A transdisciplinary research agenda for understanding insect responses to ecological light pollution informed by evolutionary trap theory.

Evolutionary traps are phenomena in which rapid environmental change causes environmental cues that historically guided adaptive behavioral or life-history decisions to become poor predictors of the consequences of such decisions for an organism's fitness. Evolutionary trap theory offers an ideal framework for understanding and mitigating the effects of ecological light pollution (ELP) on insects. We emphasize the utility of an evolutionary trap perspective in demonstrating the importance of an integrated understanding of the sensory, behavioral, evolutionary, and demographic mechanisms underlying insect responses to ELP. We also highlight neglected areas of research where greater focus can help enhance understanding of how ELP affects the persistence, evolutionary trajectory, and population dynamics of insects across space and time.

Color polarization vision mediates the strength of an evolutionary trap.

Evolutionary traps are scenarios in which animals are fooled by rapidly changing conditions into preferring poor-quality resources over those that better improve survival and reproductive success. The maladaptive attraction of aquatic insects to artificial sources of horizontally polarized light (e.g., glass buildings, asphalt roads) has become a first model system by which scientists can investigate the behavioral mechanisms that cause traps to occur. We employ this field-based system to experimentally investigate (a) in which portion(s) of the spectrum are polarizationally water-imitating reflectors attractive to nocturnal terrestrial and aquatics insects, and (b) which modern lamp types result in greater attraction in this typical kind of nocturnal polarized light pollution. We found that most aquatic taxa exhibited preferences for lamps based upon their color spectra, most having lowest preference for lamps emitting blue and red light. Yet, despite previously established preference for higher degrees of polarization of reflected light, most aquatic insect families were attracted to traps based upon their unpolarized spectrum. Chironomid midges, alone, showed a preference for the color of lamplight in both the horizontally polarized and unpolarized spectra indicating only this family has evolved to use light in this color range as a source of information to guide its nocturnal habitat selection. These results demonstrate that the color of artificial lighting can exacerbate or reduce its attractiveness to aquatic insects, but that the strength of attractiveness of nocturnal evolutionary traps, and so their demographic consequences, is primarily driven by unpolarized light pollution. This focuses management attention on limiting broad-spectrum light pollution, as well as its intentional deployment to attract insects back to natural habitats.

Lamp-lit bridges as dual light-traps for the night-swarming mayfly, Ephoron virgo: interaction of polarized and unpolarized light pollution.

Ecological photopollution created by artificial night lighting can alter animal behavior and lead to population declines and biodiversity loss. Polarized light pollution is a second type of photopollution that triggers water-seeking insects to ovisposit on smooth and dark man-made objects, because they simulate the polarization signatures of natural water bodies. We document a case study of the interaction of these two forms of photopollution by conducting observations and experiments near a lamp-lit bridge over the river Danube that attracts mass swarms of the mayfly Ephoron virgo away from the river to oviposit on the asphalt road of the bridge. Millions of mayflies swarmed near bridge-lights for two weeks. We found these swarms to be composed of 99% adult females performing their upstream compensatory flight and were attracted upward toward unpolarized bridge-lamp light, and away from the horizontally polarized light trail of the river. Imaging polarimetry confirmed that the asphalt surface of the bridge was strongly and horizontally polarized, providing a supernormal ovipositional cue to Ephoron virgo, while other parts of the bridge were poor polarizers of lamplight. Collectively, we confirm that Ephoron virgo is independently attracted to both unpolarized and polarized light sources, that both types of photopollution are being produced at the bridge, and that spatial patterns of swarming and oviposition are consistent with evolved behaviors being triggered maladaptively by these two types of light pollution. We suggest solutions to bridge and lighting design that should prevent or mitigate the impacts of such scenarios in the future. The detrimental impacts of such scenarios may extend beyond Ephoron virgo.

Perennial grasslands enhance biodiversity and multiple ecosystem services in bioenergy landscapes.

Agriculture is being challenged to provide food, and increasingly fuel, for an expanding global population. Producing bioenergy crops on marginal lands--farmland suboptimal for food crops--could help meet energy goals while minimizing competition with food production. However, the ecological costs and benefits of growing bioenergy feedstocks--primarily annual grain crops--on marginal lands have been questioned. Here we show that perennial bioenergy crops provide an alternative to annual grains that increases biodiversity of multiple taxa and sustain a variety of ecosystem functions, promoting the creation of multifunctional agricultural landscapes. We found that switchgrass and prairie plantings harbored significantly greater plant, methanotrophic bacteria, arthropod, and bird diversity than maize. Although biomass production was greater in maize, all other ecosystem services, including methane consumption, pest suppression, pollination, and conservation of grassland birds, were higher in perennial grasslands. Moreover, we found that the linkage between biodiversity and ecosystem services is dependent not only on the choice of bioenergy crop but also on its location relative to other habitats, with local landscape context as important as crop choice in determining provision of some services. Our study suggests that bioenergy policy that supports coordinated land use can diversify agricultural landscapes and sustain multiple critical ecosystem services.

The cancer diaspora: Metastasis beyond the seed and soil hypothesis.

