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Plant morphologyand recruitmentof the third trophic level: subtle and little-recognizeddefenses? Robert J. Marquis, Dept of Biology, Univ. of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, MO 63121-4499, USA and Christopher Whelan, The Morton Arboretum, Lisle, IL 60532, USA

We present the new hypothesis that plant morphological traits that make plants more accessible to predatorsand parasitoids (in contrast to attracting them) may be shaped by the third trophic level. We review data that demonstrate selective impacts of the third trophic level, other than ants and mites, on plant fitness. This third trophic level impact comes about because predators and parasites reduce damage caused by herbivores of those plants. Because of this impact, we suggest that there may be selection for changes in plant morphological traits that make herbivoresmore accessible to the third trophic level. Both invertebrate and vertebrate members of the third trophic level may be involved, potentially influencing such traits as pubescence type and density, leaf morphology, canopy density, perch and stem shape, branching angles, and distance between leaves and perches. Such influences may have been previously overlooked because: 1) there has been little investigation of third trophic level impacts on plant fitness other than by predatory ants and mites; and 2) changes in plant morphology that make plants accessible to the third trophic level are likely to be subtle.

For plant-herbivore systems, impacts of the first trophic level on the third trophic level have been explored both theoretically and empirically (Price et al. 1980, Price 1986, 1992, Hunter and Price 1992, Rowell-Rahier and Pasteels 1992). However, potential 'top down' effects of predators and parasites on plant traits are less well known. One clear example of the evolutionary impact of the third trophic level on the first trophic level is the production by plants of novel traits (e.g., extrafloral nectaries or domatia) that result in the defense of plants by predatory arthropods, either ants (e.g., Janzen 1966, Letourneau 1983, Koptur 1985, Kelly 1986, Schupp 1986) or mites (O'Dowd and Willson 1989, O'Dowd et al. 1991). Ants (Huxley and Cutler 1991) or mites (Grostal and O'Dowd 1994) molest or kill the plant's herbivores or remove their eggs. Such impact on the herbivores has been proposed (mites: O'Dowd and Willson 1989) or demonstrated (ants: Huxley and 330

Cutler 1991) to reduce herbivory and increase growth and reproduction of the plant. In return, the plants produce food and/or provide shelter for the ants and mites. The evolutionary legacy of interactions between plants, herbivores, and ants and mites are novel, and sometimes large structures. In the extreme, these structures include extrafloral cup nectaries up to 7.4 mm in diameter (e.g., Pithecellobium macradenium) (Elias 1972); groove extrafloral nectaries which run the length of a leaf petiole (up to 15 cm) (as in Ochroma pyramidale) (O'Dowd 1980); special pads in leaf axils that produce food (Muillerian)bodies in Cecropia (Janzen 1969); hollow pockets in leaves or stems that provide shelter to ants as in Clidemia and Topobaea (Davidson and McKey 1993); and tissue pockets or tufts of trichomes in vein axils that provide shelter to mites (O'Dowd and Willson 1989). The hypothesis is that plants have evolved such traits to attract ants (Bentley 1977) and mites (O'Dowd and Willson 1989) to the plants, and to retain them on the plant once they have been attracted. More detailed observation and experimentation in ant-plant interactions has demonstrated that the degree of protection provided by ants varies by microhabitat and ant species (e.g., Horvitz and Schemske 1990). Despite this variation, there is general acceptance that ant-defense of plants has been a significant force in the evolution of plant traits (McKey 1984, 1989, Beattie 1985, Benson 1985, Huxley and Cutler 1991). In the scheme of plant defense classification, plant traits that reinforce ant and mite visitation by providing food and/or housing are treated synonymously with biotic defense. However, evidence is accumulating to suggest that other members of the third trophic level may also select for plant morphological traits. Modifications of plant morphology that make the herOIKOS 75:2 (1996)

bivores of plants more accessible to parasitoids, or to vertebrate and invertebrate predators, may increase plant fitness. The result of selection on plant morphology by the third trophic level may be manifested in subtle modifications of branching pattern, twig length and thickness, and foliage density, morphology, and distribution, all of which are much less obvious than the novel structures evolved in plants to attract ants and mites. Such changes in morphological traits make the herbivores of plants more accessible to predators and parasitoids. Increased accessibility could result from either increased encounter rates and/or decreased handling time. In contrast, the novel structures described above actively attract such predators (and in some cases, parasitoids: see below), and increase their fidelity or retention on the plant. Traits that increase accessibility might also increase retention of invertebrate predators if accessibility leads to increased encounter rates and/or decreased handling times. If it can be shown that members of the third trophic level other than ants or mites influence plant traits, then we need to expand our view of biotic defenses, third trophic level impacts on the first trophic level, and potential plant mutualists. Our objective with this communication is to review available evidence that members of the third trophic level besides ants may have evolutionary impacts on plant morphological traits through indirect effects on plant fitness. Plants vary in heritable, morphological traits. Some of these traits affect the efficiency with which third trophic level foragers capture second trophic level enemies of plants. Those plants that have morphologies that enhance encounter rates and/or decrease handling time of third trophic level predators on second level consumers, will have increased growth rates and elevated reproductive success. Therefore, plants with these morphologies will become more common in the population at the expense of those plants with morphologies that lead to decreased efficiency of third trophic level predators. The steps necessary to demonstrate such an influence include: 1) decreased plant fitness in the presence of herbivores due to their feeding on plant tissue; 2) increased plant fitness in the presence of the third trophic level due to its negative impact on herbivore feeding (and therefore, positive influence on plant growth and reproduction); and 3) a causal relationship between variation in a plant trait (or set of traits) and the magnitude of impact of the third trophic level on herbivore feeding on the plant. Finally, in order to establish the likelihood of an evolutionary response to selection imposed by the third trophic level on a plant trait, 4) a heritable basis for intraspecific variation in that plant trait must be demonstrated. OIKOS 75:2 (1996)

