Trace Fossils and Extended Organisms: a Physiological Perspective

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Palaeogeography, Palaeoclimatology, Palaeoecology 192 (2003) 15^31 www.elsevier.com/locate/palaeo

Trace fossils and extended organisms: a physiological perspective

J. Scott Turner

Department of Environmental and Forest Biology, SUNY College of Environmental Science and Forestry, Syracuse, NY 13210, USA

Received 7 January 2002; accepted 6 December 2002

Abstract

Organism-built structures have long been useful artifacts for students of evolution and systematics, because they represent a permanent record of a set of behaviors. These structures also represent an investment of energy by an organism, and to persist in the fossil record, the energetic investment in the structure must pay off for the organisms that build it, in either improved survivorship, increased physiological efficiency or enhanced fecundity. A useful way to think about this aspect of organism-built structures is to treat them as external organs of physiology, channeling or tapping into energy sources for doing physiological work. This paper reviews briefly how burrows and nests can act as external organs of physiology at various levels of organization, and introduces the notion of organism-built structures as adaptive structures, in which feedback controls confer adaptability to organisms’ external constructions, and which promote homeostasis of the organism and its local environment. Miller’s concept of trace fossils as behavioral tokens reflects this aspect of animal-built structures, and may illuminate many unanswered questions concerning their origins and persistence in the fossil record. ß 2002 Elsevier Science B.V. All rights reserved.

Keywords: biogenic structures; extended physiology; extended organism; boundary layer; induced £ow; natural convection; kelp; termite; £uid mechanics; soil water

1. Introduction known from the fossil record, or to some organism whose existence can only be inferred from its Trace fossils commonly present two challenges traces. On the other hand, a trace fossil is also a to the paleontologist. On the one hand, a trace remnant of a process, a ‘frozen behavior’, in fossil indicates that an organism left an impres- which case the challenge is to reconstruct the pro- sion on its environment at some time in the past, cesses that gave rise to it. Usually, this involves even if the organism itself left no remains. In this deriving a behavior or sequence of behaviors in- case, the challenge is to connect the trace fossil to volved directly in its construction, such as infer- the organism that built it, whether to an organism ring a burrowing behavior from the ways sediments are rearranged in a burrow (Bromley, 1990; Crimes, 1994). * Tel.: +1-315-470-6806; Fax: +1-315-470-6934. Trace fossils can also be remnants of structures E-mail address: [email protected] (J.S. Turner). that did things for the organisms that built them,

PALAEO 3000 13-2-03 16 J.S. Turner / Palaeogeography, Palaeoclimatology, Palaeoecology 192 (2003) 15^31 which makes them more than simply the impressions of a past existence or outcomes of past behaviors (Miller, 2002). It makes them akin to organs of an ‘extended physiology’, means of co- opting the physical environment into physiological function. In short, trace fossils can represent the remnants of ‘extended organisms’ (Turner, 2000a; Miller, 2002). This presents a third challenge for the paleontologist: recovering the past physiology the trace fossil represents. This aspect of trace fossils ^ ichnophysiology, if I may coin a Fig. 1. Conventional and extended physiology compared. term ^ is the subject of my contribution to this (a) Simpli¢ed scheme of phosphorylation of ADP by tapping a potential energy gradient in proton concentration ([Hþ]) volume. I will develop three broad themes. First, across the inner membrane of the mitochondrion. (b) Simpli- ichnophysiology, like all types of paleophysiology, ¢ed scheme of a structure that converts a variation of wind involves inference about function from structure, speed (U) into a potential energy gradient in pressure (P), which requires a set of rules for how structure which then does work moving air through the structure. maps onto function. Extended physiology has a somewhat di¡erent set of mapping rules than the ogy, it behooves us ¢rst to clarify what physiology conventional physiology that is con¢ned within is. an organism’s skin. This can make the ‘reverse At root, physiology involves the adaptively engineering’ of organs of extended physiology a controlled £ow of matter, energy, or information bit tricky. Second, extended physiology is often ^ physiological work ^ across a boundary of some powered by external sources of energy, such as sort. Conventional physiology, what one might tides, currents, winds, gravity and light. These di- call ‘blood-and-guts’ physiology, is concerned verse sources of energy enable a remarkably di- with boundaries found within organisms, such as verse array of structures that could be organs of cell membranes, or epithelia that separate one extended physiology. An incipient ichnophysiol- compartment of a body from another. For exam- ogy should be cognizant of this diversity, and I ple, oxidative phosphorylation of ATP in the o¡er a few examples from the extended physiol- mitochondrion is powered by the managed £ow ogy of modern organisms. Finally, extended phys- of protons down a gradient in chemical potential iology involves the adaptive modi¢cation of the between the organelle’s inter-membrane space and physical environment, which blurs the distinction its matrix (Fig. 1a). If the protons follow a par- between the living organism and its supposedly ticular pathway, determined by the complement inanimate surroundings. This raises interesting of proteins within the mitochondrion’s inner questions of scale and category, for it puts no membrane, then the work of phosphorylation intrinsic limit on how broadly extended physiol- can be done. Otherwise, the protons either do ogy ^ whether present or past ^ can a¡ect envi- not £ow, or do no work if they do £ow, in which ronments. This poses many challenging questions case their energy is dissipated as heat (Nicholls, for ichnology, and I o¡er two: what is a trace 1982). fossil; and how is ichnology to be distinguished Physiological boundaries can exist at multiple from the broader disciplines of paleontology, geo- levels, and these nest hierarchically, like Ma- physiology and ecology? tryoshka dolls. The managed £ow of protons in the mitochondrion is supported by other managed £ows across the cell membrane, across exchange 2. Extended physiology and the inference of epithelia in the lungs or digestive tract, and so function from structure forth (Weibel et al., 1987). There is no good reason why physiology must be limited to conven- If trace fossils can be remnants of past physiol- tional boundaries within organisms, however.

