Physiology and Behaviour of African Mole-Rats

A special issue of Animals (ISSN 2076-2615). This special issue belongs to the section "Mammals".

Deadline for manuscript submissions: closed (31 December 2023) | Viewed by 19885

Special Issue Editor


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Guest Editor
Natural and Agricultural Sciences, University of Pretoria, Pretoria, South Africa
Interests: mole-rats; rodents; physiology; seasonality; chronobiology; mammals; neuroanatomy; immunocytochemistry; behaviour; reproduction

Special Issue Information

Dear Colleagues,

African mole-rats are fascinating in almost every aspect of their biology. More than 30 species of bathyergid mole-rats are endemic to Africa, and all these species are subterranean. Although the subterranean niche provides protection against predators and environmental extremes, it also imposes rather harsh constraints on the sensory, thermoregulatory and energetic capacities of its inhabitants. Mole-rats are extremely well-adapted to their habitat, displaying many morphological, physiological and behavioural adaptations. Sensory adaptations include a mosaic of progressive and regressive features to compensate for the lightless environment, while low body temperatures and behavioural adjustments counter thermoregulatory and energetic constraints. African mole-rats have very diverse and interesting social and reproductive organisations, the mechanisms of which have not yet been fully elucidated. Furthermore, in recent years, mole-rats, and in particular naked mole-rats, have become popular models for biomedical research, such as hypoxia, pain insensitivity, ageing and cancer resistance.

The numerous remarkable features of African mole-rat biology provide scope for diverse research themes. Therefore, this Special Issue will showcase the unique biology of African mole-rats with a collection of papers addressing their physiology and behaviour. You are invited to submit articles focusing on any aspect of African mole-rat physiology or behaviour.

Dr. Maria K. Oosthuizen
Guest Editor

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Keywords

  • Bathyergidae
  • African mole-rat
  • sociality
  • thermoregulation
  • sensory
  • subterranean
  • rodent
  • physiology
  • behaviour

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Published Papers (7 papers)