Do cancer cells escape the confinement of their original habitat in the primary tumor or are they forced out by ecologic changes in their home niche? Describing metastasis in terms of a simple one-way migration of cells from the primary to the target organs is an insufficient concept to cover the nuances of cancer spread. A diaspora is the scattering of people away from an established homeland. To date, "diaspora" has been a uniquely human term used by social scientists; however, the application of the diaspora concept to metastasis may yield new biologic insights as well as therapeutic paradigms. The diaspora paradigm takes into account, and models, several variables including: the quality of the primary tumor microenvironment, the fitness of individual cancer cell migrants as well as migrant populations, the rate of bidirectional migration of cancer and host cells between cancer sites, and the quality of the target microenvironments to establish metastatic sites. Ecologic scientific principles can be applied to the cancer diaspora to develop new therapeutic strategies. For example, ecologic traps - habitats that lead to the extinction of a species - can be developed to attract cancer cells to a place where they can be better exposed to treatments or to cells of the immune system for improved antigen presentation. Merging the social science concept of diaspora with ecologic and population sciences concepts can inform the cancer field to understand the biology of tumorigenesis and metastasis and inspire new ideas for therapy.

Ecological novelty and the emergence of evolutionary traps.

Human-induced rapid environmental change (HIREC; e.g., climate change or exotic species) has caused global species declines. Although behavioral plasticity has buffered some species against HIREC, maladaptive behavioral scenarios called 'evolutionary traps' are increasingly common, threatening the persistence of affected species. Here, we review examples of evolutionary traps to identify their anthropogenic causes, behavioral mechanisms, and evolutionary bases, and to better forecast forms of HIREC liable to trigger traps. We summarize a conceptual framework for explaining the susceptibility of animals to traps that integrates the cost-benefit approach of standard behavioral ecology with an evolutionary approach (reaction norms) to understanding cue-response systems (signal detection). Finally, we suggest that a significant revision of conceptual thinking in wildlife conservation and management is needed to effectively eliminate and mitigate evolutionary traps.

How the type of anthropogenic change alters the consequences of ecological traps.

Understanding altered ecological and evolutionary dynamics in novel environments is vital for predicting species responses to rapid environmental change. One fundamental concept relevant to such dynamics is the ecological trap, which arises from rapid anthropogenic change and can facilitate extinction. Ecological traps occur when formerly adaptive habitat preferences become maladaptive because the cues individuals preferentially use in selecting habitats lead to lower fitness than other alternatives. While it has been emphasized that traps can arise from different types of anthropogenic change, the resulting consequences of these different types of traps remain unknown. Using a novel model framework that builds upon the Price equation from evolutionary genetics, we provide the first analysis that contrasts the ecological and evolutionary consequences of ecological traps arising from two general types of perturbations known to trigger traps. Our model suggests that traps arising from degradation of existing habitats are more likely to facilitate extinction than those arising from the addition of novel trap habitat. Importantly, our framework reveals the mechanisms of these outcomes and the substantial scope for persistence via rapid evolution that may buffer many populations from extinction, helping to resolve the paradox of continued persistence of many species in dramatically altered landscapes.

Avian use of perennial biomass feedstocks as post-breeding and migratory stopover habitat.

Increased production of biomass crops in North America will require new agricultural land, intensify the cultivation of land already under production and introduce new types of biomass crops. Assessing the potential biodiversity impacts of novel agricultural systems is fundamental to the maintenance of biodiversity in agricultural landscapes, yet the consequences of expanded biomass production remain unclear. We evaluate the ability of two candidate second generation biomass feedstocks (switchgrass, Panicum virgatum, and mixed-grass prairie) not currently managed as crops to act as post-breeding and fall migratory stopover habitat for birds. In total, we detected 41 bird species, including grassland specialists and species of state and national conservation concern (e.g. Henslow's Sparrow, Ammodramus henslowii). Avian species richness was generally comparable in switchgrass and prairie and increased with patch size in both patch types. Grassland specialists were less abundant and less likely to occur in patches within highly forested landscapes and were more common and likely to occur in larger patches, indicating that this group is also area-sensitive outside of the breeding season. Variation in the biomass and richness of arthropod food within patches was generally unrelated to richness and abundance metrics. Total bird abundance and that of grassland specialists was higher in patches with greater vegetation structural heterogeneity. Collectively, we find that perennial biomass feedstocks have potential to provide post-breeding and migratory stopover habitat for birds, but that the placement and management of crops will be critical factors in determining their suitability for species of conservation concern. Industrialization of cellulosic bioenergy production that results in reduced crop structural heterogeneity is likely to dramatically reduce the suitability of perennial biomass crops for birds.

A framework for understanding ecological traps and an evaluation of existing evidence.

When an animal settles preferentially in a habitat within which it does poorly relative to other available habitats, it is said to have been caught in an "ecological trap." Although the theoretical possibility that animals may be so trapped is widely recognized, the absence of a clear mechanistic understanding of what constitutes a trap means that much of the literature cited as support for the idea may be weak, at best. Here, we develop a conceptual model to explain how an ecological trap might work, outline the specific criteria that are necessary for demonstrating the existence of an ecological trap, and provide tools for researchers to use in detecting ecological traps. We then review the existing literature and summarize the state of empirical evidence for the existence of traps. Our conceptual model suggests that there are two basic kinds of ecological traps and three mechanisms by which traps may be created. To this point in time, there are still only a few solid empirical examples of ecological traps in the published literature (although those few examples suggest that both types of traps and all three of the predicted mechanisms do exist in nature). Therefore, ecological traps are either rare in nature, are difficult to detect, or both. An improved library of empirical studies will be essential if we are to develop a more synthetic understanding of the mechanisms that can trigger maladaptive behavior in general and the specific conditions under which ecological traps might occur.