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Physiological processes occur at an organism’s nisms, and it asks questions like: what is the ven- outermost boundary, across the integumentary tilatory rate (how fast could the animal run)?; boundary between ‘inside’ and ‘outside’ the or- what is the cost of ventilation (what is the cost ganism. If an organism constructs a boundary of locomotion)?; how is its function regulated outside its body that adaptively manages a £ow (what are the stresses the bone is likely to experi- of matter, energy or information, this is as surely ence)?; and so forth. If a putative ichnophysiol- physiology as are similarly managed £ows across, ogy is to have value, it must be able to address say, a cell membrane. A termite mound, for ex- such questions. Its ability to do so is both com- ample, captures wind energy to power ventilation plicated and enriched by the peculiar rules of ex- of its colony (Fig. 1b). The mound is simply the tended physiology. next larger Matryoshka doll of the termites’ ex- To illustrate, let us explore the function of a U- tended physiology (Turner, 2000a). burrow, a common architectural motif among an- That biogenic structures can be organs of ex- imal burrows, both modern and fossil (Vogel, tended physiology is not, in itself, interesting. To 1978; Bromley, 1990). Let us imagine an organ- assert that a termite mound is a wind-ventilated ism, like a lugworm, that uses its muscles to structure is akin to saying that a leg bone signi¢es power ventilation through this burrow. The phys- that the animal to which it was attached could iological function, ventilation, has a cost, which is run. All would agree, I think, on the triviality of roughly the energy needed to overcome the mo- both assertions. Physiology, in whatever form it mentum loss from viscous interactions of the takes, is essentially a science of rates and mecha- water with the burrow walls. The lugworm-like

Fig. 2. Design constraints on induced ventilation of a U-burrow by external currents. (a) Currents through tubes driven by unsteady forces are determined by the frequency of change of those forces. As the frequency of the oscillatory £ow increases (pro- portional to the Womersley number, the volume of induced £ow through the burrow declines and falls progressively out of phase with the external £ow. (b) When the forces driving induced £ow are steady (equivalent to a frequency of 0 Hz), induced £ow is unidirectional and steady. (c) At moderate frequencies of unsteady £ow, induced £ow through the burrow (dotted line) is attenuated only slightly compared to the driving force. (d) At high frequencies of unsteady £ow, induced £ow through the burrow is strongly attenuated and markedly out of phase with the external forces driving it.

PALAEO 3000 13-2-03 18 J.S. Turner / Palaeogeography, Palaeoclimatology, Palaeoecology 192 (2003) 15^31 creature might derive a bene¢t from the ventila- Making the burrow longer, for example, might tion, let us say in enhanced productivity of the increase the production rate of food in the sedi- sediments surrounding the burrow. The physio- ments surrounding the burrow, but that bene¢t logical function of the burrow is therefore amena- will always be limited by the increased cost of ble to a simple cost^bene¢t analysis: pumping that a longer burrow would require. To use the metaphor of the Matryoshka doll, ðventilation costÞþproductivity ¼ net return the shape, even the design motif, of the outermost (debits are in parentheses). doll is, to some extent, determined by the nature of the innermost doll. The cost of running a muscle-ventilated burrow is But what if cost of ventilation was met in some met by an expenditure of ATP, determined by the other way? Some U-burrows are ‘self-ventilated’ energy required to make good the viscous losses by so-called induced £ow, in which the two open- in the £ow, adjusted for the worm’s e⁄ciency at ings of the burrow span a gradient in momentum converting ATP to £ow. The bene¢t ^ the en- in a surface boundary layer (Vogel, 1978, 1981). hanced productivity in the burrow’s surroundings The cost of ventilation is now no longer met by ^ involves the production of high quality food ATP alone, and the architectural constraints on that can be eaten by the lugworm and converted muscle-ventilated burrows may no longer apply to to usable energy, also expressible as ATP. The a self-ventilated burrow. Such burrows could, for cost^bene¢t analysis can therefore be expressed example, be made longer than ‘expected’ for as an ATP budget: muscle-ventilated burrows, because the increased productivity in the sediments is no longer o¡set ATP þ ATP ¼ ATP in return net by an increased cost of pumping. Self-ventilation which is, at root, an energy budget, and therefore is not all free lunch, though, because it now relies constrained by conservation of energy. This on a potentially unreliable or chaotic source of makes reverse engineering of the burrow’s func- energy: winds die and freshen, currents ebb and tion easier, because all these terms could, in prin- £ow, £ows are often turbulent, and so forth. The ciple, be recovered from our hypothetical fossil U- qualitatively di¡erent nature of the power supply burrow. Viscous losses can be calculated from the now imposes its own constraints and rules on how fossil burrow’s dimensions and elementary princi- the structure might best be built. To return to our ples of £uid mechanics. Pumping e⁄ciency can be nesting dolls metaphor, the shape and design mo- inferred from observations of modern inhabitants tif of the outermost Matryoshka doll may be de- of U-burrows. Enhancement of productivity could termined as much by the nature of the environ- be inferred from, say, the local distribution of ox- mental source of energy as by how it interacts idation potential, evident as the ‘halos’ of oxida- with those qualities in the innermost doll. tion that surround many fossil burrows. Consider, for example, induced ventilation of a Reverse engineering is only as good as the as- U-burrow by a so-called unsteady £ow, such as a sumptions that underlie it. As always, the un- tidal or wave surge. Water in the burrow would stated assumptions are the riskiest. Reducing the undergo periodic acceleration or deceleration as function of the muscle-ventilated burrow to the the velocity of the external £ow changed with common energy currency of ATP carries subtle time. Each time this happens, some energy that implications for the structure of the ‘organ’ that otherwise might power ventilation now must over- e¡ects the function. For example, the ATP ergon- come momentum: the more frequently this hap- omy of organisms is tightly regulated, and this pens, the greater this diversion will be (Fig. 2). In imposes a degree of regulation on all the physio- short, U-burrows exposed to unsteady £ows be- logical systems that support it, whether these be have essentially as low pass ¢lters. When rate of conventional or extended. The architecture of the change is slow, as it might be in the ebb and £ow muscle-ventilated U-burrow is determined largely of a tidal surge, water in the burrow is accelerated by its impact on the organism’s ATP ergonomy. only rarely, and more of the energy in the tidal