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Research

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12 pages, 1129 KiB  
Article
Non-Invasive Quantification of Faecal and Urine Reproductive Hormone Metabolites in the Naked Mole-Rat (Heterocephalus glaber)
by Tshepiso Lesedi Majelantle, Andre Ganswindt, Stefanie Birgit Ganswindt, Nicole Hagenah, Daniel William Hart and Nigel Charles Bennett
Animals 2023, 13(19), 3039; https://doi.org/10.3390/ani13193039 - 27 Sep 2023
Cited by 1 | Viewed by 1181
Abstract
The naked mole-rat (Heterocephalus glaber) occurs in colonies with a distinct dominance hierarchy, including one dominant, breeding female (the queen), 1–3 breeding males, and non-reproductive subordinates of both sexes that are reproductively suppressed while in the colony. To non-invasively evaluate reproductive [...] Read more.
The naked mole-rat (Heterocephalus glaber) occurs in colonies with a distinct dominance hierarchy, including one dominant, breeding female (the queen), 1–3 breeding males, and non-reproductive subordinates of both sexes that are reproductively suppressed while in the colony. To non-invasively evaluate reproductive capacity in the species, we first had to examine the suitability of enzyme immunoassays (EIAs) for determining progestogen and androgen metabolite concentrations in the naked mole-rat, using urine and faeces. A saline control and gonadotrophin-releasing hormone (GnRH) were administered to twelve (six males and six females) naked mole-rats which were previously identified as dispersers and housed singly. The results revealed that urine is possibly not an ideal matrix for progestogen and androgen metabolite quantification in naked mole-rats as no signal was detected in the matrix post GnRH administration. A 5α-Progesterone EIA and an Epiandrosterone EIA were identified as suitable for quantifying faecal progesterone metabolites (fPMs) and faecal androgen metabolites (fAMs) in males and females, respectively. The results suggest that there are individual variations in baseline fPM and fAM concentrations, and only two out of six females and no males exhibited an increase in fPM concentrations greater than 100% (−20% SD) post GnRH administration. Conversely, only four out of six females and three out of six males had an increase in fAM concentrations greater than 100% (−20% SD) following GnRH administration. These results imply that some naked mole-rat individuals have a reduced reproductive capacity even when they are separated from the queen. Full article
(This article belongs to the Special Issue Physiology and Behaviour of African Mole-Rats)
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15 pages, 1393 KiB  
Article
Pup Recruitment in a Eusocial Mammal—Which Factors Influence Early Pup Survival in Naked Mole-Rats?
by Michaela Wetzel, Alexandre Courtiol, Heribert Hofer, Susanne Holtze and Thomas B. Hildebrandt
Animals 2023, 13(4), 630; https://doi.org/10.3390/ani13040630 - 11 Feb 2023
Viewed by 2397
Abstract
In eusocial insects, offspring survival strongly depends on the quality and quantity of non-breeders. In contrast, the influence of social factors on offspring survival is more variable in cooperatively breeding mammals since maternal traits also play an important role. This difference between cooperative [...] Read more.
In eusocial insects, offspring survival strongly depends on the quality and quantity of non-breeders. In contrast, the influence of social factors on offspring survival is more variable in cooperatively breeding mammals since maternal traits also play an important role. This difference between cooperative insects and mammals is generally attributed to the difference in the level of sociality. Examining offspring survival in eusocial mammals should, therefore, clarify to what extent social organization and taxonomic differences determine the relative contribution of non-breeders and maternal effects to offspring survival. Here, we present the first in-depth and long-term study on the influence of individual, maternal, social and environmental characteristics on early offspring survival in a eusocial breeding mammal, the naked mole-rat (Heterocephalus glaber). Similarly to other mammals, pup birth mass and maternal characteristics such as body mass and the number of mammae significantly affected early pup survival. In this eusocial species, the number of non-breeders had a significant influence on early pup survival, but this influence was negative—potentially an artifact of captivity. By contrasting our findings with known determinants of survival in eusocial insects we contribute to a better understanding of the origin and maintenance of eusociality in mammals. Full article
(This article belongs to the Special Issue Physiology and Behaviour of African Mole-Rats)
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15 pages, 2389 KiB  
Article
Laterality in the Damaraland Mole-Rat: Insights from a Eusocial Mammal
by Paul J. Jacobs and Maria K. Oosthuizen
Animals 2023, 13(4), 627; https://doi.org/10.3390/ani13040627 - 10 Feb 2023
Cited by 3 | Viewed by 2026
Abstract
Lateralization is the functional control of certain behaviors in the brain being processed by either the left or right hemisphere. Behavioral asymmetries can occur at an individual and population level, although population-level lateralization is less common amongst solitary species, whereas social species can [...] Read more.
