Succession and climatic stochasticity induce long-term decline of a forest browser.

Removal of predators and creation of early seral habitat have, in many systems, caused substantial population growth of herbivores. Hyperabundant herbivores, in turn, induce cascading ecosystem effects, but few studies have investigated long-term browser density trends in relation to succession and stochastic climate events. Here, we use annual, empirical population estimates of a forest browser to relate forest succession to long-term decline of an herbivore that prefers early seral habitat. From 2007-2021, concurrent with reduced timber harvest, we used line-transect distance sampling to document annual changes in Columbian black-tailed deer (Odocoileus hemionus columbianus) density on a mid-sized (17.3km2) predator-free island. We documented successional changes associated with forest aggradation and decreased forage quality for deer: early successional shrub/scrub habitat declined 3.8%/year; timber volume increased 4.5%/year; and canopy coverage increased 2.5%. In 2007-2008, deer densities were the greatest observed (~44/km2), but then an historic snowstorm reduced deer density by 39%. From 2010-2021, as forests continued to mature, deer density decreased 4.0%/year, declining to 20 deer/km2. Using a multivariate approach to combine habitat variables (i.e., early seral coverage, timber volume, and canopy closure) into a measure of forest maturation, we found a significant negative relationship between deer density and forest aggradation. Thus, consistent with predictions for bottom-up limited browsers, we observed significant annual declines in a deer population throughout an extended period of forest regrowth. Despite declines, deer density on the island exceeds mainland densities, and overbrowsing likely continues to disrupt ecosystem processes.

Saxitoxin and the Ochre Sea Star: Molecule of Keystone Significance and a Classic Keystone Species.

Saxitoxins (STXs) are paralytic alkaloids produced by marine dinoflagellates in response to biotic and abiotic stressors yielding harmful algal blooms. Because STX impacts coastal, near-shore communities to a greater extent than would be predicted by its relative abundance, it has been referred to as a "molecule of keystone significance" in reference to Robert Paine's Keystone Species Concept. Pisaster ochraceus, the predator upon which Paine's concept was founded, inhabits waters regularly plagued by harmful algal blooms, but the effects of STX on Pisaster have not yet been investigated. Here, we used laboratory and field experiments to examine the potential consequences of exposure to STX on sea stars' feeding, attachment to the substrate, and success in fertilization. Pisaster exhibited similar feeding behaviors when offered non-toxic prey, STX-containing prey, or a combination of the two. Although feeding behavior is unaffected, consumption of STX poses a physiological tradeoff. Sea stars in the laboratory and field had significantly lower thresholds of the force needed to detach them from their substrates after either being exposed to, or consuming, STX. High pressure (or high performance) liquid chromatography analysis indicated an accumulation of STX (and structural analogues) in sea stars' viscera, likely due to trophic transfer from toxic prey. Incidence of fertilization tended to decrease when gametes were exposed to high, yet ecologically relevant, STX concentrations of STX. These findings suggest that the molecule of keystone significance, STX, produced during harmful algal blooms extends its impacts to rocky intertidal communities by way of the keystone predator P. ochraceus.

Community ecology and the evolution of molecules of keystone significance.

Molecules of keystone significance are vital in structuring ecological communities. Select bioactive compounds can cause disproportionately large effects by connecting such seemingly disparate processes as microbial loop dynamics and apex predation. Here, we develop a general theory and propose mechanisms that could lead to the evolution of keystone molecules. Introduced into a respective community by one, or only a few, autotrophic or microbial species, these compounds often originate as chemical defenses. When co-opted by resistant consumer species, however, they are used either in chemical defense against higher-order predators or as chemosensory cues that elicit courtship and mating, alarm, and predatory search. Requisite to these multifunctional properties, biosynthetic capacity evolves along with mechanisms for resistance and/or toxin storage in primary producers. Subsequently, consumers acquire resistances or tolerances, and the toxins are transferred through food webs via trophic interactions. In consumers, mechanisms eventually evolve for recognizing toxins as feeding cues and, ultimately, as signals or pheromones in chemical communication within or between species. One, or a few, active compounds can thus mediate a vast array of physiological traits, expressed differentially across many species in a given community. Through convergent evolution, molecules of keystone significance provide critical information to phylogenetically diverse species, initiate major trophic cascades, and structure communities within terrestrial, freshwater, coastal-ocean and open-ocean habitats.

Chemical neuroecology and community dynamics.

Chemical neuroecology examines the relationships between chemosensory physiology, behavior, and population and community dynamics. A keystone species, for example, is one whose impact on communities is far greater than would be predicted from its relative abundance and biomass. Neurotoxins, then, could function in keystone roles. Rare within natural habitats, they exert strong effects on species interactions at multiple trophic levels. Effects of two guanidine alkaloids, tetrodotoxin (TTX) and saxitoxin (STX), coalesce neurobiological and ecological perspectives. These potent neurotoxins function as chemical defenses by binding to voltage-gated sodium channels on nerve and muscle cells. When borrowed by resistant consumer species, however, they are used in chemical defense against higher-order predators or as chemosensory excitants in mediating critical behavioral interactions. Through a combination of diverse physiological traits, TTX and STX exert profound impacts reverberating across multiple trophic levels and determining a wide range of community-wide attributes. Such traits ultimately render TTX and STX fully functional as keystone molecules, with vast ecological consequences for species assemblages and rates of material exchange.