PALAEO 3000 13-2-03 J.S. Turner / Palaeogeography, Palaeoclimatology, Palaeoecology 192 (2003) 15^31 19 current can power ventilation. Flow through the ral environments, and many biogenic structures burrow tracks the change of external £ow closely, appear directed to managing it. At the simplest, £ow is voluminous, and the burrow is ventilated we can distinguish two broad types: turbulence uniformly. However, if external £ows change enhancers, which take a laminar or near turbulent quickly or frequently, more energy is diverted to £ow, and generate turbulence, and turbulence changing momentum, less energy is available to dampers, which convert turbulent £ows into slow- power ventilation, and £ows fall progressively er or near laminar £ows. In both cases, the struc- out of phase with changes of the external £ow. ture is being used to manage the distribution of Volume of £ow also declines: once this falls below energy in the £ow. The concept of a power spec- the burrow’s volume, dead spaces appear in the trum is useful for understanding how. burrow, akin to the anatomical dead space of the Turbulent £ow is characterized by chaotic lung (Fig. 2). Now, burrow length and volume changes in velocity, which can be partitioned may be limited to the extent of dead space, rather into unsteady £ows of various frequencies. The than any energetic limitation on cost of pumping. total energy in the £ow is simply the Fourier Just to complicate things, the burrower may in- sum of the energy in all the component frequen- vest ATP energy, as it does in muscle-powered cies. Various types of £ow partition the energy ventilation, but use it to compensate for the short- di¡erently. By shu¥ing energy around between comings of induced ventilation. The burrow’s res- various frequency components, biogenic struc- ident might be forced, for example, to reduce tures can a¡ect how the energy might be made dead space by pumping intermittently in syn- to do work, or be dissipated as heat, or be con- chrony with the oscillation of induced £ow, an verted to potential energy, such as pressure. A investment that can only be predicted if the na- kelp forest, for example, modi¢es the distribution ture of the driving £ow is known. of energy in the waves passing through it (Fig. 3). Thus, the nature of the external source of Total wave energy is lower in the forest’s lee, as power for extended physiology complicates the indicated by the overall lower energy densities mapping of function onto structure on which there. The reduction in the higher frequency com- good reverse engineering depends. This makes ponents, though, is disproportionate to the reduc- ichnophysiology more di⁄cult, but not intract- tion in the lower frequencies. able. If a trace fossil is embedded in su⁄cient A biogenic structure can enhance turbulence by clues that betoken the energetic milieu in which setting up a competition of sorts between the £u- it existed, such as evidence of turbulence, good id’s momentum (which tends to keep the £uid inferences of function are still possible. £owing in a straight line), and its viscosity (which tends to draw the £uid along the contour of the object in the £ow). Usually this comes about by a 3. A potpourri of extended organisms structure forcing a £uid to abruptly change direction. A ‘moderate’ £ow around a smooth cylinder, This limitation is o¡set, though, by the wealth for example, may be laminar or nearly so, but and diversity of external sources of energy for large £utes or ¢ns on the cylinder may generate powering physiology, which enriches the range turbulent vortices at its edges, the vortices in ef- of structures that could serve as organs of ex- fect being ‘torn away’ by the forces which alter- tended physiology. The best way to illustrate nately impel the £uid to keep £owing in the same this diversity is among the realm of living organ- direction (momentum) and those that draw the isms, both conventional and extended. £uid along the trailing edge of the ¢n (viscosity). Turbulence can also be enhanced by £exible struc- 3.1. Turbulence managers and the modi¢cation of tures that dynamically shape the £uid £owing past landscapes them. Fronds on kelp, for example, undulate as sea water £ow past them, shedding vortices from Turbulent £ow is a ubiquitous feature of natu- their tips.