Lateralization is the functional control of certain behaviors in the brain being processed by either the left or right hemisphere. Behavioral asymmetries can occur at an individual and population level, although population-level lateralization is less common amongst solitary species, whereas social species can benefit more from aligning and coordinating their activities. We assessed laterality (individual and population) through turning biases in the eusocial Damaraland mole rat, Fukomys damarensis. We considered factors such as breeding status (queen or subordinate), environment (wild-caught or captive), sex (male or female), colony and body mass. All individuals together demonstrated significant left-turning biases, which was also significant at the population level. Wild-caught animals were more strongly lateralized, had a wider spread over a laterality index and lacked the population-level left-turning bias as compared to captive mole rats. Subordinate animals were more lateralized than queens, demonstrating social status differences in turning biases for social mole rats. This emphasizes the importance of animal handling and context when measuring and interpreting behavioral asymmetries. Full article
(This article belongs to the Special Issue Physiology and Behaviour of African Mole-Rats)
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13 pages, 1242 KiB  
Article
Social Isolation Does Not Alter Exploratory Behaviour, Spatial Learning and Memory in Captive Damaraland Mole-Rats (Fukomys damarensis)
by Arantxa Silvia Blecher and Maria Kathleen Oosthuizen
Animals 2023, 13(3), 543; https://doi.org/10.3390/ani13030543 - 3 Feb 2023
Viewed by 1821
Abstract
Exploratory behaviour, spatial learning and memory affect the survival of animals and appear to be dependent on the specific habitat that a species occupies. Good spatial navigation and memory are particularly important for subterranean animals, as it is energetically expensive to inhabit this [...] Read more.
Exploratory behaviour, spatial learning and memory affect the survival of animals and appear to be dependent on the specific habitat that a species occupies. Good spatial navigation and memory are particularly important for subterranean animals, as it is energetically expensive to inhabit this niche. Damaraland mole-rats are subterranean mammals that live in colonies with organised social structures. Damaraland mole-rats have been maintained in the laboratory for many years and can be housed in groups or individually. We evaluated the effect of social isolation on the exploratory behaviour and spatial memory of single-housed and colony-housed animals and also considered potential differences in animals with different social statuses. We predicted that solitary housing would increase anxiety-like behaviour and result in higher activity and more errors when solving a maze. Exploration by colony- and single-housed mole-rats was tested in an open-field test, where all individuals explored readily. Single-housed queens and non-breeding females showed increased activity and spent more time in tunnels, which can be explained by increased anxiety. In the Y-maze, improvements in solving the maze were observed in all experimental groups, except in single-housed non-breeding females. In addition, all males showed a decrease in the number of errors in the maze. Spatial learning is thus apparent but could not be conclusively proven. It was possibly underestimated, as magnetic cues that may be used by mole-rats as stimuli for navigation were removed in the experimental setup. Overall, it appears that social isolation has a limited effect on the exploratory behaviour and spatial learning of Damaraland mole-rats. Full article
(This article belongs to the Special Issue Physiology and Behaviour of African Mole-Rats)
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15 pages, 2701 KiB  
Article
Aggression, Boldness, and Exploration Personality Traits in the Subterranean Naked Mole-Rat (Heterocephalus glaber) Disperser Morphs
by Tshepiso Lesedi Majelantle, Andre Ganswindt, Christian Walter Werner Pirk, Nigel Charles Bennett and Daniel William Hart
Animals 2022, 12(22), 3083; https://doi.org/10.3390/ani12223083 - 9 Nov 2022
Cited by 4 | Viewed by 2668
Abstract
Animal personality traits (consistent behavioral differences between individuals in their behavior across time and/or situation) affect individual fitness through facets, such as dispersal. In eusocial naked mole-rat (Heterocephalus glaber) colonies, a disperser morph may arise with distinct morphological, behavioral, and physiological [...] Read more.
Animal personality traits (consistent behavioral differences between individuals in their behavior across time and/or situation) affect individual fitness through facets, such as dispersal. In eusocial naked mole-rat (Heterocephalus glaber) colonies, a disperser morph may arise with distinct morphological, behavioral, and physiological characteristics. This study aimed to quantify the personality traits of a cohort of disperser morphs of naked mole-rat (NMR). Behavioral tests were performed on twelve disperser morphs (six males and six females) in an observation tunnel system that was novel and unfamiliar. Novel stimuli (fresh snakeskin, tissue paper, and conspecific of the same sex) were introduced for fifteen minutes, and the behavioral acts of the individual were recorded. A total of 30 behaviors were noted during the behavioral tests of which eight were used to quantify aggression, boldness, and exploration. The NMR disperser morphs showed consistent individual differences in boldness, and exploration across time and test, indicating a distinct personality. In addition, new naked mole-rat responses including disturbance behaviors; confront, barricade, and stay-away, were recorded. Further investigations into the relationships between animal personality traits and social hierarchy position in entire colonies are needed for more informative results as we further investigate the role of personality in cooperatively breeding societies. Full article
(This article belongs to the Special Issue Physiology and Behaviour of African Mole-Rats)
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Review

