Measuring the Toughness of Primate Foods and its Ecological Value

Measuring the Toughness of Primate Foodsand its Ecological Value

Peter W. Lucas & Lynn Copes & Paul J. Constantino &

Erin R. Vogel & Janine Chalk & Mauricio Talebi &Mariana Landis & Mark Wagner

Received: 7 March 2011 /Accepted: 5 June 2011 /Published online: 23 September 2011# Springer Science+Business Media, LLC 2011

Abstract The mechanical properties of plant foods play an important role in thefeeding process, being one of many criteria for food acceptance or rejection byprimates. One of the simplest justifications for this statement is the general findingthat primates tend to avoid foods with high fiber. Although fiber is largely tasteless,odorless, and colorless, it imparts texture, a sensation in the mouth related to thephysical properties of foods. All primates encounter such mechanical resistance

Int J Primatol (2012) 33:598–610DOI 10.1007/s10764-011-9540-9

P. W. Lucas (*)Department of Bioclinical Sciences, Faculty of Dentistry, Kuwait University, Safat 13110, Kuwaite-mail: [email protected]

L. CopesSchool of Human Evolution and Social Change, Arizona State University, Tempe, AZ 85287-2402,USA

P. J. ConstantinoDepartment of Biological Sciences, College of Science, Huntington, WV 25755, USA

E. R. VogelDepartment of Anthropology, Rutgers, The State University of New Jersey, 131 George Street, NewBrunswick, NJ 08901, USA

J. ChalkCenter for the Advanced Study of Hominid Paleobiology, Department of Anthropology,The George Washington University, Washington, DC 20052, USA

M. TalebiDepartamento de Ciencias Biologicas, Universidade Federal de São Paulo, Bairro Eldorado,09972-270 Diadema, SP, Brazil

M. LandisPró-Muriqui Association, Parque Estadual Carlos Botelho, São Miguel Arcanjo, SP CEP 18230-000,Brazil

M. WagnerSchool of Engineering and Applied Science, The George Washington University, Washington,DC 20052, USA

when they bite into plant food, and studies on humans show that an incisal bite facilitatesquick oral assessment of a property called toughness. Thus, it is feasible that primatesmake similar assessments of quality in this manner. Here, we review methods ofmeasuring the toughness of primate foods, which can be used either for making generalsurveys of the properties of foods available to primates or for establishing themechanisms that protect these foods from the evolved form of the dentition.

Keywords Fiber content . Methods . Plant cell walls . Primate feeding toughness

Introduction

Little would seem more trivial than biting into an apple. Yet mechanical analyses offirst bites like this started only recently (Osborn et al. 1987; Paphangkorakit andOsborn 1997, 1998; Vincent et al. 1991, 2002) and there is much to learn about therelationship between food physical properties and oral processing that could havegreat relevance to food choice by primates. Despite great interest in the subject,information linking food properties and microstructure to what happens in the mouthis still lacking. Much can be learned not only via in vivo experiment, but also byconducting in vitro tests with models of teeth (Sui et al. 2006), particularly ifcoupled to real-time imaging of the damage they produce. These may help toestablish patterns of failure of foods that work in vivo could verify.

The concept of fiber content plays an important role in the understanding of thefeeding patterns, both of herbivores in general (van Soest 1994) and primates inparticular (Chapman et al. 2004; Ganzhorn 1992; Oates et al. 1990; Wrangham et al.1991, 1998), on the basis of its chemical impediment to digestion. However, fiberalso has a strong effect in a physical context because it imparts toughness (Lucas etal. 2000), which may have general ecological importance in relation to leafconsumption (Onoda et al. 2011). Yet the chemical and physical aspects of fiberbehavior are probably not highly correlated (Choong et al. 1992; Hill and Lucas1996), suggesting a need to examine them separately.

