Postnatal ontogeny of limb proportions and functional indices in the subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae)

Burrow construction in the subterranean Ctenomys talarum (Rodentia: Ctenomyidae) primarily occurs by scratch‐digging. In this study, we compared the limbs of an ontogenetic series of C. talarum to identify variation in bony elements related to fossorial habits using a morphometrical and biomechanical approach. Diameters and functional lengths of long bones were measured and 10 functional indices were constructed. We found that limb proportions of C. talarum undergo significant changes throughout postnatal ontogeny, and no significant differences between sexes were observed. Five of six forelimb indices and two of four hindlimb indices showed differences between ages. According to discriminant analysis, the indices that contributed most to discrimination among age groups were robustness of the humerus and ulna, relative epicondylar width, crural and brachial indices, and index of fossorial ability (IFA). Particularly, pups could be differentiated from juveniles and adults by more robust humeri and ulnae, wider epicondyles, longer middle limb elements, and a proportionally shorter olecranon. Greater robustness indicated a possible compensation for lower bone stiffness while wider epicondyles may be associated to improved effective forces in those muscles that originate onto them, compensating the lower muscular development. The gradual increase in the IFA suggested a gradual enhancement in the scratch‐digging performance due to an improvement in the mechanical advantage of forearm extensors. Middle limb indices were higher in pups than in juveniles–adults, reflecting relatively more gracile limbs in their middle segments, which is in accordance with their incipient fossorial ability. In sum, our results show that in C. talarum some scratch‐digging adaptations are already present during early postnatal ontogeny, which suggests that they are prenatally shaped, and other traits develop progressively. The role of early digging behavior as a factor influencing on morphology development is discussed. J. Morphol. 275:902–913, 2014. © 2014 Wiley Periodicals, Inc.     

Home-Range Dynamics in a Solitary Subterranean Rodent

Despite an important role of subterranean rodents as ecosystem engineers, their belowground mobility is poorly documented. It is supposed that their underground burrow systems, once established, are relatively stable because of high-energy costs of digging. We chose the silvery mole-rat, Heliophobius argenteocinereus (Bathyergidae, Rodentia) from mesic Afrotropics as a representative of solitary subterranean rodents to investigate how, and how fast these rodents process their established burrow systems. We combined radio-tracking of individual animals with subsequent mapping of their burrow systems, and we developed a new method for assessing the rate of burrowing. Mole-rats continuously rebuilt their burrow systems; they excavated approx. 0.7 m of new tunnels per day and backfilled on average 64% of all tunnels. On average, every 32 d they established a new nest. They often completely backfilled newly excavated peripheral burrows, while other parts of their burrow systems were more permanent. Their home-ranges were dynamic and continuously shifted in space. Burrow system processing continued even in the advanced dry season, when soil is difficult to work.     

Stereotypies resulting from a deviation in the ontogenetic development of gerbils

As a reaction to intensive housing conditions, Mongolian gerbils (Meriones unguiculatus) regularly develop stereotypic digging in early ontogeny. To determine how the development of stereotypic digging deviates from the development of digging in a natural setting, the development of digging in laboratory cages and an artifical burrow were compared. In the burrow treatment, young gerbils were raised inside the burrow and left it for the first time at a mean age of 21 days. They showed a strong tendency to retreat into the burrow and spent 91.6% of the time in it. Their digging consisted of short, non-stereotypic digging bouts. In contrast, digging of the young gerbils in the laboratory cages became increasingly longer and consisted of long-lasting, stereotypic digging bouts along with short, non-stereotypic bouts. This development deviated from the development in the burrow significantly from day 24. Stereotypic digging was interpreted as an intensification of digging due to a lack of retreating structures in the laboratory cages. Stereotypic digging was considered as an abnormal behavior because it failed to regulate retreating behavior.     