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20 pages, 9575 KiB  
Review
Naked Mole-Rats Demonstrate Profound Tolerance to Low Oxygen, High Carbon Dioxide, and Chemical Pain
by Vince G. Amoroso, Aishi Zhao, Isabel Vargas and Thomas J. Park
Animals 2023, 13(5), 819; https://doi.org/10.3390/ani13050819 - 24 Feb 2023
Cited by 2 | Viewed by 5857
Abstract
Naked mole-rats (Heterocephalus glaber) are very unusual among subterranean mammals in that they live in large colonies and are extremely social, spending large amounts of time gathered together in underground nests more than a meter below the surface. Many respiring individuals [...] Read more.
Naked mole-rats (Heterocephalus glaber) are very unusual among subterranean mammals in that they live in large colonies and are extremely social, spending large amounts of time gathered together in underground nests more than a meter below the surface. Many respiring individuals resting in deep, poorly ventilated nests deplete the oxygen supply and increase the concentration of carbon dioxide. Consistent with living in that atmosphere, naked mole-rats tolerate levels of low oxygen and high carbon dioxide that are deadly to most surface-dwelling mammals. Naked mole-rats appear to have evolved a number of remarkable adaptations to be able to thrive in this harsh atmosphere. In order to successfully survive low oxygen atmospheres, they conserve energy utilization by reducing the physiological activity of all organs, manifest by reduced heart rate and brain activity. Amazingly, they resort to the anaerobic metabolism of fructose rather than glucose as a fuel to generate energy when challenged by anoxia. Similarly, high carbon dioxide atmospheres normally cause tissue acidosis, while naked mole-rats have a genetic mutation preventing both acid-induced pain and pulmonary edema. Together, these putative adaptations and the tolerances they provide make the naked mole-rat an important model for studying a host of biomedical challenges. Full article
(This article belongs to the Special Issue Physiology and Behaviour of African Mole-Rats)
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12 pages, 269 KiB  
Review
Socially Induced Infertility in Naked and Damaraland Mole-Rats: A Tale of Two Mechanisms of Social Suppression
by Nigel C. Bennett, Christopher G. Faulkes and Cornelia Voigt
Animals 2022, 12(21), 3039; https://doi.org/10.3390/ani12213039 - 4 Nov 2022
Cited by 5 | Viewed by 2470
Abstract
The naked mole-rat (Heterocephalus glaber) and the Damaraland mole-rat (Fukomys damarensis) possess extreme reproductive skew with a single reproductive female responsible for reproduction. In this review, we synthesize advances made into African mole-rat reproductive patterns and physiology within the [...] Read more.
The naked mole-rat (Heterocephalus glaber) and the Damaraland mole-rat (Fukomys damarensis) possess extreme reproductive skew with a single reproductive female responsible for reproduction. In this review, we synthesize advances made into African mole-rat reproductive patterns and physiology within the context of the social control of reproduction. Non-reproductive female colony members have low concentrations of luteinising hormone (LH) and a reduced response of the pituitary to a challenge with gonadotropin releasing hormone (GnRH). If the reproductive female is removed from the colony, an increase in the basal plasma LH and increased pituitary response to a GnRH challenge arises in the non-reproductive females, suggesting the reproductive female controls reproduction. Non-reproductive male Damaraland mole-rats have basal LH concentrations and elevated LH concentrations in response to a GnRH challenge comparable to the breeding male, but in non-breeding male naked mole-rats, the basal LH concentrations are low and there is a muted response to a GnRH challenge. This renders these two species ideal models to investigate physiological, behavioural and neuroendocrine mechanisms regulating the hypothalamic-pituitary-gonadal axis. The recently discovered neuropeptides kisspeptin and RFamide-related peptide-3 are likely candidates to play an important role in the regulation of reproductive functions in the two mole-rat species. Full article
(This article belongs to the Special Issue Physiology and Behaviour of African Mole-Rats)
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