On the chemical side, the nutritional concept of fiber depends principally ondigestibility and includes any relatively indigestible component of the food. Some ofthese compounds offer little fracture resistance, such as pectin (Milton 1991). Theintercellular region can be lignified, but contrary to its reputation, if lignin could beisolated intact, it will not have much fracture resistance because it is akin toadhesives such as phenolic (epoxy) resins (Atkins and Mai 1985). Highly lignifiedwoods are less tough than those with lower lignin content (Lucas et al. 1997). Toattain high toughness, these resins need to be incorporated into a composite togetherwith fibers (in the sense of elongate rods) as in a modern glass- or carbon-fibercomposite. What provides the cell wall with its toughness is not the sum of itsindividual components, but the synergistic mechanisms that only a fiber compositecan create from brittle components. One of these mechanisms is the ability torecover from relatively large deformations without permanent damage. In wood, thisis partly due to the ability of elements of the intercellular matrix, which is a variablemixture of compounds including types of long-chain polysaccharides lumpedtogether as “hemicelluloses” and highly cross-linked lignin, to detach from cellulose

Measuring the Toughness of Primate Foods 599

fibrils when it is loaded. The matrix molecules can then reattach to the fibrils byforming new bonds in a different location so as to adjust the framework withoutdeveloping cracks, somewhat as does Velcro (Keckes et al. 2003). In this way, thetissue adjusts without developing flaws. However, once damaged via a crack,elongated woody cells—those with secondary cell walls—undergo large-scale wholecell buckling that absorbs a great deal of energy obstructing the progress of thatcrack (Gordon and Jeronimidis 1974; Jeronimidis 1980). Thus, structures made ofwood can possess many small flaws, but are perfectly safe unless any of themprogress to a damaging length (Gordon 1978). In modern tough ceramics,microcracking is typical (Evans 1990) and in vitro studies of tooth enamel, abiological ceramic, show that it benefits from the presence of built-in flaws calledtufts (Chai et al. 2009). The key mechanical advantage of composite structures liesin their toughness, in that other properties obey rules of mixtures and are thusrendered suboptimal by combinations of different components (Lucas et al. 2000),but their organization is critical in determining this. The organization of thesecondary cell wall of woody tissue as, for example, around the veins of leaves andin the shells of seeds and some fruits exocarps, yields much higher toughness valuesthan tissues with just a primary cell wall, such as typical fruit flesh or thephotosynthetic tissues of leaves (at the same cell wall volume fraction - Lucas et al.2000).

It is possible that the mechanical aspect of fiber is actually critical in feedingdecisions by primates because it is sensed relatively immediately when food isloaded by the teeth. The resistance of food to an incisal bite in humans is known toinfluence consumer acceptance of foods and seems to depend largely on foodtoughness (Agrawal and Lucas 2003; Ang et al. 2006; Goh et al. 2003; Sui et al.2006; Vincent et al. 1991, 2002). If primates make oral assessments in the manner ofhumans, then it is possible that the toughness of plant items is more strongly relatedto feeding preferences than fiber content (Choong et al. 1992; Hill and Lucas 1996).If so, rather than try to capture the physical effect of fiber via chemistry, it isadvantageous to measure toughness directly. Though there has now been considerablework reported on the fracture toughness of foods consumed by wild primates (Dominy2004; Elgart-Berry 2004; Teaford et al. 2006; Wright 2005; Wright et al. 2008; Vogelet al. 2008, 2009; Yamashita 2003; Yamashita et al. 2009), there is a need to reviewthe methods used to see how they correspond and if there are alternatives.

We can define toughness in 2 ways, both of which describe the intrinsic resistanceof a solid to fracture (Lucas et al. 2008). Here, we define it as the work done inextending a given unit area of crack. We call this quantity R, measured in Joules permeter squared (J m–2). The other definition describes the effect of a crack on thestress field in an object that has linear elastic behavior. Symbolized as T, it is thevalue of a quantity combining the average stress and the square root of crack length(MPa m1/2) at the critical point when the stress is sufficient for the crack to extend.In a linear elastic solid, T is roughly equivalent to (ER) ½, but the relation becomesless tenable in biological structures with more complex behavior. Here we discuss 2levels of mechanical investigation of primate foods. One is designed to obtainestimates of toughness for the purpose of broad generalizations—for the type ofcomparative survey that primatologists often engage in. The other level is morespecific and shows how an understanding of mechanical behavior of foods lies at the

600 P.W. Lucas et al.

frontier of material science methods and analysis and why the interest in biomaterialssuch as foods is currently so strong. One test not discussed is chipping. It differsfrom the tests described here in that the crack is not directed, instead being allowedto find its own path. On heterogeneous orthotropic structures such as woody tissue,this type of “free-running crack” test is often necessary. However, chipping hasrecently discussed in relation to food testing (Lucas et al. 2009) and is also thesubject of another article in this issue (Constantino et al. in press).

