4.2.1. Falling soil hypothesis
Burrow structure can reflect the energetic cost of burrowing (Vleck, 1981; White, 2001). A new hypothesis, but partly based on previous observations on helical burrowing in scorpions and evidence from vertical burrows in pocket gophers, is that the spirals may allow the animals to excavate a steep descent without much soil falling back into the burrow during excavation; that is, the spirals would serve to hold much of the newly excavated soil that would otherwise fall back into the burrow terminus as its being removed, preventing or impeding further excavation.
The first line of evidence supporting this hypothesis is found in the relationship between climate-soil type-soil moisture and burrow depth-number of spirals in scorpions. Scorpions occupying dry climates with sandy dry soils construct deeper burrows with more spirals than those in wetter climates. Polis (1990) hypothesized that by attenuating the burrow angles the spirals would facilitate the vertical movements of scorpions in burrows that are required to be deep enough to reach optimal temperature and humidity. Adams et al. (2016) countered that several species of scorpions construct simple vertical burrows without spirals that descend 70–90° from the horizontal to 15–10 cm deep. This comparison is confounded by soil type and moisture, however. Compared to those in more mesic environments, scorpion burrows in more arid climates are deeper and possess more spirals (references in Adams et al., 2010). For example, burrows of the scorpion Urodacus yaschenkoi in loose sandy soil with little clay content were significantly shallower in depth and angle, and with more spirals, compared to those in damp, low-lying areas subject to flooding (Koch, 1977, 1978; Shorthouse and Marple, 1980). Similarly, the deepest scorpion burrows with the most spirals in South Africa were found in soils with high sand content and low content of silt, clay, and organic matter, as well as low soil moisture, compared to scorpion burrows in other areas (Abdel-Nabi et al., 2004).
A second piece of related evidence comes from burrows of the pocket gopher, Thonomys bottae , which excavates lateral tunnels running parallel to the surface but must push excavated soil to the surface to clear the burrows. According to Vleck (1981), “Thonomys in cohesive soils often dig nearly vertical laterals and have little difficulty pushing lumps of excavated soil out or plugging the lateral afterward (unpublished data). However, in cohesionless sands like those in the study area, pocket gophers’ efficiency in pushing soil declines as slope increases. At steep angles of ascent, much of a load of sand may fall back down the tunnel, increasing the number of trips necessary to push a given amount out. Laboratory observations indicate that T. bottae may also have difficulty in plugging the surface openings of vertical tunnels in cohesionless soils. The slope of laterals is probably dictated by soil characteristics and the differential efficiency of pushing soil with changes in slope. Laterals that ascend at shallow angles may be the most efficient solution in sandy soil.”
White (2001) demonstrated that the energetically cheapest method of reaching an appropriate depth is to burrow the shortest possible distance, which would be straight down (a vertical burrow). However, they also noted that burrow structure may not be determined solely by energetic concerns, and constructing a burrow from the surface at 90° may not be possible. The burrow entrance constructed by the scorpionU. yaschenkoi is angled at about 25–30° (Koch 1978; Shorthouse and Marples 1980), only marginally shallower than the angle of repose of dune sand (32°: Robinson and Seely 1980). Thus, if burrows were constructed at angles > 32°, sand would fall into, and fill the burrow (White, 2001). Beyond the entrance run, the burrows begin to spiral and descend steeply, as the soil becomes moister and more cohesive with increasing depth. Burrows constructed by U. yaschenkoi, thus, minimize both the energy used during burrow construction by descending as steeply as possible, and the energy required for burrow maintenance by constructing an entrance run that is shallower than the angle of repose of dune sand (White, 2001).
As with scorpions, helical burrows of deep-nesting monitor lizards also exhibit a straight, gently sloping entrance run followed by a deeply descending helix (Doody et al., 2015; 2018). The major difference is that the lizard burrows are soil-filled—-the soil is not removed during construction. Thus, White’s (2001) calculations of energy expended moving soil out of the burrow would not apply to the lizard burrows because the lizards do not remove the soil (except for the first ~0.5 m straight run). This focuses attention on the digging action by asking: why not excavate straight down or straight at a steep angle of incline? The answer may lie in the ability of the spiral, combined with the lizard’s body, in preventing loose, excavated soil from falling back into the burrow terminus. Resisting the effects of gravity by repeatedly removing falling soil would not only incur extra costs, but could prohibit burrow construction.