Neuroecology, chemical defense, and the keystone species concept.

Neuroecology unifies principles from diverse disciplines, scaling from biophysical properties of nerve and muscle cells to community-wide impacts of trophic interactions. Here, these principles are used as a common fabric, woven from threads of chemosensory physiology, behavior, and population and community ecology. The "keystone species" concept, for example, is seminal in ecological theory. It defines a species whose impacts on communities are far greater than would be predicted from its relative abundance and biomass. Similarly, neurotoxins could function in keystone roles. They are rare within natural habitats but exert strong effects on species interactions at multiple trophic levels. Effects of two guanidine alkaloids, tetrodotoxin (TTX) and saxitoxin (STX), coalesce neurobiological and ecological perspectives. These molecules compose some of the most potent natural poisons ever described, and they are introduced into communities by one, or only a few, host species. Functioning as voltage-gated sodium channel blockers for nerve and muscle cells, TTX and STX serve in chemical defense. When borrowed by resistant consumer species, however, they are used either in chemical defense against higher order predators or for chemical communication as chemosensory excitants. Cascading effects of the compounds profoundly impact community-wide attributes, including species compositions and rates of material exchange. Thus, a diverse array of physiological traits, expressed differentially across many species, renders TTX and STX fully functional as keystone molecules, with vast ecological consequences at multiple trophic levels.

Chemosensory reception, behavioral expression, and ecological interactions at multiple trophic levels.

Chemoreception may function throughout an entire animal lifetime, with independent, stage-specific selection pressures leading to changes in physiological properties, behavioral expression, and hence, trophic interactions. When the California newt (Taricha torosa) metamorphoses from an entirely aquatic larva to a semi-terrestrial juvenile/adult form, its chemosensory organs undergo dramatic reorganization. The relationship between newt life-history stage and chemosensory-mediated behavior was established by comparing responses of adults (as determined here) to those of conspecific larvae (as studied previously). Bioassays were performed in mountain streams, testing responses of free-ranging adults to 13 individual l-amino acids. Relative to stream water (controls), adults turned immediately upcurrent and moved to the source of arginine, glycine or alanine release. These responses were indicative of predatory search. Arginine was the strongest attractant tested, with a response threshold (median effective dose) of 8.3x10(-7) mol l(-1) (uncorrected for dilution associated with chemical release and delivery). In contrast to adult behavior, arginine suppressed cannibal-avoidance and failed to evoke search reactions in larvae. For a common set of arginine analogs, the magnitudes of adult attraction and larval suppression were not positively correlated. Suppression of cannibal-avoidance behavior in larvae was unaffected by most structural modifications of the arginine molecule. Adult behavior, on the other hand, was strongly influenced by even subtle alterations in the parent compound. Reactions to arginine in both adults and larvae were eliminated by blocking the external openings of the nasal cavity. Stimulating adult predatory search in one case and inhibiting larval cannibal avoidance in the other, arginine is a chemical signal with opposing behavioral effects and varying ecological consequences. Significant differences between responses of adults and larvae to changes in arginine structure suggest alternative, chemosensory receptor targets. Although arginine reception functions throughout an entire newt lifetime, an ontogenetic shift in larval and adult chemoreceptive ability changes behavioral expression, and thus, reflects the unique selection pressures that act at each life-history stage.

The scent of danger: arginine as an olfactory cue of reduced predation risk.

Animal perception of chemosensory cues is a function of ecological context. Larvae of the California newt (Taricha torosa), for example, exhibit predator-avoidance behavior in response to a chemical from cannibalistic adults. The poison tetrodotoxin (TTX), well known as an adult chemical defense, stimulates larval escape to refuges. Although they are cannibals, adult newts feed preferentially on worms (Eisenia rosea) over conspecific young. Hence, larval avoidance reactions to TTX are suppressed in the presence of odor from these alternative prey. The free amino acid, arginine, is abundant in fluids emitted by injured worms. Here, we demonstrate that arginine is a natural suppressant of TTX-stimulated larval escape behavior. Compared to a tapwater control, larvae initiated vigorous swimming in response to 10(-7) mol l(-1) TTX. This excitatory response was eliminated when larval nasal cavities were blocked with an inert gel, but not when gel was placed on the forehead (control). In additional trials, a binary mixture of arginine and 10(-7) mol l(-1) TTX failed to induce larval swimming. The inhibitory effect of arginine was, however, dose dependent. An arginine concentration as low as 0.3-times that of TTX was significantly suppressant. Further analysis showed that suppression by arginine of TTX-stimulated behavior was eliminated by altering the positively-charged guanidinium moiety, but not by modifying the carbon chain, carboxyl group, or amine group. These results are best explained by a mechanism of competitive inhibition between arginine and TTX for common, olfactory receptor binding sites. Although arginine alone has no impact on larval behavior, it nevertheless signals active adult predation on alternative prey, and hence, reduced cannibalism risk.