Materials and Methods

We tested various turgid parenchyma tissues, the characteristic nutrient-containingtissue of plants, from grape, apple (Red Delicious), and papaya flesh, and also turnipcortex to illustrate patterns in toughness with the different techniques. We tested thegrape tissue with wedge and wires. For turnip cortex, we produced slices of 0.2–2.5 mmthickness with a razor blade for scissors tests to compare with wedges. For apple, wetested the specimens with all techniques without skin, but also with it to produce abilayered specimen. In addition, we also tested pieces of (dried) prune with skin. In alltests, the testing direction was radial, with fracture directed toward the fruit center.

Wedge Test

This test dates back to the earliest experiments in fracture mechanics (Lawn 1993)and has been employed successfully in food research for about 20 years (Vincent1990; Vincent et al. 1991; Khan and Vincent 1993, 1996). The usual geometry insuch tests is shown in Fig. 1 and requires a block of tissue underneath a sharpwedge, broader than block width and directed across that dimension. When presseddownwards, the wedge tip initiates a crack. The initial force peak at initiation is notimportant and the test is often best started after the crack is initiated (Fig. 1a). Beyond thispoint, the crack propagates slowly through the block, pushed by the wedge forcing thecrack walls apart. The crack tip advances just ahead of the tip of the wedge, generallygrowing at the same rate and thus controlled. The type of force recorded is shown inFig. 1b. The wedge must be stopped before the crack reaches the lower surface of theblock. Then it is reversed to the point at which the test was started and a second runmade, identical to the displacement of the first (Fig. 1c). The force involved in thissecond pass will be low, involving excess energy imparted to the crack walls inbending and friction. The second force trace is then deducted from the first to give theeffective work done (shaded in Fig. 1d). Suppose this subtraction to be a reasonablyconstant wedging force Fwedge. Then, with crack dimensions w (the block width) and d(crack depth), the toughness is R = Fwedged/wd. The numerator Fwedged gives the workdone, while wd gives the crack area; this simplifies further to R = Fwedge/w. The testshere used a stainless steel wedge of 15° included angle.

Wire Test

This is a newer test, with features in common with the wedge, but offeringpotentially more information about food response (Kamyab et al. 1998). It involves


drawing a taut wire of submillimeter diameter through a tissue block (Fig. 2a). Thisinitiates a small crack below the wire. Provided that the wire remains taut, theapparent toughness is then calculated just as with wedging with R = Fwire/w . Theword apparent here means that no second pass is made through the cracked block.Instead, there is a theoretical method that both accounts for friction and improves theresolution of the wire method in determining fracture resistance (Goh et al. 2005).The 1-pass test can be repeated with wires of different diameter and the resultingapparent toughness values plotted against wire diameter (Fig. 2b). The generalexpectation is that of a gradient (Fig. 2c), which can be extrapolated to an intercepttoughness that could be obtained with a (fictive) 0-diameter wire. This interceptvalue is an estimate of the essential work of fracture independent of wirecharacteristics. In the tests reported here, wire diameters of 0.15, 0.25, and0.65 mm were employed.

Scissors Test

This is but one version of a number of tests designed to obtain the toughness ofmaterial in sheet or rod form, such as leaves or petioles (Ang et al. 2008; Aranwelaet al. 1999; Edwards et al. 2000; Henry et al. 1996; Lucas and Pereira 1990; Lucaset al. 1991, 2011; Onoda et al. 2008; Read and Sanson 2003; Sanson 2006; Vincent1992; Wright and Cannon 2001; Wright and Illius 1995). All such methods dateback to Atkins and Mai (1979), who showed that toughness estimates could beobtained by the guillotining of thin sheets of material. Onoda et al. (2011)demonstrate that most of the methods that ecologists use give reasonably comparable

Fig. 1 Wedging requires 2identical passes through a foodblock of width w whileregistering the force F. In (a),the test is started within theblock with the force-displacement in the first passrecorded as in (b), where thework done is the shaded area.The wedge is then reversed as in(c). The second ‘empty’ passfollows the same course to pro-duce a second force trace. Thework in doing so is deductedfrom that needed to fracture thematerial, giving work necessaryfor fracture by subtraction(shaded).


