Why Animals Construct Helical Burrows:
Construction vs. Post-Construction Benefits
J. Sean Doodya*, Shivam Shuklaa and
Stephen T. Hasiotisb
aDept. of Integrative Biology, University of South
Florida, St. Petersburg Campus, 140 7th Ave. South,
St. Petersburg, Florida 33701 USA
bDept. of Geology, University of Kansas, 1475 Jayhawk
Blvd, Lindley Hall, rm 215, Lawrence, Kansas 66045 USA
*Corresponding author:
jsdoody@usf.edu
Abstract
The extended phenotype of helical burrowing behavior in animals has
evolved independently many times since first appearing after the
Cambrian explosion (~540 million years ago). A number of
hypotheses have been proposed to explain the evolution of helical
burrowing in certain taxa, but no study has searched for a general
explanation encompassing all taxa. We reviewed helical burrowing in both
extant and extinct animals and from the trace fossil record and compiled
from the literature 10 possible hypotheses for why animals construct
helical burrows, including our own ideas. Of these, six were
post-construction hypotheses—-benefits to the creator or offspring,
realized after burrow construction—-and four were construction
hypotheses reflecting direct benefits to the creator during
construction. We examined the fit of these hypotheses to a total of 21
extant taxa and ichnotaxa representing 59–184 spp . Only two
hypotheses—-antipredator, biomechanical advantage—-could not be
rejected for any species (possible in 100% of spp. ), but six of
the hypotheses could not be rejected for most species (possible in
86–100 % of spp. ): microclimate buffer, reduced falling
sediment (soil), anticrowding, vertical patch, and the above two
hypotheses. Four of these six were construction hypotheses, raising the
possibility that helical burrowing might have evolved without providing
post-construction benefits. Our analysis showed that increased drainage,
deposit feeding, microbial farming, and offspring escape could not
explain helical burrowing behavior in the majority of taxa (5–48%).
Overall, the evidence does not support a general explanation for the
evolution of helical burrowing in animals. The function and evolution of
the helix as an extended phenotype would seem, at least in some cases,
to provide different advantages for different taxa. Although direct
tests of many of the hypotheses would be difficult, we nevertheless
offer ways to test some of the hypotheses for selected taxa.
Key words: behavior; extended phenotype; costs-benefit; spiral burrow;
helix; ichnotaxa
Introduction
An extended phenotype, when referring to a single species, includes some
architecture or entity (e.g., beaver dam, termite mound) in which the
phenotype is the fitness of the construction for survival and
reproduction (Dawkins, 1982, 2004). Scientific interest in extended
phenotypes has been widespread and sustained, encompassing diverse areas
ranging from parasite manipulation of hosts (Hughes and Libersat, 2019)
to relationships between genomes and phenotypes (Hunter, 2018) to human
sexual selection theory (Luoto, 2019).
Burrow architectures are classic extended phenotypes that show great
diversity and complexity and can reflect important fitness-related
traits (Hansell, 2005). In a classic example, the old-field mouse,Peromyscus polionotus , constructs complex burrows with a long
entrance tunnel that leads into a nest cavity and a secondary escape
tunnel, while its sister species, the deer mouse (P. maniculatus )
builds shorter, single-tunnel burrows (Weber et al., 2013). The complex
burrowing behavior of P. polionotus is derived, has a strong
genetic component, and its putative adaptive function is to facilitate
escape in an open, exposed habitat (Wolfe and Esher, 1977; Weber and
Hoekstra, 2009; Weber et al., 2013).
A diversity of terrestrial and aquatic animals excavates mysterious
helical burrows that comprise multiple, symmetrical spirals descending
into a medium (i.e., substrate, sediment). The first of these kinds of
burrows appeared with the Cambrian explosion ~540
million years ago (e.g., Goldring and Jensen, 1996; Hasiotis, 2012;
Sappenfield et al., 2012; Zhang et al., 2015) and many others are known
only from fossils, including the remarkable 3-meter-deep burrows
assigned to the ichnotaxon Daimonelix that were constructed by
the terrestrial beaver Palaeocaster from the Miocene (Barbour,
1892; Martin and Bennett, 1977). Various forms of Daimonelix are
now known to have been constructed by a variety of terrestrial
vertebrates since the Late Permian, approximately 260 million years ago
(Smith, 1987; Fischer and Hasiotis, 2018; Raisanen and Hasiotis, 2018).
Living examples of species that construct helical burrows include
terrestrial taxa, such as some pocket gophers, monitor lizards, and
scorpions, and marine forms such as some shrimp and some polychaetes
(e.g., Powell, 1977; Koch, 1978; Löwemark and Schäfer, 2003; Hasiotis
and Bourke 2006; Netto et al., 2007; Wilkins and Roberts, 2007; Doody et
al., 2015).
