The gut microbiota may have a vital role in obesity development (Backhed et al., 2004; Collins et al., 2013; Le Chatelier et al., 2013; Zhao, 2013). For example, endotoxin produced by an opportunistic pathogen in the gut, such as Escherichia coli, induced obesity and insulin resistance when a purified form was subcutaneously infused into mice (Cani et al., 2007a). A greater abundance of opportunistic pathogens, such as Betaproteobacteria, was found in the gut of diabetic patients compared with healthy controls (Larsen et al., 2010). A more recent comparative metagenomic analysis of the fecal samples of 171 diabetic patients and 174 healthy controls showed that diseased samples had lesser abundance of butyrate-producing bacteria, such as Faecalibacterium prausnitzii, but greater abundance of opportunistic pathogens, including Clostridium bolteae and Desulfovibrio sp. (Qin et al., 2012). Another study found that the early onset of high-fat-diet-induced T2D was characterized by an increased bacterial translocation from the intestine towards tissues (Amar et al., 2011). An opportunistic pathogen, Enterobacter cloacae B29, isolated from the gut of a morbidly obese and diabetic patient, induced obesity and insulin resistance in germ-free mice (Fei and Zhao, 2013). Taken together, these studies indicate that a dysbiotic gut microbiota may causatively contribute to obesity and diabetes development, and thus may serve as a potential new target for disease control.
A majority of studies on mole-rat polyethism have been performed with animals housed in terrariums or artificial burrow systems. These animals are typically fed ad libitum, have no access to compact soil for digging and extending the burrow system, do not face predation and have no dispersal opportunities. Thus, these laboratory conditions fail to simulate the costs and benefits of different behaviours associated with the natural environment. Consequently, laboratory-based findings obtained in captive mole-rat family groups should necessarily be viewed with caution unless they are supplemented and confronted with findings obtained from free-living animals. In the wild, eusocial mole-rats live permanently in large burrow systems sealed off from the surface and consisting of up to three km of branched and reticulated tunnels extending over an area which can exceed 1 ha20,21,22. The burrow systems usually have long-lasting communal nests and axial tunnels providing access to areas where they branch into shallower foraging tunnels22,23,24. In some mole-rat species, the burrow systems of neighbouring groups can be interconnected by open or partially blocked tunnels, thus forming vast communication networks22,25.
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Differences in the proportions of radio-fixes inside the nest and within defined distance ranges from the nest could also reflect task allocation. Task allocation has rarely been described in non-human mammals (e.g.33) except for captive African mole-rats13,15,16. We can assume that in free-ranging radio-tracked mole-rats a high proportion of radio-fixes close to the nest indicates guarding of the nest area. On the contrary, large proportion of time spent away from the nest would likely involve digging and gathering food. Larger individuals are usually better suited for guarding and protecting (against intruders or predators such as snakes) than smaller animals, therefore we might expect the largest of the radio-tracked mole-rats to mostly remain close to the nest to guard/protect the nest or breeding female. Nevertheless, there is also a possibility that instead of this they would patrol peripheral parts of the burrow system/territory (cf. ref. 20). In our study breeding males and other large individuals of either sex tended to spend relatively more time close to the nest (Table 2; Fig. 1), which is in agreement with the first of the two options. However, it should be noted that the relatively larger proportion of radio-fixes close to the nest, together with the generally low outside-nest activity of large individuals could be mainly due to their lower incentive to work rather than their active protection of the nest area. Breeding females were no less active than similar-sized non-breeders, but they were also relatively often located close to the nest, which fits with their biological role.
The amount of activity performed by individuals of a captive mole-rat family group usually varies. Breeders and larger non-breeders usually perform less activity than smaller non-breeders (e.g. [11], [12]), but several exceptions were reported (e.g. [13], [14]). To better understand this phenomenon, more data are necessary from free-living mole-rat family groups.
A convincing method to reveal differences between individuals' activity patterns within an animal group in the field is radio-telemetry. In free-living social bathyergids, this method was used so far only twice. Lovegrove [10] radio-tracked five individuals of F. damarensis. These animals spent only 24% of their time outside the nest and their daily activity patterns were irregular, with on average six short bouts of activity per day and no conspicuous differences between the individuals. The second radio-telemetry study was carried out on Heterocephalus glaber but it brought no data on individuals' activity patterns [15].
