4.1.2. Microclimate buffer hypothesis
An often-cited potential function of helical burrows is to buffer the
burrow microclimate from the outside environment; microclimate factors
discussed include temperature, humidity, and salinity. Indeed, in our
review, the hypothesis could not be rejected for most taxa (86%, Table
1). Koch (1978) showed that scorpion (Urodacus ) species in more
open areas in more arid parts of Australia construct deeper burrows with
more spirals than those that construct burrows under cover objects in
more mesic areas, concluding “It is clear that deep spiral burrow
construction has evolved as an adaptation for the avoidance of harsh
surface conditions, and has enabled species of the genus Urodacusto spread to otherwise inhospitable arid environments.” While animals
constructing deeper burrows in more arid environments to buffer against
extreme temperatures and low humidity is logical—-Koch successfully
leverages the literature on arthropods in this argument—-this apparent
relationship does not necessarily have a direct bearing on the presence
of, or number of spirals in, a helix, which may simply be a correlate of
depth, without implicating microclimate buffering.
The ichnogenus Daimonelix has been interpreted as multi-purpose
burrows (i.e., polychresichnia; Hasiotis, 2003) in which the helix
functions to buffer inhabitants from surface extremes. Noting the
seasonally hot and dry paleoclimate inhabited by Palaeocaster ,
the Miocene terrestrial beaver tracemaker of some Daimonelix ,
Martin and Bennett (1977) proposed that the helix would contribute to
keeping burrow humidity high. Myer (1999), after calculating the
comparative volumes and surface areas of helical vs. straight burrows,
concluded that the Daimonelix helical design would have resulted
in a more consistent temperature and humidity when extreme variations
were experienced at the surface. In support, Smith (1987, 1993, see also
Smith et al., 2021) hypothesized that the helical burrows ofDiictodon , a mammal-like therapsid from the Permian of South
Africa and another Daimonelix tracemaker, offered climate control
(cool, moist conditions) during extremely hot and dry atmospheric
conditions; limited air flow of the helix would allow the humidity of
the terminal chamber to rise, especially if near the water table.Daimonelix burrows in Triassic (therapsids) and Jurassic
(mammals) continental deposits also occur in floodplain and alluvial
plain settings formed under megamonsoonal and tropical wet-dry climates,
respectively (Fischer and Hasiotis, 2018; Raisanen and Hasiotis, 2018).
Thus, the hypotheses of microclimate mediation and predator avoidance
would apply to these Mesozoic burrows as well.
According to Adams et al. (2016), Koch’s (1978) assertion that scorpion
burrows are more helical and deeper in more arid areas is supported by
exposure to more wind and eddies in a turbulent boundary layer on plains
and sand dunes (Stull, 1988; Turner and Pinshaw, 2015) and higher rates
of water loss in burrowing scorpions than in non-burrowing species
(Gefen and Ar, 2004). Scorpions typically have very low rates of
evaporative water loss through their cuticle, however (Hadley 1970,
1990; Toolson and Hadley 1977). Thus, helical burrows as an adaptation
to sustain high relative humidity, thereby reducing the evaporative
water loss of scorpion inhabitants, is plausible.
Interestingly, deep and shallow helical scorpion burrows were found to
occur together in the same area in central Australia (Hasiotis and
Bourke, 2006; Hembree and Hasiotis, 2006). This association indicates
that there may be other factors at work, such as: (1) the occurrence of
different species with slightly different burrow morphologies; or (2)
ontogenetic variation in burrow size, with older and larger scorpions
having larger diameter, deeper, and more levels of helices in the
burrow. Also, perhaps, the orientation of the dune slope on which the
burrow is constructed may play a role in the burrow depth, with deeper
burrows on north-facing slopes because of the greater amount of solar
insolation.
Some monitor lizards (Varanus ) construct helical burrows solely
for nesting; the 2–4 m deep burrows are unique among helical burrows in
that they are soil-filled (Doody et al., 2014, 2015, 2018a, b, 2021).