results. A standard scissors test involves food in the form of a sheet or rod, usuallyless than 1 mm in thickness, placed between the blades of a pair of scissors (Fig. 3).The crosshead of the tester drives the blade handle down with the load monitored atthe same point to make a cut over a given displacement. As with wedging, thescissors are then returned to their original position and the specimen removed. Thescissors are then driven down again over the same displacement, recording thefrictional work done between the blades themselves. The work done in this emptypass will be substantially greater than in wedging because the blades actually

Fig. 2 In (a), a taut wireis passed through the foodblock of width w giving aforce-displacement plot such asshown in (b). In (c), repeat testswith wires of different diametersideally give an intercept valuefor a wire of 0-diameter.

Fig. 3 Scissors test setupallowing their easy removal forcleaning of the blades. Ideally,the specimen should be taped tothe specimen support on eitherside of the blades to reduceextraneous work. The rollercontains ball-bearingsminimizing friction (and thuswork losses) against the bladehandle.


damage each other (Atkins and Mai 1979), but assuming that this workapproximates that done in fracturing the specimen, then deducting this from thework done in the first pass gives the work of fracture. All that remains then is tomeasure the cut length and its thickness, dividing these into the work done infracture to get a toughness estimate. Most often, the tests are run the other wayaround, with the empty pass done first. Regardless of the sequence of cuts though,the scissors blades must be cleaned before the test (never between the cut and emptypass) to get accurate results. In the tests reported here, we used cobalt-chromescissors (Dovo, Solingen, Germany).

Results

Toughness estimates on turnip cortex using scissors and wedges are compared inFig. 4. The wedge gave a mean toughness of 420 Jm–2 (SD 130 Jm–2). Forsections <1.0 mm in thickness, the scissors underestimated these values, but theyincreased with thickness. For sections >1 mm thickness, scissors produced valuessimilar to the wedge tests, but with greater variability. For grape and papaya flesh,the apparent toughness measured with the wire test declined with wire diameter(Fig. 5a, b), but wedge tests appear to give lower values than wires, approximatingthe intercept toughness (Fig. 5b).

The toughness of apple flesh alone averaged 204.2 Jm–2 (SD 59.5 Jm–2) with awire of 0.25 mm diameter. Both wedge and wire had no difficulty fracturing theflesh (Fig. 6a, b). However, when a block topped with apple skin was provided,wires of 0.15–0.65 mm diameter failed to break though the skin without permanentlybending. Instead of the skin fracturing, the major events were bursting cells in theunderlying flesh (Fig. 6c). In contrast, wedging proceeded without difficulty,breaking the skin first, followed by the flesh. When we tested flaccid (dried) fruit,there was wholesale collapse of the flesh, again without skin fracture (Fig. 6d).

Fig. 4 Toughness values obtained from scissor tests (filled circles) on slices of turnip tissue of giventhickness compared to the mean (horizontal dashed line) ±1 SD (shaded) from wedge tests. Up to ca.1 mm section thickness, results with scissors lie mostly below wedge values, depending on sectionthickness.


Fig. 5 (a) Plot of apparent toughness versus wire diameter for the flesh of grapes. The data points (opencircles) showed considerable variation, but average toughness (black circles with standard deviation bars)clearly depends on diameter. (b) Field tests on ripe papaya for 2 wire diameters (circles) versus the mean(dashed line) ±1 SD (shaded) from wedge tests.

Fig. 6 Top row shows tests on apple flesh. (a) A frame from a real-time microscopic video recordingshowing a wedge (15° included angle) penetrating easily. Scale bar=2 mm. In (b), a wire of 0.25 mmdiameter on the same food material also fractures flesh easily. Bottom row shows the effect of anadditional overlying fruit skin. In (c), a wire of 0.65 mm test bends against the skin of a bilayered applespecimen, causing collapse of the underlying flesh (expressed juice is running down the side of the block)without breaking the skin. In (d), a test on dried fruit (prune) magnifies the collapse of the flesh due to theflaccidity of its cells.