Mole-rats were captured at two trapping sites 250 m apart (in burrow systems of two different family groups) using the Hickman live-traps set into tunnels uncovered near fresh mole-hills. One adult female (F202, weighing 220 g) was captured at site 1. Since the efficiency of the traps was low, at site 2 we combined the traps with a partial excavation of deep tunnels around an accidentally found nest. Here, we captured a family of 11 individuals: eight females (33, 90, 106, 108, 166, 192, 207 and 208 g) and three males (221, 231 and 454 g). The largest male had massive head muscularity, pigmented corners of the mouth and a conspicuously large penis and testes. All other family members displayed conspicuously submissive behaviour towards him. We therefore suppose that he was the breeding male of the family. No breeding female (female with enlarged teats and perforate vagina) was captured. All males and 2 females (192 g and 207 g) from site 2 and the female from site 1 were shortly anesthetized by ketamine and xylazine and fitted with radio-collars (Brass collar, Pip transmitter with a position-based activity indicator; Biotrack Ltd, Dorset, UK). The weight of the radio-collars was less than 5% of the body mass of the smallest radio-tracked animal under study. The activity indicator changed the signal rate of the transmitter when the collar departed from a vertical position (e.g. when the animal lowered its head to a curled-up position, as when sleeping), which was used to identify the body position of the animals encountered inside the nest. All animals were released into burrows at their capture sites within 72 hours after their capture. Radio-tracking started 20 days after the release of the last animals. At this time the animals of site 2 already used a communal nest newly built at the same place where the original one had been destroyed, and it was detected that they freely move across the previously damaged area by re-established tunnel connections. Female 202 left site 1 shortly (between 7 and 14 days) after release and before the radio-tracking started (which was 43 days after her release) she established a new home-range 180 m away. We therefore consider her a dispersing individual.
Although the biology of African mole-rats is of a great interest to scientists and even to the general public for a long time, efforts to study these animals under natural conditions lag behind. Our study is the first to use radio-telemetry in a study of social mole-rats in more than 20 years. Although the sample size is limited to only six individuals, the study brings several remarkable findings. We proved that temporal and spatial activity pattern differ sharply between a breeding male and non-breeders of the same free-living family group. Unique findings are also those concerning the dispersing female. Since she most likely lived solitarily during the whole period of the study, we obtained a rare chance to describe an activity pattern in a social species which is not actually affected by social interactions, but is still performed under natural conditions.
We found that non-breeding family members of F. mechowii spent only 24% of their time outside the nest. This is the same value as found in F. damarensis [10]. On the contrary, the free-living solitary Heliophobius argenteocinereus spent as much as 37% of time outside the nest [4]. Considering a principle that the cooperative foraging reduces the risk of starvation [28] the difference is not surprising. The mentioned principle can be interpreted as that under the same conditions the solitary mole-rat must devote larger amount of time to search for food to achieve the same low risk of starvation as a member of a family group.
We observed conspicuous differences in the amount of activity between individuals within the radio-tracked family. The breeding male and the smallest non-breeder radio-tracked (the female F234) stood out from the family, being the least and the most active individuals, respectively (which also corresponds with the smallest and the largest individual HR). Analogous laboratory data on differences in activity between particular members of captive mole-rat families are equivocal. In many studies the least active (or the least working) individuals were breeders (e.g. [12], [29], [30]). On the contrary, no differences in the amount of activity between breeders and non-breeders were found in captive F. anselli [14], [31]. In Cryptomys hottentotus the breeders were even the most active individuals in a family group [32]. A similar disagreement is characteristic for the relation between relative body mass and the performed activity in non-breeders. Smaller non-breeders usually perform more work (or activity in general) than the larger non-breeders [11], [12], [30], [33] but the opposite was observed in one study on F. damarensis [13]. Recently, some light has been shed to this problematic by Scantlebury et al. [34] who investigated daily energy expenditure (DEE) in free-living F. damarensis using doubly labelled water (DLW) technique. They found that larger individuals, including breeders, have lower DEE than smaller non-breeders, which is in concordance with our results as well as with the results of most laboratory studies. However, the difference disappeared in the wet season. The breeders and larger non-breeders are thus probably able to mobilize their workforce under some circumstances, for example, when the soil is softened by rains to ease burrowing. 2ff7e9595c
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