The relentless, independent evolution of helical burrowing behavior
across disparate unrelated taxa dating back hundreds of millions of
years attests to its apparent utility. Yet, the reason(s) for the
evolution of the helix from more simple burrows remains largely
speculative and unresolved. One problem is that little is known of the
natural history of the tracemakers of the fossil burrows or trace
fossils (e.g., Bromley, 1996; Hasiotis 2007). Another problem is no
study has considered all taxa in the search for a general explanation,
although a diversity of functions is certainly possible and is sometimes
suggested. To illustrate, collectively, helical burrows have been
proposed to have evolved to buffer microclimate of the burrow from
harsher outside conditions (e.g., temperature, aridity, salinity),
promote drainage during flooding, thwart predators, reduce burrow
interference with conspecifics, increase surface area to expose more
sediment for deposit-feeding, or promote bacterial farming (e.g., Martin
and Bennett, 1977; Koch, 1978; Dworschak & Rodriguez, 1997; Myer, 1999;
Netto et al., 2007; de Gibert et al., 2012; Doody et al., 2015; Raisanen
and Hasiotis, 2018; Muñiz and Belaústegui, 2019). Moreover, some have
hypothesized that helical burrows could serve multiple functions
(behavioral category polychresichnia; Hasiotis, 2003) (Koch, 1978; Netto
et al., 2007; Carvalho and Baucon, 2010; deGibert et al., 2012; Raisanen
and Hasiotis, 2018).
These hypotheses offered to explain helical burrowing behavior generally
invoke adaptation in the form of ‘post-construction’ benefits to the
creator. Indeed, an adaptive function(s) of helical burrows seems
plausible, given its multiple origins and the increased effort required
to create a helix compared to a simpler (straight) burrow of the same
incline (volumetric calculations by Meyer, 1999). Much less attention
has been given to ‘construction’ costs-benefits of helical burrows, or
those that provide no benefit to the occupant after burrow construction,
but rather are restricted to cost-benefits of burrowing behavior itself.
In an exception, White (2001) estimated the total cost of helical burrow
construction in scorpions by calculating the net cost of soil transport
and the costs of the animal moving itself and soil horizontally, and
vertically against gravity. Helical burrowing scorpions minimized both
(i) the energy used during burrow excavation by descending as steeply as
possible, and (ii) the energy required for burrow maintenance, by
constructing an entrance run that is shallower than the angle of repose
(rest) of dune sand (White, 2001).
Recently, two species of monitor lizards were found to excavate deep,
helical burrows for the sole purpose of nesting and the authors
discussed the fit of some post-construction (adaptive) hypotheses for
the function of the helix in these lizards (Doody et al., 2014, 2015,
2018a, b, 2021). The communal nests of the yellow-spotted monitor
(Varanus panoptes ) and Gould’s monitor (V. gouldii ) are by
far the deepest extant vertebrate ground nests known (averaging 2–3 m
deep and reaching 4 m deep). The burrows are soil-filled, and consist of
an incline to a depth > 1m, followed by 2–7 tight
descending spirals that terminate in a slightly enlarged nest chamber
(Fig.1a,b). Mothers excavate the burrows, lay their eggs, and then
abandon the burrows. Unlike scorpions, the lizards do not transport the
soil out from the burrows—-they remain soil-filled and the lizards
‘swim’ through the excavated soil after laying eggs. Thus, White’s
(2001) calculations and conclusions for scorpions and potentially other
animals do not apply to the lizards. Although a few of the
post-construction hypotheses might apply to the lizard burrows (e.g.,
the helix potentially reducing egg predation), ‘construction’ benefits
may provide a more parsimonious explanation than ‘post-construction’
benefits; e.g., the helix preventing soil from falling back into the
burrow as it’s removed; falling soil might make burrow creation
impossible or extremely difficult in a steep and straight inclined
burrow.
Herein we generate and review the major ‘construction’ and
‘post-construction’ hypotheses for why animals evolve the extended
phenotype of helical burrows. We address 10 hypotheses including those
extracted from the literature and our own. We ask if any of the
hypotheses could be general for all taxa. If not, we ask the opposite
question: Why did helical burrowing evolve for different reasons in
different taxa? To address these two overarching questions, we examined
the fit of each hypothesis to each of 21 taxa representing 77–188 spp.,
based on natural history, behavior, and deductive reasoning, from
published sources. We outline potential future tests of hypotheses for
selected taxa.