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cluded frequencies, meanwhile, is converted to dy- namic pressure, which diverts £ow around the barrier. It is noteworthy that turbulence dampers can encompass both bushes (which extrude into the boundary layer) and their topological inverse, ‘bushy networks’ of tunnels or spaces through which £uid can £ow. Mounds of macrotermitine termites, for example, contain within them a retic- ulum of tunnels connecting the subterranean colony with the mound’s porous surface (Fig. 4; Turner, 2000b, 2001). These damp the turbulent winds intercepted by the mound. Movements of air in tunnels just below the mound surface are oscillatory and strongly in£uenced by the £uctua- tions in turbulent winds. In tunnels near the subterranean colony, however, only long-period changes of wind speed in£uence the movements Fig. 3. An energy spectrum showing the dissipation of turbu- of air. lent energy in o¡shore waves by a bed of the macroalga Turbulence dampers can also a¡ect relief Laminaria hyperborea, o¡ the rocky coast of Norway. After around them, which might be preserved as trace Mork (1996). fossils. The best-known example is plants stabilizing sediments or sands in eolian and £uvial envi- Like induced £ow, turbulence enhancement can ronments (Kind, 1992; Buckley, 1987). In such be used to do work that otherwise would have to environments, granules kept aloft by the high fre- be done by muscle power. Sediment feeders, for quency components of turbulent £ow are re-de- example, ordinarily dig through the sediments and posited when a bush damps the energy in these separate the nutrients from the sediment burden. high frequencies. Some structures are more e¡ec- Simuliid larvae (Diptera) use turbulence to do the tive than others: rounded bushes stabilize sedi- job for them (Chance and Craig, 1986). When feeding, they extend the body upward from the lateral substratum, generating a turbulent wake. This connectives lofts nutrient-laden sediments upwards to the lar- va’s mouth, where they are ¢ltered and the food chimney items consumed. Interestingly, these larvae aggre- mound gate while feeding, which generates downstream surface conduit turbulence more e¡ectively than would be the case for solitary individuals, an interesting inter- section between sociobiology and extended phys- fungus radial gardens iology. Such structures might leave lenses of sedi- channel ment excavation in their lee that could be nest galleries preserved as trace fossils. cellar The quintessential turbulence damper is a bushy structure, which constrains £ow to open path- ways between the solid elements of the structure. This tends to exclude energy in the high frequency Fig. 4. Cross section of a mound of Macrotermes michaelse- components of a turbulent £ow, leaving only en- ni, showing the ‘bushy network’ of tunnels within the ergy in the low frequency components to power mound, and locations of the colony and fungus gardens. £ow through the barrier. The energy in the ex- From Turner (2001).

PALAEO 3000 13-2-03 J.S. Turner / Palaeogeography, Palaeoclimatology, Palaeoecology 192 (2003) 15^31 21 ments more e¡ectively than £at bushes, for example (Buckley, 1987). The e¡ects can extend beyond simple particle capture. Tufts of grass in steppe environments, for example, trap both organic and inorganic particles, both of which make their way into the plant. The resulting accumula- tion imparts considerable heterogeneity to the distribution of matter in the steppe (Kelly and Burke, 1997), which persists several months after the death of the grass clump. Foliose lichens similarly draw most of their nutrients from aerosol- ized particles, and their interception can concen- trate minerals in the lichen to a considerable degree (Getty et al., 1999). Turbulence enhancement and turbulence damping can have wide-scale e¡ects on landscapes. For Fig. 5. Management of energy in £ow by kelp. Momentum example, there has long been a debate over the imparted to kelp can do work of stretching the stipe, increas- e¡ects of o¡shore kelp beds on longshore trans- ing its risk of failure. If the frond dissipates some of this port of sands (e.g. Bally, 1987; Kobayashi et al., momentum as turbulent vortices, the elastic deformation of 1993; Elwany et al., 1995; Andersen et al., 1996; the stipe can be lessened. Seymour, 1996). O¡shore kelp forests are popu- larly thought to protect beaches, in the same way the o¡shore £ow to heat: less is therefore able a windbreak protects soil in a ¢eld: by dissipating to power elastic deformation of the stipe, reducing part of the energy in o¡shore waves (e.g. Fig. 3), its risk of failure, and less is available to mobilize sands and sediments are not so likely to be mo- sands from the beach. This raises the interesting bilized by turbulent waves, and so accumulate on question: could the modi¢cation of an ancient the shore. Whether or not a kelp forest actually beach qualify as a trace fossil of the ancient has this e¡ect depends in large part on how the kelp forests o¡shore? kelp manages the energy in the £ow (Fig. 5). Dur- ing a wave-driven surge through the forest, mo- 3.2. Symbiosis and organs of extended physiology mentum will be transferred from the £uid to the kelp, some of which powers elastic deformation of Some biogenic structures power extended phys- the stipe. If stipe deformation is completely elas- iology not only for the creatures that build them, tic, the presence of the kelp forest has no e¡ect on but for other organisms as well, integrating, if you the energy in the waves. As the crest of an o¡- will, two ATP ergonomies. The best-known exam- shore wave passes through, the wave does work ples involve structures that exploit microbially on the stipe, but the energy is recovered when the generated redox potential gradients in sediments wave’s trough passes by: the stipe now does work or soils (Rhoads and Young, 1971; Meadows and on the wave (Fig. 6). Thus, there is no appreciable Meadows, 1991; Fenchel and Finlay, 1994; change in the distribution of wave energy near- White, 1995; Ziebis et al., 1996). Generally, wet shore to a kelp forest compared to an unforested sediments contain within them a highly strati¢ed shore (Fig. 7). Some kelp forests, though, clearly vertical gradient in redox potential (Fig. 8). The do reduce the energy in a passing wave (Fig. 3). gradient arises from a dominance of various com- They do so by turbulence-enhancing devices, like munities of micro-organisms whose composition long fronds, with outlines and sculpturing that varies with depth. Surface sediments are dominat- promote the shedding of turbulent vortices (Bally, ed by obligately aerobic bacteria, protists and 1987; Friedland and Denny, 1995; Hurd et al., meiofauna, while obligately anaerobic methano- 1997). These represent a diversion of energy in gens prevail in deep sediments (Fenchel and Fin-

