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).