Materials and Methods
We surveyed the scientific literature for evidence of helical burrows in
invertebrates and vertebrates using two-way searches on Google Scholar
and Google (general web search). We excluded species for which there was
only one (or less) spiral turn (e.g., Linsenmair, 1967; Basan and Frey,
1977; Hembree, 2009; Carvalho and Baucon, 2010; Kinlaw and Grasmueck,
2012; Hembree, 2014; Mikus and Uchman, 2013; Vazirianzadeh et al., 2017;
Paul et al., 2019). We also excluded studies describing burrows that
were weakly helical, weakly sinusoidal or ‘loosely spiraling’ (e.g.,
Finlayson 1935 in Johnson, 1989; Koch, 1978; Coelho et al., 2000; Kinlaw
and Grasmueck, 2012). Although there is likely a continuum of sinuosity,
we found a somewhat dichotomous grouping of burrows that were slightly
curved vs. repeatedly or regularly spiral or helical. We thus only
included species with burrows described as ‘tortuous’ or ‘possessing
regularly descending spiral coils,’ or a ‘helix’ (e.g., Powell, 1977;
Koch, 1978). Although the behavior of constructing weakly helical
burrows could be important in understanding the evolution of helical
burrowing behavior (indeed Urodacus scorpions do both), the
number of taxa exhibiting weakly spiral burrowing are too numerous to
consider here. Moreover, the degree of burrow sinuosity has not been
quantified for most taxa, making interspecific comparisons difficult. We
included papers on both extant and extinct helical burrows produced by
animals, although the producers of helical burrows—-trace fossils
reported as ichnotaxa or described in open nomenclature—-in the fossil
record are often unknown. For trace fossils, several tracemakers from
different species as well as different phyla can produce a similar type
of trace fossil morphology (ichnotaxon), for example Daimonelix(Raisanen and Hasiotis, 2018). Thus, our data rows in Table 1 often
reflected more than one species. We also do not consider burrows that
occurred in one horizontal plane, including sinusoidal traces (e.g.,Sinusichnus ; Belaústegui et al., 2014; Soares et al., 2020) and
the spiral feeding traces that occur in soft sediment in one surface
plane (e.g., the polychaete Paraonis fulgens ; Risk and
Tunnicliffe, 1978).
We compiled hypotheses offered for the function of the helix, against
which we could assign the likelihood that the hypothesis fit a
particular taxon or ichnotaxon. For this we used ‘possible’, ‘not
likely’ or ‘n/a’ (not applicable); ‘n/a’ indicated that there was
virtually no chance of a fit, based on deductive reasoning. For example,
the hatchling escape hypothesis developed for lizards, which proposes
that the helix loosens the soil to facilitate hatchlings escaping the
burrow through meters of resistant soil, would not be applicable to
aquatic species with open burrows. We subjectively assigned ‘not likely’
if a good fit was unlikely, and we explained our reasoning in the text.
Unlike with ‘n/a’, ‘not likely’ could change with the addition of new
information or if our reasoning or that of others, was less informed.
The assignment of ‘possible’ indicated a good fit or potential fit,
based on the available evidence, context, and our reasoning or that of
other authors. In many cases, however, designation of ‘possible’
reflects that difficulty in testing hypotheses—-for example, directly
testing the antipredator hypothesis for most extinct species is not
possible. Thus, we could not conclusively claim that a hypothesis was
general even if it scored ‘100% possible’ for all taxa. However, by
eliminating some taxa for each hypothesis (by assigning ‘n/a or ‘not
likely’) we could potentially conclude that some or all of the
hypotheses could be general for all taxa.
Results
Table 1 shows the results of the fit of hypotheses for the function of
helical burrows to 21 taxa representing 59–184 species. The wide range
in the potential number of species reflects both our lack of knowledge
of the burrow types in extant and extinct conspecifics and the
uncertainty of the species richness of ichnotaxa.
Of the 10 hypotheses, six are post-construction hypotheses and four are
construction hypotheses. Of the 21 taxa, 12 (57%) are extant, eight
(38%) are ichnotaxa and one includes both (5%; Table 1).
Two of the hypotheses, antipredator and biomechanical advantage, were
designated as ‘possible’ for all taxa (score of 100%; Table 1). Other
high-scoring hypotheses were the anticrowding (95%), vertical patch
(95%), falling sediment (soil) (95%), and microclimate buffer
hypotheses (86%). Two hypotheses, deposit feeding and increase
drainage, received moderate scores (both 48%), mainly due to the fit of
each to only terrestrial or only aquatic animals (Table 1). The
remaining two hypotheses, microbial farming and offspring escape,
received low scores (24% and 5%, respectively).
Although the hypothesis sample sizes precluded statistical comparison,
the mean score for construction hypotheses (91.5 ± 2.99% SE; N=4) was
higher than the mean score for post-construction hypotheses (49.3 ±
14.06% SE; N=6).
Discussion
Our review revealed that six of the 10 hypotheses for why animal
construct helical burrows could not be confidently rejected for most of
the taxa (86–100% possible; Table 1). These hypotheses range from
‘indirectly testable’ (falling sediment, vertical patch, biomechanical)
to ‘extremely difficult or impossible to test’ (antipredator,
anticrowding). Interestingly, four of those six hypotheses are
‘construction’ hypotheses, raising the possibility that helical
burrowing could save on energy costs associated with constructing a
helix without implicating post-construction adaptive benefits. Our
analysis also eliminated some hypotheses as general explanations for the
behavior; hypotheses involving increased drainage, deposit feeding,
microbial farming, and hatchling escape could not explain helical
burrowing behavior in the majority of the animals (5–48%, Table 1).
The function and evolution of the helix as an extended phenotype remain
unknown but would seem, in some cases, to provide different advantages
for different taxa. In the following sections we discuss the fit of each
hypothesis to selected taxa.