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organism that controls a ventilatory £ow (Ander- sen and Kristensen, 1991). In many burrow fossils, such activity is marked by ‘halos’ of discol- oration or altered composition of sediments around the fossil (Bromley, 1990). The extent and shape of the halos, being a map of prevailing oxidation potential, o¡ers a window into the extended physiology of the structure.

3.3. Gravity-powered extended physiology

Gravity is another important source of potential energy for organs of extended physiology. A remarkable example involves the feeding behavior of £amingos in tidal mud£ats. A £amingo feeds by stirring up sediments with its feet, which are then processed through ¢lters in the £amingo’s beak. While feeding, the bird’s head is held in one position and the body (along with the treading feet) is rotated about the head. The result is a circular trench with a hummock of ¢ltered silt in the center. When the tide recedes, these trenches retain water throughout the low tide period (Fig.

Fig. 6. Recovery of wave energy by the elastic stipe of a kelp. Details in text. lay, 1994). In between lies an assemblage of metabolic guilds of micro-organisms, including aceto- gens, sulfate reducers, and nitrogen reducers, each occupying sediments corresponding to a particular band of redox potential. Metabolism in such sediments involves passing of electrons from guild to guild along the vertical gradient in redox potential, which is limited by the slow rate of di¡u- sion of electron carriers from one guild to the next in the chain. A biogenic structure, like a lugworm burrow, that spans the redox potential gradient can, by introducing oxygen deep within the sediments, stimulate metabolism in the surrounding sediments. This can redound to the bene¢t of the organism building the structure as well as Fig. 7. An energy spectrum comparing energy in waves on- the organisms associated with it. Metabolism of shore from a bed of the giant kelp Macrocystis pyrifera with the sediments is now controlled not by the slow energy in waves adjacent to the kelp bed. After Elwany et al. di¡usion of microbial metabolites, but by another (1995).

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9). The retention of water, in combination with the birds’ droppings and the anoxic sediments brought to the surface by the bird’s treading feet, supports a £ourishing growth of bacteria, algae, protists and microinvertebrates. At high tide, £amingos return to the trenches to sort the sediments again. Thus, the feeding trenches are persistent structures, essentially £amingo-con- structed ponds irrigated by tides, their productivity powered by the intrusion of the feeding trenches into anoxic sediments. More commonly, gravity powers £uid transport by acting upon density gradients within £uids. The downward £ow of water is an obvious example: even though gravity imparts a downward acceleration to both air and water, it is the water that falls because its density is greater. Natural convection is powered by more subtle variations of density, the most familiar the £ows induced by Fig. 9. Flamingo feeding trenches, located on the tidal mud local heating or altering mixtures of gases or sol- £ats of the Walvis Bay Lagoon in Namibia. (a) Feeding utes. These often support a physiological func- trench following receding of tide. (b) Collection of feeding tion. trenches, showing build-up of topography and retention of water following the receding of tide. (c) Fresh feeding trench, Many biogenic structures interact with gravity showing exposed discolored anoxic muds. (d) Feeding to modify water £ows through soils. Water trans- trenches following an extended period of exposure, showing port through soil is a sort of competition between rich microbial growth. The true color of the water retained its downward acceleration by gravity, and its re- in the trenches is bright yellow-green. Turner (unpublished). tention by matric forces within the soil’s void spaces (‘capillary action’). If soils are ¢nely divid- ed, and the spaces between particles are narrow (that is, the void space is dominated by ‘micropores’), matric forces predominate, so that water in rainfalls is retained in the surface layers of the soil (Childs and George, 1948; Campbell, 1977). This water usually evaporates away rapidly following a rainfall, or is so tightly held that plants or other organisms can extract it only at great metabolic expense. When soils are clumped, on the other hand, and the spaces between particles are wide (that is, the void space is dominated by ‘macropores’), gravity tends to win. Rainfalls in- ¢ltrate rapidly into the soil, and are protected from loss by evaporation. The weak matric forces also mean that water is more readily available to soil organisms (Trojan and Linden, 1992). Earthworms and other soil organisms alter the water economy of soils by retarding or reversing Fig. 8. Distribution of microbial communities and redox po- the course of soil weathering (Hoogerkamp et al., tential in a typical anaerobic sediment. From Turner (2000a). 1983; Joschko et al., 1992; Trojan and Linden,