This places some doubt on microclimate buffering as an explanation for
helical burrowing in the lizards (Doody et al., 2015). If climate
control is the chief function of the helix, why add soil to the helix,
or why not construct a soil-filled straight burrow? The answer is not
clear. Since the soil-filled monitor burrows are not inhabited by the
lizards themselves, the removal of soil would not be considered when
calculating the relative costs of straight vs. helical burrows. Most
other nesting monitor lizards construct shallower (<0.5 m
deep) burrows in which they remove and then back-fill the soil (Pianka
and King, 2004); thus, the habit of leaving the soil in the burrow
exhibited by the deep-helical-nesting monitor lizards would likely be a
derived behavior. Although the deep-nesting, helical burrowing monitor
lizards do remove soil from the first ~0.5 m of the
burrow length, the remaining soil is not removed. Although it is
possible that monitor lizards evolved helical burrow construction in
response to dry conditions, and then subsequently evolved leaving the
soil in the burrow to further insulate it or to thwart predators, this
sequence of evolutionary events is less parsimonious.
The aquatic helical burrows of the ichnogenus Gyrolithes,constructed from the Permian to the present-day, have been interpreted
as a refuge from extreme salinity fluctuations in transitional
environments between the continental and marine realms (Beynon and
Pemberton, 1992; Buatois et al., 2005; Netto et al., 2007; Hasiotis et
al., 2013). Theoretically, the effect of salinity fluctuations would be
diminished because fine sediment of infaunal habitats slows down the
exchange of pore water (Rhoads, 1975; Saunders et al., 1965). This
hypothesis was based on the idea that Gyrolithes was restricted
to shallow marine environments (Gernant, 1972). However, some (e.g., all
Cambrian) Gyrolithes are found in open-marine environments, which
is suggestive of normal salinity conditions, shedding considerable doubt
on salinity buffering as the primary function of the helix (Netto et
al., 2007; de Gibert et al., 2012; Laing et al., 2018). Moosavizadeh and
Knaust (2021) similarly questioned the modulation of salinity as the
principal function of Gyrolithes due to their apparent
high-salinity paleoenvironments. Similarly, Lapispira has been
found in fully marine deposits (Lanes et al., 2008), shedding doubt on
the salinity buffering hypothesis for that ichnotaxon (de Gibert et al.,
2012).
There are several important caveats to consider when interpreting
behavior and purpose of burrow construction. One of the basic principals
in ichnology is that any one particular burrow architecture—in this
case, helical burrow Gyrolithes —can be used under different
conditions for different purposes (e.g., Ekdale et al., 1984; Bromley,
1996). Some Gyrolithes occur in the transitional zone where
salinities vary between marine, brackish, and fresh water, whereas
others occur in normal marine settings. There are also helical burrows
assigned to Gyrolithes that reflect parts of larger burrow
systems, such as Ophiomorpha and Thalassinoides (Mayoral
and Muñiz, 1995, 1998; Dworschak and Rordrigues, 1997). The occurrence
of Gyrolithes has been attributed to brackish water conditions
but not necessarily extreme in fluctuations, but more like mesohaline or
polyhaline salinities. For example, Jackson et al. (2016) and
Oligmueller and Hasiotis (2022) described Gyrolithes from Lower
Permian river-dominated delta deposits in Antarctica and Upper
Cretaceous intertidal deposits in Colorado (USA), respectively. Both of
these occurrences are in the transitional zone where salinity
fluctuations were a daily phenomenon. Perhaps the helical burrow was a
way for the constructor to limit the amount of water in the burrow
exchanged with the flow and mixing of freshwater with marine water or
the changing tides. Also, the helical structure of Gyrolithesmight have been an advantage to the constructor so as not to be
hydrodynamically removed from the burrow by changing water currents, or
as predator avoidance as the tracemaker withdraws itself into the
burrow.
Evidence for the microclimate buffering hypothesis is indirect at best
for most taxa. In particular, the unique soil-filled burrows of the
monitor lizards raises doubts. Addressing this hypothesis requires
understanding which extended phenotype evolved first—-the helix or the
soil-filled aspect of the burrow. The two known helical-burrowing
monitor lizards are sister taxa, and most other species construct
simple, inclined soil-filled nesting burrows (Pianka and King, 2008).
The ancestral burrow morphology for the helical nesters is thus
soil-filled (back-filling or leaving the soil in place). The helical
burrows are also extremely deep (Doody et al., 2014, 2015, 2018a, b,
2021)—-another derived trait. The most parsimonious evolutionary
sequence of burrow construction for the deep-nesting monitor lizards is
thus, soil-filled first, deep next, and then the helix. Why construct a
helix when the deep, plugged burrow would already provide buffering
between the burrow and the outside environment? The hypothesis appears
to be a poor fit to the monitor lizards.