First trace and body fossil evidence of a burrowing, denning dinosaur

A fossil discovery in the mid-Cretaceous Blackleaf Formation of southwest Montana, USA, has yielded the first trace and body fossil evidence of burrowing behaviour in a dinosaur. Skeletal remains of an adult and two juveniles of Oryctodromeus cubicularis gen. et sp. nov. a new species of hypsilophodont-grade dinosaur, were found in the expanded distal chamber of a sediment-filled burrow. Correspondence between burrow and adult dimensions supports Oryctodromeus as the burrow maker. Additionally, Oryctodromeus exhibits features of the snout, shoulder girdle and pelvis consistent with digging habits while retaining cursorial hindlimb proportions. Association of adult and young within a terminal chamber provides definitive evidence of extensive parental care in the Dinosauria. As with modern vertebrate cursors that dig, burrowing in Oryctodromeus may have been an important adaptation for the rearing of young. Burrowing also represents a mechanism by which small dinosaurs may have exploited the extreme environments of polar latitudes, deserts and high mountain areas. The ability among dinosaurs to find or make shelter may contradict some scenarios of the Cretaceous-Paleogene impact event. Burrowing habits expand the known range of nonavian dinosaur behaviours and suggest that the cursorial ancestry of dinosaurs did not fully preclude the evolution of different functional regimes, such as fossoriality.     

Acoustic signals of a solitary subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae): physical characteristics and behavioural correlates

The purpose of this study was to analyse and describe vocalizations of a solitary subterranean rodent, Ctenomys talarum. In adult C. talarum five different sounds (four true vocalizations and one mechanical sound) were recorded during different behavioural contexts. Using data from the laboratory and literature, we classified these vocalizations as territorial, distress, and mating calls. We found that the vocalization range in C. talarum is shifted towards low frequencies, which transmit better in underground burrows and match well the hearing range described for other species of subterranean rodents. These low-frequency vocalizations, also found in other non-related subterranean rodents, may reflect an adaptation to the acoustic conditions of the habitat. Electronic Publication     

Burrowing behaviour in the crayfish, Cambarus diogenes diogenes girard

The crayfish, Cambarus diogenes diogenesGirard (1852), spends most of its life cycle in individually constructed underground burrows. The architectural behavioral patterns and sequences with which adult C. d. diogenes excavate an underground chamber were evaluated. Two motor patterns (Pushing and Carrying) and three burrow stages (shallow depression, angular pit, and burrow with two openings) were identified. During the development of burrowing behaviour in juveniles, a third motor pattern (Fanning) occurred. While the three motor patterns are functional soon after hatching, crayfish may learn to orient the Carrying motor pattern for the most efficient excavation of a stage-3 burrow with two openings. The ground-water level determined the final structure of a burrow.     

Is communal burrowing or burrow sharing a benefit of group living in the lesser cavy <Emphasis Type="Italic">Microcavia australis</Emphasis>?

Burrow systems play an important role in the life of rodents in arid environments. The objectives of this study were to examine the hypothesis that group living is beneficial to the semifossorial rodent, and determine whether Microcavia australis (Geoffroy and d’Orbigny, 1833) burrows communally and/or shares burrow systems. I related the structure of burrow systems to the number of cavies inhabiting them, in two habitats with different soil hardness and different plant cover (El Leoncito and Ñacuñán). El Leoncito has a harsh climate, with lower plant density and softer soil than Ñacñuán. A total of 18 burrow systems were characterized at Ñacuñán, and 12 at El Leoncito. Social groups at El Leoncito have a higher number of individuals than at Ñacuñán, but the structure of burrow systems in softer soil is narrower (small area size), with fewer holes, less slope and depth of galleries, and with no relationship between the number of holes and burrow area. Therefore, considering the development of the burrow system as an indicator of the cost of burrowing, I conclude that communal burrowing to reduce the energetic cost of burrowing per capita is not the primary cause of cavy sociality. M. australis were not active diggers, because digging behaviour was rarely recorded at either site. Burrow systems of cavies persisted over the years of study, occupied by the same cavies and new offspring, and digging new burrow systems and tunnels was a relatively rare event at both sites. Under the burrow-sharing hypothesis, sociality could prevail in M. australis that regularly dig to build and maintain a burrow system which they use for a long time.     

Energetics and thermoregulation during digging in the rodent tuco-tuco (Ctenomys talarum)

For subterranean rodents, searching for food by extension of the tunnel system and maintenance of body temperature are two of the most important factors affecting their life underground. In this study we assess the effect of ambient temperature on energetics and thermoregulation during digging in Ctenomys talarum. We measured V˙o₂ during digging and resting at ambient temperature (T_a) below, within, and above thermoneutrality. Digging metabolic rate was lowest at T_a within the thermoneutral zone and increased at both lower and higher temperatures, but body temperature (T_b) remained constant at all T_as. Below thermoneutrality, the cost of digging and thermoregulation are additive. Heat production for thermoregulation would be compensated by heat produced as a by-product of muscular activity during digging. Above thermoneutrality, conduction would be an important mechanism to maintain a constant T_b during digging.     

