reliably from the video recordings. Therefore, this report only provides a qualitative description of the observed behaviour.
Porcupines were observed to clean or groom themselves on 26 video clips. Grooming of the hind part of the body was frequent, and consisted of manipulation of the quills with the mouth. During this behaviour, the hindleg was not lifted (Fig. 2).
In contrast, a behaviour in which the animals put their snout under the lifted hindleg, while squatting on the other hindleg, was observed in 13 video clips (Fig. 3; for videos, see the Supplementary material); 11 of these events took place in the shelter. Additionally, postures suggestive of the behaviour, yet without clear view of the hindleg and hence without definite confirmation, were observed on 26 videos (of which 24 were recorded in the shelter).
Our observations confirm the occurrence of a behaviour that is exactly as one would expect a porcupine to perform coprophagy. Together with the circumstantial evidence mentioned in the Introduction, this adds an important argument to the case that the porcupine digestive strategy includes coprophagy.
There are several reasons why coprophagic behaviour might have gone unnoticed in porcupines so far. The extensive auto-grooming behaviour of the animals might make a classification of coprophagic behaviour as ‘cleaning’ behaviour likely, as for example in a study on the den behaviour of beavers (Mott et al. 2011; cf. Table 1 of that study) that did not account for the coprophagy reported in this species (Richard 1959). Therefore, we recommend that the combination of a lifted hindleg and the absence of more scratching mouth movements may be particularly indicative of porcupine coprophagy.
Additionally, it must be noted that coprophagy is not as fixed and obligatory a pattern as rumination in camelids and ruminants is; rather, it can vary depending on the diet provided (Fekete and Bokori 1985; Carabaño et al. 1988; Martino et al. 2007; Nogueira-Filho et al. 2013; Meredith and Prebble 2017; Guerra Aldrigui et al. 2018a). The natural diet of porcupines of the Hystrix genus can vary considerably and has been described as herbivorous (Hafeez et al. 2011; Khan et al. 2021), with a minor animal component (Akram et al. 2017; Mori et al. 2021). In particular, scavenging has been observed in this genus (Duthie and Skinner 1986; Coppola et al. 2020). In some zoos, their diet may contain bones or antlers, boiled beef or day chicks, dog food, or eggs, whereas in other zoos, they may receive only plant-based diets (M. Polotzek, pers. obs.). Especially, when fed a more omnivorous diet, coprophagic behaviour may be reduced or not even occur at all.
Because our observations were made on zoo animals, the question may arise whether coprophagic behaviour should be considered a welfare indicator. In particular for porcupines, few studies exist that report husbandry-related details. Porcupines can be target-trained (Fernandez and Dorey 2021) but do not cooperate in a classic cooperation task (Truax et al. 2022). Using a controlled feeding by visitors can make these animals, that are often poorly visible due to their nocturnal habits, very attractive display animals (Hammer and Hammer 2016). But to our knowledge, no assessment of their welfare in zoos has been performed. To what extent practicing coprophagy should be considered as contributing to zoo animal welfare can only be decided indirectly. In rabbits, feeding diets without hay that reduce coprophagy have been associated with gastrointestinal stasis (lack of peristalsis) (Meredith and Prebble 2017), yet the effect cannot be ascribed to lacking coprophagy but to a lack of structural dietary fibre that stimulates the gut. The forceful prevention of coprophagy has been reported to cause growth and health problems linked to vitamin deficiency (Barnes 1962), and the measures necessary for this prevention—making the access to the anus and any deposited soft faeces impossible, typically by a combination of a collar, or a ‘straight jacket’, or a cup around the anus and a meshed floor, or by keeping animals in cages so small that they cannot turn around (Armstrong and Softly 1966; Sukemori et al. 2000)—evidently represent welfare impairments. However, to our knowledge, neither have problems related to a lack of gut peristalsis ever been reported in porcupines, nor have direct welfare impairments linked to a reduction in coprophagy because of specific diets ever been implied in any species. Indirectly, however, diets that lead to a reduction in coprophagy in animals that may use this strategy are typically high in energy and protein and low in fibre (Meredith and Prebble 2017), and therefore, typically lead to obesity (Prebble et al. 2015b), and to less time spent foraging (Prebble et al. 2015a) (and consequently more time spent in inactivity or undesired behaviours). In two zoo-managed prehensile-tailed porcupines (Coendou prehensilis), the provision of a fibre-rich diet item led to an increase in the daily foraging time and a decrease in inactivity (Dunham et al. 2023). Rather than considering observations of coprophagy an important management tool, the issue of nutritional and behavioural management is more easily monitored via diet composition and overall body condition and activity budgets.
The present study does not conclusively prove coprophagy in porcupines. When describing the digestive physiology of porcupines, a cautionary approach that at least includes the possibility of coprophagy appears advisable. For final proof, more elaborate and invasive approaches would be required, such as the killing of an animal immediately at the beginning or after the corresponding observation (and investigation of the colon or stomach contents), or the combination of a passage study together with uninterrupted video observation to link secondary marker excretion peaks to images suggestive of re-ingestion of faeces (Guerra Aldrigui et al. 2018b). For future studies, we recommend the latter approach.
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We thank the staff of Zoo Cleves for their help and patience.
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Polotzek, M., Schirmer, J., Schindler, J. et al. Behaviour indicative of coprophagy in zoo-managed porcupine (Hystrix indica). Mamm Biol 103, 633–638 (2023). https://doi.org/10.1007/s42991-023-00376-1
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DOI: https://doi.org/10.1007/s42991-023-00376-1