Increased drainage hypothesis
A third hypothesis for helical burrows in terrestrial taxa proposes that
the helix provides improved drainage in flood conditions via increased
surface area, thereby preventing or reducing burrow flooding that could,
for example, cause mortality or expulsion of scorpions or failure of
lizard eggs (Koch, 1978; Doody et al., 2015). This explanation was
rejected for a majority of taxa (possible in 48% of taxa, Table 1).
Koch (1978) proposed that the extensive spiraling of Urodacusscorpion burrows would reduce the effect of sheet flooding during the
wet season. This idea may be supported by seasonal flash flooding
apparently experienced by Diictodon (the constructor ofDaimonelix; King, 1996), although this hypothesis was not
explicitly discussed (Smith, 1987; Smith et al., 2021). Indeed, somewhat
ironically, the taphonomy of helical burrows relies on flooding in
alluvial environments (e.g., Smith et al., 2021).
Although the helix itself may not beneficial for drainage after
flooding, the upturned terminal chambers on many of the Miocene and some
of the Jurassic Daimonelix burrows (Martin and Bennett, 1977;
Raisanen and Hasiotis, 2018) have been thought to trap air in the burrow
chamber so that during flooding, the burrower would not drown in its
burrow (Hasiotis et al., 2004).
Nesting in both V. panoptes and V. gouldii in northern
Australia is during the late wet season and early dry season, and there
can be substantial rainfall including ‘sheet’ flooding during the first
two months of incubation for the earlier nests (Australia Bureau of
Meteorology). Although the lizard burrows are soil-filled, the soil is
somewhat loose early in incubation. The loose soil combined with the
increased surface area of the helix could improve drainage above the
nest thereby preventing egg inundation, or reducing the amount of time
eggs are inundated. Lizard eggs can withstand inundation for up to six
hours based on previous experiments (Heger and Fox, 1992; Losos et al.,
2003).
Deposit-feeding hypothesis
Some marine forms such as Gyrolithes (e.g., Dworschak and
Rodriquez, 1997; Pervesler and Hohennegger, 2006; Carvalho and Baucon,
2010) may construct helical burrows for deposit feeding in shallow to
deep-water marine settings. Specifically, the increased surface area of
the helix compared to a straight burrow would enhance deposit feeding by
optimizing the utilization of nutrients in a given sediment volume in
animals, such as shrimp, polychaetes, and other vermiform animals. For
example, the helices found in the burrows of the thalassinidian shrimpAxianassa australis may allow the animals to burrow to greater
depths with gentle slopes in order to exploit deeper sediment layers
rich in organic matter (Dworschak and Rodriguez, 1997; see also Atkinson
and Nash, 1990; Nickell and Atkinson, 1995 for similar conclusions for
the shrimp Callianassa subterranea ). Although deposit feeding inA. australis burrows needs confirmation, the poor fit of the
diameter of the shrimp to the burrow diameter suggests deposit feeding,
because suspension feeders tend to fit closely into their burrows
(Dworschak and Pervesler, 1997; see also Pervesler and Dworschak, 1985);
a close fit is necessary for effective ventilation of the burrow for
respiration and feeding in suspension feeders (Dworschak, 1981, 1987).
Wetzel et al. (2010) considered deposit feeding as likely inGyrolithes , partly based on the finding of an abundance of plant
material in the vicinity of the burrows (Dworschak and Rodriguez, 1997).
Laing et al. (2018), however, considered deposit feeding unlikely inGyrolithes , whether made by polychaetes or decapod crustaceans,
based on the lack of evidence of active infill or fecal pellets.
However, the presence or absence of backfill menisci and/or fecal
pellets are not necessary to determine if a burrow is used for
deposit-feeding. There are many callianassid and thalassinid shrimp that
produce fecal pellets while in their burrows and either used them to
construct burrow walls or expel them from the burrow by recirculating
the water (e.g., Kennedy et al., 1969; Curran and Seike, 2016; Netto et
al., 2017).
Helical burrows in terrestrial animals are likely not involved in
feeding, based on the lack of food resources deep in the ground (with
the exception of roots and tubers, which are shallow and close to the
surface), and based on the lack of frequent branching and fecal fillings
(Toots, 1963). The common mole rat does construct complex, shallow
burrows to feed on roots and tubers, but apparently does not construct
helical burrows (e.g., Spinks et al., 2000). Analogous burrow
morphologies to these modern burrowers have been found in Lower Jurassic
continental erg deposits of the Navajo Sandstone in Utah (Riese et al.,
2011).