Meyer (1999) used volumetric calculations to conclude that a helix would cost 36–61% more effort than a straight burrow. We do not challenge the calculations or logic used by Meyer (1999); rather, we note that those calculations did not consider the cost of repeatedly moving the same soil that falls into the (shifting) burrow terminus during construction. Thus, the need for constructing deep burrows—-which apparently evolved to provide moist conditions during the long dry season incubation period in Varanus lizards (see Doody et al., 2015, 2018)—-may have ‘prompted’ helical construction to reduce the energetic cost of repeatedly removing falling soil, or the falling soil could have prohibited construction altogether. Another factor to consider is the degree of firmness or cohesiveness of the soil in whichDaimonelix was excavated. If the burrow walls contain scratch marks (sensu Zonneveld et al., 2022), then the sediment was cohesive and much less likely to collapse in on itself. This would limit the amount of effort in moving excavated material as long as the matrix did not collapse in on it. Vertical burrows in stiff or firm, cohesive sediment would also stay open; however, the biomechanics of the organism would determine if a vertical burrow was a constructable and/or livable situation (c.f., Hasiotis and Mitchell, 1993).
Could the falling soil hypothesis explain helical burrows in other animals? The challenge of constructing a burrow vertically while resisting the effects of gravity on both the body and loosened soil could be general. Even in aquatic burrows the excavated soil must be removed upwards against gravity, and a straight vertical shaft could inhibit or prohibit this. Consider the amount of effort an organism expends in maintaining its position in a vertical burrow excavated in soil, 1–5 m deep, with appendages sprawled while excavating or maintaining the burrow and removing the material to the surface. An arthropod (e.g., arachnid, crustacean, or hexapod) with 6, 8, or 10 pairs of appendages could accomplish this feat (e.g., Hasiotis and Mitchell, 1993; Hasiotis et al., 1993). Such burrow construction by a tetrapod would be extremely difficulty for carrying material while removing it from the bottom or maintaining its position in the burrow to maintain the burrow walls (Hasiotis et al., 1999).
A gently inclined, long burrow might incur a lower energetic cost to construct depending on the degree of inclination and distance between the burrow entrance and terminus. Soil profiles have surface and subsurface horizons from top to bottom with distinct composition and firmness (e.g., Kraus, 1999; Brady and Weil, 2002). A gently inclined burrow would increase the probability of spending more time within a horizon with similar composition and firmness, whereas a vertical burrow would have a higher probability of passing more quickly through multiple horizons with different composition and firmness. If an inclined burrow passes from a surface horizon that is relatively loose and contains organics (i.e., A horizon) into a subsurface horizon (E, B, or C horizon) that is more cohesive and firmer, than a higher energetic cost might be incurred. The degree of energetic costs depends on the development and thickness of each horizon, which reflects overall soil formation.
The solution to conserve energy expenditure during construction would seem to be a zigzag or switchback pattern which could eventually ‘tighten’ into a helix. However, some marine organisms construct(ed) helical burrows in the horizontal direction (e.g., Dworschak and Rodrigues, 1997; Minter et al., 2008); the falling soil hypothesis is not a good fit as an explanation for helical burrows in these species. Similarly, some helical sections in the burrows of the shrimpCallianassa bouvier may be excavated in the upwards direction (Dworschak and Pervesler, 1988).
Some skinks construct a switchback style of burrow that mimics a spiral (Hembree and Hasiotis, 2006). These switchbacks come from the main part of the inclined burrow, which is flattened, elliptical in cross-section, and resembles an upside-down U or reniform-shape (Hasiotis et al., 2004; Hembree and Hasiotis, 2006). A possible function of this switchback structure, which is not visible from the surface of the soil, is to escape the burrow if a predator enters. Likewise, if the hidden switchback burrow opening is discovered, a potential predator might not be able to follow the tortuous path into the main part of the burrow.
Testing the falling soil hypothesis in monitor lizards could involve observing nesting females in a captive situation to determine how well mothers prevent soil from reaching the burrow terminus; alternatively, recreating a helix in the laboratory with a model lizard could shed insights into this ability, as would experiments with humans attempting to construct a helical burrow.