Preliminary evidence: third trophic level impacts of birds on fitness of Quercus alba From 1989-1991, we conducted an experiment to determine the effect of insectivorous birds on fitness of white oak saplings (Quercus alba) in the Missouri Ozark Plateau (Marquis and Whelan 1994). We compared herbivorous insect abundance, subsequent leaf damage, and plant growth between control saplings and saplings which were enclosed in cages to reduce access by insectivorous birds. During both the 1989 and 1990 seasons, the total number of insects inside of cages compared to control trees over the season was doubled. As a result, damage doubled in 1989 (mean 26% versus 13%) and increased by one-third in 1990 (mean 34% versus 26%))for caged versus control trees, respectively. Growth (total twig and leaf biomass) was decreased by one-third in cage versus control plants over the twoyear study period. Greater leaf biomass will increase the total photosynthetic potential of the plants, and eventually, because of increased carbon assimilation, their ability to reach the canopy and reproduce. These results satisfy criteria 1) and 2) and suggest that insectivorous birds may be selective agents for plant traits that facilitate bird foraging. Greater damage to caged plants than to control plants suggests white oak saplings which enhance the foraging ability of birds more than others should have reduced herbivore loads, and as a result, increased growth. Insectivorous birds are known to forage preferentially on certain plant species that differ with respect to foliage characteristics (Balda 1969, Franzreb 1978, Holmes et al. 1979, Holmes and Robinson 1981, Robinson and Holmes 1984, Airola and Barrett 1985, Holmes and Schultz 1988, Peck 1989), but there are no reports of birds showing foraging preferences among individual plants of the same species. However, evidence demonstrating differential foraging within plants by birds (Holmes et al. 1979, Pierce and Grubb 1981, Holmes 1986, Whelan 1989) suggests that birds have the potential to discriminate among plant conspecifics. Differential foraging within a plant is likely a product of both differential prey distribution (Heinrich 1979, Bergelson and Lawton 1988) and variation in plant traits that influence foraging (Whelan 1989). In an experiment in which prey type. abundance and distribution were controlled, Whelan (1989) demonstrated that plant traits do contribute to differential bird foraging, suggesting the plausibility of criterion 3. For example, both Dendroica caerulescensand D. virens demonstrated foraging preferences for foliage of sugar maple, Acer saccharum, distal as opposed to proximal to the trunk. Perch diameter and distance to foliage from perches (Levey et al. 1984, Whelan 1987, 1989), as well as foliage density (Pearson 1975, Greenberg 1984) are plant traits that likely affect bird foraging ability within plants and thus their preference for one plant over another. White oak 331

has extremelyvariable twig sizes and lengths within fensessuch as plant pubescence,as suggestedby Spiller plants(R. J. Marquisand C. J. Whelan,unpubl.)which and Schoener(1990), it seems entirelylikely that they could accomodatebirds in a wide range of body sizes. may cause selectionon plant architectureas well. Potentially,these traits could be modifiedby selection. Predatory fish Other systems Predatory and parasitic insects

Indirect selection by predators on plant traits also could be occurringin aquaticsystems.It is in aquatic systems that true "trophic cascades" (sensu Strong 1992) occur, i.e., in which experimentalremovalof a higher trophic level results in virtual clearing of the substrateof plant biomass(Poweret al. 1985,Mengeet al. 1986a,b, Power 1990). This suggests that there should be strongselectionon plantsto be accessibleto the third trophic level, i.e., the enemies of the plant enemies.However,the possibilityof a trophiccascade need not be a necessarypreconditionfor such selection to occur. Even underlower herbivorepressure(that is, in the absenceof a trophiccascade),such selectionstill may be occurring.For example, snail abundanceincreaseswith aquaticmacrophytediversityin ponds of southernSweden(Br6nmark1985)and increasedcomplexity of macrophytearchitectureseems to provide safe haven for snails from their fish predators(Covich and Knezevic1978).In this case, therewould be selection on the plant for both decreasedcomplexity(decreasein enemy-freespace) and increasedsimilarityto otherplantspecies,so that once predatorsand parasites learn the hiding sites of one species, this information can be appliedto all plant species.