Discussion

The simple experiments above suggest that there will be inevitable discrepanciesbetween toughness estimates made by different investigators dependent onmethodology. One of the key influences is probably tissue thickness. It is a generalfinding that the properties of cellular solids depend on the ratio of cell size tospecimen thickness (Ashby et al. 2000), with the recommendation that specimens beat least seven cells thick to obtain properties that typify bulk tissue. In plant tissues,tissue thickness needs to be at least ca. 1.0 mm for this criterion to be filled (Lucas etal. 2000). Leaves are mostly much thinner than this unless they are succulents(Choong et al. 1992). Thus, when leaves are tested in stacks, the calculatedtoughness rises with accumulated thickness (M. F. Choong, cited in Lucas 2004).However, the toughness of leaves as estimated by scissors, or any other kind ofbladed test (Onoda et al. 2011), is not wrong: the estimate is indeed the toughness ofthat leaf. However, what the test result may not predict is the resistance a primatemight perceive if the leaf were to be folded, or leaves were to be stacked, duringchewing (Byrne and Byrne 1993; Tonooka 2001).

When food can be shaped into a block, wedge or wire tests are preferable toscissors. The wire test is preferable to wedging in theory because it takes accountof the variable sharpness of the wire and because the slope of the toughness–diameter plot (Fig. 2c) can give information on yielding behavior (Goh et al.2005). However, it looks extremely difficult in practice to obtain such informationaccurately in the field. Grape flesh is easy to work with compared to the flesh ofwild fruits. However, no reliable gradient could be calculated in Fig. 5a, not somuch because of the quantity of wire diameters available, but because of the datascatter. The tests on papaya flesh (Fig. 5b) were conducted in the field at ParqueCarlos Botelho, Saõ Paulo (Brazil), where attempts to use the technique on fruitsconsumed by Brachyteles arachnoides failed. In contrast, wedge tests wererelatively straightforward.

The wedge is attractive for many reasons other than its calculation. For one thing,it teaches exactly why toughness has nothing to do with stress levels per se. Thewidth of the block, which determines the stress needed to bend the crack faces awayfrom each other, makes no difference to the test result. In fact, there is no need tomeasure any dimension precisely other than the block width, which needs to haveparallel faces for this purpose. The test does not begin on the upper surface of atissue block, so this does not need to be flat, and can be adapted to smallerspecimens (only 2 mm in height) than a wire test. In practice, the crack may arrestduring wedging because of structural variations within the material, needing to bereinitiated by the wedge tip. However, this can be employed profitably to establish atoughness gradient in food (Dominy et al. 2008). Friction is often low with fruitflesh, but the test becomes more difficult when friction is high and material startsto adhere to the wedge. Even so, there are practical ways to reduce friction (usingWD-40 or mineral oil).

Most of the aforementioned details are probably unimportant for the purpose of abroad survey of the toughness of primate foods. For example, in a broad ecologicalcontext, mechanical measurements of leaves made with completely differentmethods can be compared without disturbing patterns within a large database


(Onoda et al. 2011). However, for the purpose of discerning the mechanisms bywhich plant tissues resist fracture under incisal (Agrawal et al. 2008; Deane 2009) ormolar (Lucas 2004) loading, such details are very important. Tests that measure partsof a food item in isolation may not tell much about how the whole structure behaves.In a bilayer, fractures are more likely to initiate on the outer surface if the contact issharp, i.e., of very small radius, but instead involve subsurface fracture if the contactis spread over a wider area (Lucas et al. 2008). The tests on apple flesh involving skindescribed here show this pattern. A sharp wedge (radius of blade curvature <10 μm)initiates surface fracture, but even the thinnest of the wires (radius of curvature 75 μm)produces subsurface collapse instead. This might explain why captive long-tailedmacaques, lacking sharp blades on their molars (Kay 1975), employ more musculareffort to chew apple flesh that contains skin (Hylander et al. 1992), in addition to thereported difference in toughness between skin and flesh (Williams et al. 2005). Goingfurther with the bilayer analogy, a mature leaf is a mechanical sandwich (Gibson et al.1988) with stiff outer epidermal layers on top of what is largely very thin cell-walledparenchyma. Many primates might target very young leaves, despite their higher levelsof deterrent secondary chemicals (Coley 1983; Coley and Kursar 1996), because theseleaves have not yet differentiated their epidermis and are thus not yet layered structures.These would be far easier for a primate that lacked bladed molars to fragment than olderstructured leaves that only leaf specialists with bladed molars could manage.

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Documents

Measuring the Toughness of Primate Foods and its Ecological Value