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1992). Soils normally tend to smaller and smaller solved salts, concentrating them there (Weir, particles as they weather, which results in an in- 1973). Consequently, the presence of termites im- crease over time in the dominance of micropores. parts a variegated distribution of salts in the soils, By their secretion of mucus-laden and calcareous with ‘blobs’ of high sodium, nitrogen, and calci- fecal pellets, earthworms retard or reverse this um interspersed with areas of relative impoverish- tendency, maintaining a dominance of macro- ment (Weir, 1973). pores in the soil. This results in soils with im- Finally, gravity-induced natural convection can proved in¢ltration and aeration, and more ready have interesting e¡ects in the deposition of sedi- availability of water to all soil organisms, both ments and their interpretation. The organic resi- plant and animal. All can have signi¢cant e¡ects due of surface-dwelling planktonic communities on development and maintenance of soil horizons, contributes substantially to marine sediments. as well as on transport of nutrients, minerals and Some marine sediments are strongly laminated, oxidants within soils. All can color the interpreta- which is commonly thought to re£ect episodes tion of soils or tunnels as trace fossils. of high productivity in plankton communities, Gravity-driven density gradients can interact driven by intrusions of nutrients or oxygen with boundary layer gradients in momentum to through, say, upwelling events (Fig. 10a). How- exert subtle, yet broad-scale e¡ects on transport ever, rate of sediment fall is not always deter- of water and minerals in soils. A remarkable ex- mined strictly by the community’s productivity. ample is found among macrotermitine termites, Some phytoplanktonic organisms, like Chaeto- which build large epigeous mounds above their ceros, secrete organic polymers during periods of subterranean colonies (Harris, 1956; Noirot, nutrient stress (commonly at the end of a plank- 1970; Ruelle et al., 1975). These mounds are ton bloom). These aggregate individuals into larg- physiological infrastructure for the colony, in er assemblages, which sediment faster (Grimm et which two sources of energy are integrated to reg- ulate ventilation of the subterranean nest (Lu«scher, 1961; Ruelle, 1964; Turner, 2000a, 2001). On the one hand, the mound intercepts wind energy in the surface boundary layer, using it to ventilate tunnels near the mound’s surface. On the other hand, the tunnels deep within the mound channel a natural convection of spent air upwards from the colony, driven by metabolism-induced variations of buoyancy (Turner, 2000b, 2001). Togeth- er, the two energy sources power ventilation of the colony, which supports oxygen and carbon dioxide £ux rates that are similar to those of a large ungulate herbivore (Darlington et al., 1997). Remarkably, the mound is an adaptive structure, its architecture undergoing continual modi¢cation to match ventilation rates to the respiratory demands of the colony (Korb and Lin- senmair, 1998a,b; Turner, 2000b). Along with the Fig. 10. E¡ect of self-sedimentation on patterning of lamina exchange of respiratory gases, however, the in sediments. (a) When sedimentation rate is simply tied to mound also evaporates considerable quantities planktonic productivity, banding in sediments is a good re- of water. Some of this water originates from the £ection of episodic forcing of the plankton by in£ux of nutrients, oxygen and so forth. (b) When plankton self-aggre- metabolism of the colony: a considerable propor- gate and control their own rate of sedimentation, the tion is drawn from ground water, which ‘wicks’ association between banding in sediments and forcing by cli- toward the colony along with its burden of dis- mate is less clear.

PALAEO 3000 13-2-03 J.S. Turner / Palaeogeography, Palaeoclimatology, Palaeoecology 192 (2003) 15^31 25 al., 1996, 1997; Chang et al., 1998). Laminated original ‘engineers’, it also enables other lineages sediments can result from such episodes of self- to compete for the engineers’ self-generated aggregation rather than any forcing of productiv- ‘niche’ and potentially to replace them (Laland ity by external conditions (Fig. 10b). et al., 1996, 1999; Odling-Smee et al., 1996). Thus, a particular modi¢cation of the environ- 3.4. Species identity and organs of extended ment can persist beyond the lifetimes of individu- physiology als and even the lifetimes of species lineages, akin to Miller’s (1996) conception of ‘coordinated sta- Trace fossils are often named as species, which sis’. I o¡er two examples. implies an association between particular organ- The ¢rst involves the maintenance of reef to- isms and the artifacts left by them. Consequently, pography through an interaction between reef- a trace fossil like Zoophycos, which is likely the building corals, sponges and coralline algae artifact of an interaction between more than one (Wul¡, 1984). The reef’s topography is a balance species, tends to be designated as enigmatic or between the rate of secretion of the calcite base, problematic (Miller and D’Alberto, 2001; Miller, and the rate at which the base degrades, whether 2002). Trace fossils are also commonly associated from wave action, erosion, predation or disease. with activities of individual organisms. Conse- The energy to power calcite secretion comes quently, when that individual dies, or its kind largely from photosynthetic symbionts within the goes extinct, it will no longer leave traces in the coral. Consequently, reefs tend to grow upward, fossil record. toward the light, particularly in tropical waters However, it is no longer clear that modi¢cation where dissolved nutrients are dear. If the reef of the environment, including that which could be breaches the surface, the resulting turbulent preserved as trace fossils, needs to be so strongly wave action accelerates its degradation. This is tied to individuals or species (Miller, 1996). There one reason why reefs tend to equilibrate around is a growing appreciation among ecologists that low tide levels. organisms and assemblages of organisms can act Corals can maintain topography by reducing as ‘ecosystem engineers’, modifying landscapes rates of reef degradation, but other organisms and topographies on ecosystem-wide scales (Jones may play a more signi¢cant role (Wul¡, 1984). et al., 1997). Erosion of a reef generates coral rubble, small Ecosystem engineering has two salient features. pebbles or grains of calcium carbonate (Fig. 11). First, it often involves multispecies assemblages. These accumulate initially at low points on the The mound-building termites of southern Africa, reef, but wave action ensures its ultimate move- for example, are ecosystem engineers of the savan- ment o¡ the reef. However, sponges and coralline na ecosystems they inhabit, modifying landscapes, algae can stabilize the calcite rubble and so main- soil turnovers, carbon £ux rates and mineral dis- tain the reef’s topography. The stabilization oc- tributions on massive scales (Danger¢eld et al., curs in three stages. In loose rubble, cryptic 1998). Their physiological reach is extensive be- sponges penetrate through the rubble’s interstices cause their symbiosis with fungi enables them to and stabilize it in a network of spongin ¢bers. The mobilize energy at high rates to power their ‘en- spongin-stabilized rubble, in turn, provides a sta- gineering’ activities (Darlington et al., 1997; Mar- ble substrate for erect sponges, which, in turn, set tin, 1987; Batra and Batra, 1979). Secondly, the the stage for colonization by coralline algae. results of ecosystem engineering are persistent, the These incorporate the loose rubble into new cal- structural modi¢cations wrought on the environ- cite, which serves as a basis for new coral growth. ment outlasting the organisms that actually bring The reef thus maintains a richer and more varied about the change. This, in turn, sets the selective topography than it would in the absence of these milieu for succeeding generations of organisms. colonizers of calcite rubble (Wul¡, 1984). It is Such ‘ecological inheritance’, as it has been called, useful to note that maintaining the reef is not not only promotes the survival of lineages of the the result of associations of particular species,