Digestive strategies in the South American subterranean rodent Ctenomys talarum

Ctenomys talarum is a subterranean herbivorous rodent which due to its particular life style is frequently exposed to variations in surface environmental conditions (i.e. food quality and availability, temperature). Thus, unlike other subterranean rodents, C. talarum has to buffer both the surface and burrow challenging environmental conditions. We studied the occurrence of digestive strategies at different levels of C. talarum living in their natural habitat. We determined the dimensions of different parts of the gastrointestinal tract and organs along as the activity of key digestive enzymes (disaccharidase, N-aminopeptidase) in different parts of the gut in individuals seasonally caught. The results show that C. talarum exhibits characteristics in the gut at the biochemical level (high disaccharidase activities in small intestine, high N-aminopeptidase activity in the caecum and large intestine, and a seasonal differential modulation of N-aminopeptidase activity in small and large intestines), which could represent adaptive strategies to face seasonal variations in key environmental factors.     

Mechanical similarity across ontogeny of digging muscles in an Australian marsupial (Isoodon fusciventer)

Many mammals dig, either during foraging to access subsurface food resources, or in creating burrows for shelter. Digging requires large forces produced by muscles and transmitted to the soil via the skeletal system; thus fossorial mammals tend to have characteristic modifications of the musculoskeletal system that reflect their digging ability. Bandicoots (Marsupialia: Peramelidae) scratch-dig mainly to source food, searching for subterranean food items including invertebrates, seeds, and fungi. They have musculoskeletal features for digging, including shortened, robust forelimb bones, large muscles, and enlarged muscle attachment areas. Here, we compared changes in the ontogenetic development of muscles associated with digging in the Quenda (Isoodon fusciventer). We measured muscle mass (m _m), pennation angle, and fiber length (FL) to calculate physiological cross-sectional area (PCSA; a proxy of maximum isometric force) as well as estimate the maximum isometric force (Fmax) for 34 individuals ranging in body size from 124 to 2,390 g. Males grow larger than females in this bandicoot species, however, we found negligible sex differences in mass-specific m _m, PCSA or FL for our sample. Majority of the forelimb muscles PCSA showed a positive allometric relationship with total body mass, while m _m and FL in the majority of forelimb muscles showed isometry. Mechanical similarity was tested, and two thirds of forelimb muscles maximum isometric forces (Fmax) scaled with isometry; therefore the forelimb is primarily mechanical similar throughout ontogeny. PCSA showed a significant difference between scaling slopes between main movers in the power stroke, and main movers of the recovery stroke of scratch-digging. This suggests that some forelimb muscles grow with positive allometry, specially these associated with the power stroke of digging. Intraspecific variation in PCSA is rarely considered in the literature, and thus this is an important study quantifying changes in muscle architectural properties with growth in a mammalian model of scratch-digging.     

One House Two Families: Petrel Squatters Get a Sniff of Low‐Cost Breeding Opportunities

Burrowing is a widespread nesting behaviour, found in vertebrates and invertebrates. It is particularly common in small procellariiform seabirds such as blue petrels (Halobaena caerulea) and Antarctic prions (Pachyptila desolata), two closely related petrel species. However, digging a burrow is costly and alternative strategies may evolve. Accordingly, blue petrel males can adopt two alternative nesting strategies: digging a new burrow or squatting in an empty one. Importantly, a blue petrel squatter arriving at the colony to breed is more likely to find empty Antarctic prion burrows than empty blue petrel burrows, since the former species only start breeding a month later. However, squatting in a prion’s burrow is risky for blue petrels as the legitimate owner very often returns and claims the burrow back, thus ruining the squatter’s breeding attempt. We present here results of a survey of two sympatric colonies of blue petrels and Antarctic prions on Kerguelen Island. Our data show that blue petrel squatters preferentially occupy blue petrel empty burrows. To investigate potential underlying mechanisms behind this preference, we used a simple Y‐maze design to show that blue petrels can discriminate and prefer their specific odour over the prion odour. Our results confirm the existence of alternative burrowing strategies in blue petrels and suggest that squatters could use olfaction to avoid the less suitable Antarctic prion burrows.     