Gomez and Zamora(1994) demonstratedrecentlythat seed predationby a bruchidbeetle on the woody crucifer Hormathophylla spinosawas increasedfrom 20%to 43% when the parasitoidsof the beetles were experimentallyexcludedfrom plants. Criteria1) and 2) have been demonstratedfor this system. Foraging by both parasitoids and predatory insects are known to be influencedby plant morphology;leaf density affects Coccinellaladybird beetle foraging (Kareiva and Sahakian 1990), density of trichomesor glandularhairs can affect the movement of parasitoids and insect predators(Obryckiet al. 1983,Kauffmanand Kennedy 1989,Southwood1986),and leaf slipperinessand shape can affectforagingabilityof coccinelids(Grevstadand Klepetka 1992). Therefore,we might expect selection for plant traits that increaseaccessibilityto the plant's herbivores for predaceous and parasitic insects. In essence,such selectionreducesthe "enemy-freespace" (Lawtonand Strong 1981,Gross and Price 1988)available to the herbivore.Leaf density (Kareivaand Sahakian 1990), trichomeabundance(Southwood 1986), and leaf slipperiness(Wayand Murdie1965)are known to have a geneticbasis, and thus criterion4) is met for these systems.Evolutionof certaintraits may be conConclusion strained:for example, decreasedtrichome abundance may not only make leavesmore accessibleto arthopod We propose that plant morphologicaltraits are under predatorsbut also to their prey (herbivorousinsects). indirectselectionby the thirdtrophiclevel for increased accessibilityof predatorsand parasitesto the plant's herbivores.The most obviousexampleof an evolutionary impactby the thirdtrophiclevel on plantsare traits Anolis lizards associated with the attraction of ants and mites as Spillerand Schoener(1990)have demonstratedthat leaf biotic defenses.Theseexamplesare obviousbecausethe damageto Conocarpuserectus(buttonwood)increased plants have evolved unique, specializedmorphological when plantswere caged (satisfyingpartiallycriterion1) structureswhichincreasethe fidelityof the thirdtrophic and thus unavailableto foragingAnolislizards.More- level participantsto the plants.Similarly,selectionmay over, Schoener(1987, 1988) found a negative correla- be acting on other morphologicaltraits to allow the tion betweenpresenceof Anolis lizards and degree of predator or parasite better access to its prey and/or pubescencein Conocarpus: plantswere more pubescent increaseits ability to find its prey. The relevantmoron islandswithoutlizards.Together,these data suggest phologicaltraitswhich serve to make plants accessible that on islandswith lizards,leaf damageis reducedby to predatorsand parasitoidsinclude pubescencetype theirforagingbut in theirabsenceplantsmust investin and density, canopy density, perch and stem shape, defense(i.e., plant hairs:Schoener1987).The abilityof branching angles, and distance between leaves and Anolislizardsto forage is influencedby plant morpho- perches.In a few instances,accessibilitytraitsand traits logical traits (Moermond1986), includingtwig diame- that attractthe thirdtrophiclevelmay act in antagonister and length, branchingangles,and distancebetween tic or synergisticways on the predatoror parasitoid twigs. Given that lizardsmay modify plant responseto species.For example,accessibilityof predatoryants to selectionimposed by herbivoresfor morphologicalde- plantswhich produceextrafloralnectarto attractthem 332

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can be restricted by the type and density of plant Balda, R. P. 1969. Foliage use by birds of the oak-juniper woodlandand ponderosapine forestin south-easternAritrichomes (Davidson et al. 1989, Davidson and McKey zona. - Condor71: 399-412. 1993). In turn, parasitoids may be attracted by the Beattie, A. J. 1985. The evolutionaryecology of ant-plant mutualisms.- CambridgeUniv. Press,Oxford. production of extrafloral nectar (Hespenheide 1985, W. W. 1985.Amazonant-plants.- In: Prance,G.H. Benson, their will be influKoptur 1985), yet foraging ability and Lovejoy,T. E. (eds), Key environments:Amazonia. enced by a combination of morphological features of PergamonPress,Oxford,pp. 239-266. the plant. Bentley,B. L. 1977. Extrafloralnectariesand protectionby pugnaciousbodyguards.- Annu. Rev. Ecol. Syst. 8: 407Escape from natural enemies has been proposed to 427. be important in determining how herbivorous insects Bergelson,J. M. and Lawton,J. H. 1988.Does foliagedamage influencepredationon the insect herbivoresof birch?exploit potentially available plant resources (see Ecology69: 434-445. Bernays and Graham 1988, Fox and Eisenbach 1992). E. and Graham,M. 1988.On the evolutionof host We should not, however, expect plants to be passive Bernays, specificityin phytophagousarthropods.- Ecology 69: players in the triangle. Just as there is hypothesized 886-892. selection on herbivores to find "enemy-free space", Brbnmark,C. 1985.Freshwatersnaildiversity:effectsof pond area, habitatheterogeneityand isolation. - Oecologia67: there should be selection on plants to reduce such 127-131. space. For a generalist predator or parasitoid that visits Covich,A. P. and Knezevic,B. 1978. Size-selectivepredation by fish on thin-shelledgastropods(Lymnaea);the signifimany different plant species, selection could actually canceof floatingvegetation(Trapa)as a physicalrefuge.result in convergence in the relevant plant morphologiVerh.Int. Ver. 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