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plugging the lateral afterward (unpublished data).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.