Ontogenetic integration between force production and force reception: a case study in Ctenomys (Rodentia: Caviomorpha)

During ontogeny, complex adaptations undergo changes that sometimes entail different functional capabilities. This fact constrains the behaviour of organisms at each developmental stage. Rodents have ever‐growing incisors for gnawing, and a powerful jaw musculature. The incisors are long enough, relative to their diameter, to be affected by bending stresses. This is particularly true in the subterranean Ctenomys that uses its incisors for digging. We measured bite force (BF) in individuals of different ages using a force transducer. We estimated incisor section modulus Z, a geometrical parameter proportional to bending strength. A relative strength indicator was calculated as S = Z/BF incisor length. We found that ontogenetic BF scales to body mass with positive allometry. However, an anova showed non‐significant differences in S, neither between sexes nor among age classes. This result implies that during growth, incisors might have a rather similar ability to withstand bending stresses from increasing masticatory forces, what may be considered evidence of ontogenetic integration of force production (by muscles) and force reception (by the incisors). This fact well correlates with the observation that pups and juveniles of C. talarum incorporate solid foods shortly after birth, and they are able to dig burrows early in life.     

Testing Magnetic Orientation in a Solitary Subterranean Rodent Ctenomys talarum (Rodentia: Octodontidae)

To test for the hypothesis that Ctenomys talarum can use the earth's magnetic field for spatial orientation, we carried out field and laboratory experiments to analyse if C. talarum burrows present any geomagnetic orientation in their natural habitat, if C. talarum show any spontaneous directional preference when starting to excavate their burrows and if this subterranean rodent is capable to use the earth's magnetic field to orient towards a goal in a complex maze. No correlation between the burrowing direction and the earth's magnetic field was found. We could not find any evidence for any spontaneous directional preference when starting to excavate the burrows in C. talarum. The change of the horizontal vector of the geomagnetic field did not affect the ability of this rodent to orient towards a goal in an artificial labyrinth. Explanations for these results and other possible mechanisms of orientation that could be used by C. talarum are discussed.     

Factors influencing adult emergence from soil and the vertical distribution of burrowing scarab beetles Dasylepida ishigakiensis

The present study investigates the emergence of adult white grub beetles Dasylepida ishigakiensis Niijima et Kinoshita (Coleoptera: Scrabaeidae) from soil as well as their burrowing behaviours. ‘Standby behaviour’ (i.e. adults come to the soil surface where they expose their heads) is shown in the field and, along with emergence behaviour, is entrained by LD photocycles. These 24‐h rhythms persist after transfer to continuous light conditions for 2 days. By contrast, beetles transferred from LD photocycles to continuous dark conditions fail to show standby behaviour; thus, it appears to be manifested only in the presence of illumination. Under dark conditions, beetles emerge completely from the soil directly at the time when standby behaviour is otherwise expected to occur. Emerged adults then burrow back into the soil before dawn. Virgin and mated males, as well as virgin females, which are expected to emerge from the soil for mating on later evenings, burrow to a relatively shallow depth (<2 cm), whereas mated females burrow deeper (2–10 cm). Soil properties such as moisture, grain size, topography and temperature influence the burrowing behaviour and the depths that the beetles reach.     

Craniodental and forelimb specializations for digging in the South American subterranean rodent Ctenomys (Hystricomorpha,Ctenomyidae)

We explored the distribution of tooth- and scratch-digging specializations in species of the subterranean rodent Ctenomys (tuco-tucos) from diverse environments and representing different clades. Principal component analysis of craniodental and postcranial indexes with functional relevance showed that specializations for tooth-digging on one hand, and scratch- digging on the other, formed two uncorrelated groups of variables; functionally significant enamel traits varied concurrently with the tooth-digging specialization axis. Species occupied all sectors of the morphospace showing that craniodental and forelimb specializations have not been mutually exclusive in the evolution of the genus.     

Species specific behavioural patterns (digging and swimming) and reaction to novel objects in wild type, Wistar, Sprague-Dawley and Brown Norway rats

Background

The purpose of the present study was to analyse species-specific forms of behaviour (digging and swimming) and response to novelty in laboratory rats and their wild type counterparts at a very early stage of laboratorization. Three behavioural phenomena were taken into account: burrowing, spontaneous swimming, and neophobic behaviour.

