Bare, simplified searching environments, often associated with sparsely vegetated harsh soils, may cause both plant and animal inhabitants to be apparent and conspicuous. "Apparency" has been a key concept to explain the diversity of plant defensive chemistry but has been difficult to test. In animals, there is extensive work on camouflage and crypsis, adaptations to apparency that reduce detection by predators. Here, we explore apparency as a challenge in bare soil habitats characterized by sparse vegetative cover for both plants and animals. Using experiment and observation, we show that attack rates from enemies on vulnerable plants and undefended caterpillar models are greater in barer serpentine habitats than in adjacent more vegetated ones. Palatable Streptanthus species (Brassicaceae) may have adapted to apparency with a crypsis defense, typically considered the purview of animals. In Streptanthus breweri, leaf color is locally matched to soil outcrop color, and experimental mismatching of leaf and substrate color increases damage to plants, suggesting adaptation to apparency per se. Herbivore coloration may, too, have been influenced by greater enemy pressure and apparency in these sites. Adaptation to increased enemy pressure and apparency, with concomitant trade-offs in competitive ability, may be an underappreciated aspect of specialization to harsh soils, especially in plants. Apparency may be a useful framework for understanding trade-offs driving soil specialization and global biodiversity patterns.

Plant soil specialists contribute greatly to global diversity; however, the ecoevolutionary forces responsible for generating this diversity are poorly understood. We integrate molecular phylogenies with descriptive and experimental ecological data, creating a powerful framework with which to elucidate forces driving soil specialization. Hypotheses explaining edaphic specialization have historically focused on costs of adaptation to elements (e.g., nickel, calcium/magnesium) and accompanying tradeoffs in competitive ability in benign soils. We combine in situ microhabitat data for 37 streptanthoid species (Brassicaceae), soil analyses, and competition experiments with their phylogeny to reconstruct selective forces generating serpentine soil endemism, which has four to five independent origins in this group. Coupling ancestral state reconstruction with phylogenetic independent contrasts, we examine the magnitude and timing of changes in soil and habitat attributes relative to inferred shifts to serpentine. We find large changes in soil chemistry at nodes associated with soil shifts, suggesting that elemental changes occurred concomitantly with soil transitions. In contrast, the amount of bare ground surrounding plants in the field (“bareness”), which is greater in serpentine environments, is conserved across soil-type shifts. Thus, occupation of bare environments preceded shifts to serpentine, and may serve as an evolutionary precursor to harsh elemental soils and environments. In greenhouse experiments, taxa from barer environments are poorer competitors, a tradeoff that may contribute to soil endemism. The hypothesis of occupation of bare habitats as a precursor of soil specialization can be tested in other systems with a similar integrative ecophylogenetic approach, thereby providing deeper insights into this rich source of biodiversity.

SummaryWe explored macroevolutionary patterns of plant chemical defense in Streptanthus (Brassicaceae), tested for evolutionary escalation of defense, as predicted by Ehrlich and Raven's plant-herbivore coevolutionary arms-race hypothesis, and tested whether species inhabiting low-resource or harsh environments invest more in defense, as predicted by the resource availability hypothesis (RAH).We conducted phylogenetically explicit analyses using glucosinolate profiles, soil nutrient analyses, and microhabitat bareness estimates across 30 species of Streptanthus inhabiting varied environments and soils.We found weak to moderate phylogenetic signal in glucosinolate classes and no signal in total glucosinolate production; a trend toward evolutionary de-escalation in the numbers and diversity of glucosinolates, accompanied by an evolutionary increase in the proportion of aliphatic glucosinolates; some support for the RAH relative to soil macronutrients, but not relative to serpentine soil use; and that the number of glucosinolates increases with microhabitat bareness, which is associated with increased herbivory and drought.Weak phylogenetic signal in chemical defense has been observed in other plant systems. A more holistic approach incorporating other forms of defense might be necessary to confidently reject escalation of defense. That defense increases with microhabitat bareness supports the hypothesis that habitat bareness is an underappreciated selective force on plants in harsh environments.

How easy a plant is to find, or its apparency, is thought to shape plant defenses. Recent meta-analyses suggest that the types of plant defenses employed are not well-predicted by apparency, or apparency can be confounded with life history traits like woodiness and stature. Here, we suggest that the searching environments in which plants grow also influence plant apparency and should thus affect investment in plant defense. Specifically, bare, unvegetated environments may result in greater apparency of inhabitants of all statures to enemies, as a result of loss of associational resistance. We make several predictions about plant defenses in simple searching environments. (1) Plants living in simple searching environments should be more highly defended than plants living in more vegetated, complex searching environments. (2) Plant defenses involving signals-both, signals serving to hide plants and aposematic signals-should be favored in simple searching environments. (3) Levels of damage from enemies in simple searching environments should be related to defensive strategy (resistance, aposematism, mimicry, or crypsis); apparent plants should have low damage, because, as they are easily found, they should be well-defended though physical or chemical defense. In contrast, predictions about damage levels in cryptic plants are harder to make, as damage reflects both whether plants are encountered or not, as well as overall palatability. If crypsis is favored in more palatable species, as has been suggested previously, we predict that cryptic plants should have greater variance in damage and greater maximum damage, if, once found, plants are palatable. (4) Organisms from diverse evolutionary lineages inhabiting the same simple searching environments should adapt to selection from apparency by converging on similar background matching or aposematic defenses. We then test some of these predictions with descriptive data collections in two simple searching environments: largely unvegetated graywacke scree mountaintops of New Zealand and serpentine barrens of northern California (USA). We find that plants that are more apparent (i.e., do not match local rock color as measured across 300-700 nm wavelengths) are more defended, as inferred from mean damage received. In contrast, cryptic species in the same habitats get 79 more heavily damaged, once found, suggesting overall greater palatability. There was no evidence of greater variation in damage, as measured by coefficient of variation, but maximum damage was much greater on cryptic species in both habitats. Convergence on gray substrate is found in diverse species of plants in New Zealand, as well as by scree-living grasshoppers; in California, grasshoppers have also converged on substrate color, and seed color of a non-cryptic plant also matches local outcrops. Considering searching environment and enemy searchingabilities when evaluatingplant apparencytoenemiesmay shed more lightonthis challenge to plants.