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Fig. 11. Scheme of maintenance of reef topography through stabilization of calcite rubble by sponges and coralline algae (Wul¡, 1984). Details in text.

but particular lifestyles: ‘weedy’ cryptic sponges, di¡er considerably from those on surrounding succeeded by erect sponges, succeeded by coral- soils (Fig. 12; Knight et al., 1989; Midgley and line algae, which sets the stage for the coral’s re- Musil, 1990; Esler and Cowling, 1995). In some colonization. If, say, one species of cryptic sponge instances, heuweltjies are active structures (de- competed e¡ectively against another for the task scribed below), although fossil heuweltjies are of stabilizing rubble, the e¡ect of any species turn- also common. over may be scarcely noticeable on the ‘trace’ ^ A heuweltjie gets its start when a patch of the reef topography. ground is colonized by a harvester termite, Micro- The other example is drawn from the terrestrial hodotermes viator, which gathers grass, stems and realm, and involves a landform common in the other plant material from a foraging area, and winter rainfall regions of South Africa. These returns it to the nest (Milton and Dean, 1990). landforms, called heuweltjies (pronounced hew- The centripetal transport of this material concen- vull-key; Afrikaans for ‘little hill’), are regularly trates salts, cellulose and nitrogen at the central spaced hillocks, each 20^30 m in diameter and point of the colony, as it would in any central about 2 m high (Lovegrove and Siegfried, 1989; point forager (Lovegrove, 1991). The subsequent Lovegrove, 1991). Heuweltjies are visually distinc- development of the heuweltjie, however, follows tive because they support plant communities that from a subtle interaction between seasonal and

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Fig. 12. Heuweltjies near Prince Albert, western Cape Province, South Africa. The light coloration of the heuweltjies derives from the green vegetation supported there. geographic patterns of rainfall, soil chemistry and of its distinctive plant communities. Water reten- the adaptations of plants to these patterns. In a tion is aided further by generation of macropores mediterranean climate regime like the Cape of in the soil, both by termites and by the herbivo- Good Hope, winter rainfalls are reliable, albeit rous rodents (notably mole rats) that are attracted sparse in some localities, while summers are reli- to the heuweltjie’s plants. Over the long term, ably hot and dry. Soils in the region also are well- water retention in heuweltjie soils is enhanced per- leached and acidic (Knight et al., 1989; Midgley manently by the development of an impermeable and Musil, 1990; Esler and Cowling, 1995). The calcareous basement layer at depths of 2^3 m Microhodotermes colony ameliorates these envi- (Moore and Picker, 1991), a consequence of cal- ronmental factors in various ways. For example, cite deposition from biogenic production of meth- the localized digestion of cellulose (which, in ad- ane by bacteria in the termites’ intestines, and the dition to being ¢xed carbon, is also ¢xed water) in water in the moister soils. All these factors con- the colony generates an ongoing input of meta- spire to make the heuweltjie a highly persistent bolic water through the year which supplements structure, the same spot being colonized by sub- the intermittent inputs from rainfall. Thus water sequent generations of termites. These, in turn, is more readily available throughout the year on perpetuate the ecological conditions that help the heuweltjie than it is in the surrounding soils. them and future generations thrive. Heuweltjies This, in turn, establishes the conditions for the have been dated to ages of 4000 to 5000 years, heuweltjie’s subsequent development and mainte- with e¡ects that have outlasted signi¢cant climate nance (Fig. 13). On the heuweltjie, plant cover is changes in the region (Moore and Picker, 1991). denser, and the concentration of salts and nitro- Like the coral reef, heuweltjies do not arise or gen there makes them richer, which attracts a persist because of the assemblage of any particu- wide variety of herbivores that further disturb lar species. Microhodotermes is a common player the soil (Milton and Dean, 1990). The termites, in active heuweltjies today, but fossil heuweltjies for their part, are attractive to other animals, like may have been established by other termites, per- aardvark, that disturb the soil to great depths. haps Macrotermes colonies, from a wetter time. The consequence is a eutrophication of the soils Furthermore, the composition of the plant com- on the heuweltjie, which favors the development munities varies signi¢cantly from heuweltjie to