Principal Findings

Wild-type rats and three strains of laboratory rats were involved in experiments: Warsaw-Wild-Captive-Pisula-Stryjek (WWCPS), Wistar, Sprague-Dawley, and Brown Norway rats were compared in spontaneous swimming test, while WWCPS and Wistar rats were studied in burrowing and neophobia experiments. Wild rats were found to be faster at building tunnels than Wistar rats and at constructing more complex burrow systems. The experiment on neophobia showed that Wistar rats exhibited less neophobic responses and were more often trapped. WWCPS rats showed highly neophobic behaviour and were rarely trapped in this experiment. The experiment on swimming showed that WWCPS rats showed more complex water tank related activity than their laboratory counterparts. They swam and explored under surface environment.

Conclusions

The three experiments showed profound behavioural differences in quasi-natural forms of behaviour between wild type rats (WWCPS) and three laboratory strains frequently used in behavioural studies.     

Burrow architecture and digging activity in the Cape dune mole rat

While females are traditionally thought to invest more time and energy into parental care than males, males often invest more resources into searching and displaying for mates, obtaining mates and in male–male conflict. Solitary subterranean mammals perform these activities in a particularly challenging niche, necessitating energetically expensive burrowing to both search for mates and forage for food. This restriction presumably affects males more than females as the former are thought to dig longer tunnels that cover greater distances to search for females. We excavated burrow systems of male and female Cape dune mole rats Bathyergus suillus the, largest truly subterranean mammal, to investigate whether male burrows differ from those of females in ways that reflect mate searching by males. We consider burrow architecture (length, internal dimensions, fractal dimension of tunnel systems, number of nesting chambers and mole mounds on the surface) in relation to mating strategy. Males excavated significantly longer burrow systems with higher fractal dimensions and larger burrow areas than females. Male burrow systems were also significantly farther from one another than females were from other females' burrow systems. However, no sex differences were evident in tunnel cross-sectional area, mass of soil excavated per mound, number of mounds produced per unit burrow length or mass of soil excavated per burrow system. Hence, while males may use their habitat differently from females, they do not appear to differ in the dimensions of the tunnels they create. Thus, exploration and use of the habitat differs between the sexes, which may be a consequence of sex differences in mating behaviour and greater demands for food.     

Burrow behaviour,structure and utilization of the amphibious mudskipper Periophthalmus chrysospilos Bleeker, 1853 in the Mekong Delta

Burrows of fishes are important to their creators, but knowledge of burrowing behaviour, structure and utilization are poorly understood. We report the burrowing behaviour of the amphibious mudskipper, Periophthalmus chysospilos, from estuarine and coastal sites within the Mekong Delta (Vietnam). Activities at and around the burrow were observed over 12 months (April 2020 to March 2021). Burrow casts were recovered monthly to determine burrow structure and utilization in this species. Observations revealed that males excavate burrows with their mouths during the ebb tide. Burrows were J-, Y- and U-shaped, with 1–2 openings to the surface and a bulbous egg chamber. The burrow depth (BD) and total length (BL) varied with shape and site, but not season. The BD and BL ranged from 15.1 ± 0.9 to 18.6 ± 0.80 SE cm and from 22.1 ± 1.2 to 25.7 ± 1.0 SE (standard error of mean) cm, respectively. These results provide insights into the burrowing ability and better understand the ecology of these fishes in the Mekong Delta.Running head: Burrow behaviour, structure and utilization of Periophthalmus chrysospilos.     

Push and bite: trade‐offs between burrowing and biting in a burrowing skink (Acontias percivali)

Trade‐offs are thought to be important in constraining evolutionary divergence, as they may limit phenotypic diversification. Limbless animals that burrow head‐first have been suggested to be evolutionarily constrained in the development of a large head size and sexual head shape dimorphism because of potential trade‐offs associated with burrowing. Here we use an acontiine skink (Acontias percivali) to test for the existence of trade‐offs between traits thought to be important in burrowing (speed and force). As head size dimorphism has been shown to be limited in acontiine lizards, thus suggesting constraints on head size and shape, we additionally explore the potential for trade‐offs between burrowing and biting. Our data show that A. percivali uses a burrowing style different from those previously described for caecilians and amphisbaenians, which relies on the use of extensive lateral and dorsoventral head movements. Our data also show that animals use their entire bodies to generate force, as peak force was determined by total length only. Additionally, both bite force and the time needed to burrow into the substrate were principally determined by relative head width, suggesting a trade‐off between biting and burrow speed. Performance data were indeed suggestive of a correlation between bite force and the time needed to burrow, but additional data are needed to confirm this pattern. In summary, our data suggests that trade‐offs may exist, and may have been of crucial importance in shaping the evolution of head shape in A. percivali, and burrowing lizards more generally. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 91–99.