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Fig. 13. Simpli¢ed schematic of water relations in a heuweltjie. O¡-heuweltjie soils in the rainy season do not retain water well, have poor in¢ltration, and a high proportion of leaching runo¡. In the dry season, o¡-heuweltjie soils are dry, but with water ¢xed in the form of cellulose. On-heuweltjie soils retain water better, have better in¢ltration, with leaching prevented by the formation of a calcite basement layer. On-heuweltjie soils are wetter, and water is available throughout the year supplemented by the release of ¢xed water through cellulose metabolism (metabolic water). heuweltjie (Knight et al., 1989; Midgley and Mu- ture of the extended physiology of the various sil, 1990; Esler and Cowling, 1995). In dry re- assemblages. gions, the plant communities on heuweltjies di¡er from those on heuweltjies in more mesic regions. Even within a climate region, the plant commun- 4. What is a trace fossil? ities vary substantially from heuweltjie to heuweltjie, even if the heuweltjie itself is a common fea- Trace fossils obviously are the remnants of past

PALAEO 3000 13-2-03 J.S. Turner / Palaeogeography, Palaeoclimatology, Palaeoecology 192 (2003) 15^31 29 biological activity, but interpreting them properly behavior should necessarily obscure: Miller’s no- seems to require an answer to the question: what tion of trace fossils as collections of ‘behavioral type of biological activity? Certainly, trace fossils tokens’, for example, which divorces the genera- can result from an incidental encounter of organ- tion of trace fossils from particular organisms or ism with environment ^ impressions in fossilized even particular species, o¡ers a broadly compre- mud, tracks, etc. Such fossils can o¡er penetrating hensive and nuanced view of both the generation glimpses into a past life. There is also no doubt and interpretation of trace fossils (Miller and that trace fossils re£ect the preserved remnants of D’Alberto, 2001; Miller, 2002). But is it compre- a purposeful use of the environment by an organ- hensive enough to include, say, sandy beaches as ism, whether for shelter, feeding or some other trace fossils of ancient beds of kelp? purpose. But organisms also modify environments I have to confess that I am not really in a posi- more systematically, sometimes at massive scales, tion to answer this question. As should be ob- managing and driving £uxes of soil, water, nu- vious by now, I am neither an ichnologist nor a trients, and gases through ecosystems, their reach paleontologist, but a physiologist interested in the extending even to the biosphere as a whole (Love- workings of animal-built structures. However, I lock, 1991; Jones et al., 1997). Even if one does would just o¡er the following truisms, which, to not agree with the assertion, made by some, that a physiologist like me, are fundamental, and life is the most important geological force, most which lead me to wonder whether a behaviorist would probably agree that it is at least signi¢cant. approach to trace fossils can be comprehensive And this raises the question: are fossilized rem- enough. First, I o¡er the truism that an organ- nants of this type of biological activity trace fos- ism’s activities will persist only if ¢tness is main- sils? tained or enhanced by the activity. A second tru- The answer depends, of course, on just what ism states that, at root, ¢tness and adaptation biogenic structures represent, whether they be ac- involve the mobilization of matter and energy ^ tive or fossilized. If trace fossils represent simply physiological work ^ to duplicate ‘winning’ var- the remnants of past behavior, then the answer iants among all the members of a lineage. Finally, probably would be ‘no’. The connection between there is a third truism: mobilization of matter and longshore transport of sands, for example, and energy are fundamentally processes not of behav- o¡shore kelp forests does not involve behavior, ior, nor morphology, nor genetics, but of physi- nor does it serve the interests of the kelp in any ology. obvious or untortured way. A rearrangement of Stating these truisms leads me to ask whether a sediments in a fossil burrow, on the other hand, still richer and more nuanced understanding of connects rather directly to behaviors used by an trace fossils might not follow from treating them organism. Thus, one might propose that trace fos- not as behavioral artifacts, but as remnants of sils be distinguished from other biogenic modi¢- past physiology. Certainly, the case is very strong cations of the environment by how straightfor- that extant organisms use the structures they ward the connection is to particular behaviors build as organs of extended physiology, a¡ecting or sets of behaviors by particular organisms. movements of matter and energy through organ- Such an approach has the virtue of focusing isms, assemblages of organisms, ecosystems, and ichnology on a manageable subset of all the fos- the biosphere (Turner, 2000a). There is no reason silized remnants of past interactions of living to believe that structures built by past organisms things with their physical environment. Lenses or their assemblages did not do the same. If so, do that focus can also obscure, however. The man- the artifacts of past physiology qualify as strongly agement of sandy beaches by kelp is a useful ex- as trace fossils as do artifacts of past behavior? ample: suppose kelp do derive some bene¢t by Put another way, is the focal concentration of ensuring they face sandy beaches rather than salts by a termite mound as much a trace fossil rocky shores? There is no intrinsic reason why as, say, a fossil trackway? I think the answer is delimiting trace fossils as the remnants of past clearly ‘yes’: adopting this perspective integrates

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