Towards a mechanistic understanding of the effects of artificial light at night on insect populations and communities.

Artificial light at night (ALAN) is markedly changing the night-time environment with many studies showing single-species responses. Exposure to ALAN can lead to population declines that should have consequences for the functioning and stability of ecological communities. Here, we summarise current knowledge on how insect communities are affected by ALAN. Based on reported effects of ALAN on the interactions between species, and what has been demonstrated for similar effects in other contexts, we argue that direct effects of ALAN on a few species can potentially propagate through the network of species interactions to have widespread effects in ecological communities. This can lead to a shift in community structure and simplified communities. We discuss the diversity of ALAN as a pressure and highlight major gaps in the research field. In particular, we conclude that landscape level impacts on populations and communities are understudied.

A meta-analysis of biological impacts of artificial light at night.

Natural light cycles are being eroded over large areas of the globe by the direct emissions and sky brightening that result from sources of artificial night-time light. This is predicted to affect wild organisms, particularly because of the central role that light regimes play in determining the timing of biological activity. Although many empirical studies have reported such effects, these have focused on particular species or local communities and have thus been unable to provide a general evaluation of the overall frequency and strength of these impacts. Using a new database of published studies, we show that exposure to artificial light at night induces strong responses for physiological measures, daily activity patterns and life history traits. We found particularly strong responses with regards to hormone levels, the onset of daily activity in diurnal species and life history traits, such as the number of offspring, predation, cognition and seafinding (in turtles). So far, few studies have focused on the impact of artificial light at night on ecosystem functions. The breadth and often strength of biological impacts we reveal highlight the need for outdoor artificial night-time lighting to be limited to the places and forms-such as timing, intensity and spectrum-where it is genuinely required by the people using it to minimize ecological impacts.

Longer photoperiods through range shifts and artificial light lead to a destabilizing increase in host-parasitoid interaction strength.

Many organisms are experiencing changing daily light regimes due to latitudinal range shifts driven by climate change and increased artificial light at night (ALAN). Activity patterns are often driven by light cycles, which will have important consequences for species interactions. We tested whether longer photoperiods lead to higher parasitism rates by a day-active parasitoid on its host using a laboratory experiment in which we independently varied daylength and the presence of ALAN. We then tested whether reduced nighttime temperature tempers the effect of ALAN. We found that parasitism rate increased with daylength, with ALAN intensifying this effect only when the temperature was not reduced at night. The impact of ALAN was more pronounced under short daylength. Increased parasitoid activity was not compensated for by reduced life span, indicating that increased daylength leads to an increase in total parasitism effects on fitness. To test the significance of increased parasitism rate for population dynamics, we developed a host-parasitoid model. The results of the model predicted an increase in time-to-equilibrium with increased daylength and, crucially, a threshold daylength above which interactions are unstable, leading to local extinctions. Here we demonstrate that ALAN impact interacts with daylength and temperature by changing the interaction strength between a common day-active consumer species and its host in a predictable way. Our results further suggest that range expansion or ALAN-induced changes in light regimes experienced by insects and their natural enemies will result in unstable dynamics beyond key tipping points in daylength.

Shifting daylength regimes associated with range shifts alter aphid-parasitoid community dynamics.

With climate change leading to poleward range expansion of species, populations are exposed to new daylength regimes along latitudinal gradients. Daylength is a major factor affecting insect life cycles and activity patterns, so a range shift leading to new daylength regimes is likely to affect population dynamics and species interactions; however, the impact of daylength in isolation on ecological communities has not been studied so far. Here, we tested for the direct and indirect effects of two different daylengths on the dynamics of experimental multitrophic insect communities. We compared the community dynamics under "southern" summer conditions of 14.5-hr daylight to "northern" summer conditions of 22-hr daylight. We show that food web dynamics indeed respond to daylength with one aphid species (Acyrthosiphon pisum) reaching much lower population sizes at the northern daylength regime compared to under southern conditions. In contrast, in the same communities, another aphid species (Megoura viciae) reached higher population densities under northern conditions. This effect at the aphid level was driven by an indirect effect of daylength causing a change in competitive interaction strengths, with the different aphid species being more competitive at different daylength regimes. Additionally, increasing daylength also increased growth rates in M. viciae making it more competitive under summer long days. As such, the shift in daylength affected aphid population sizes by both direct and indirect effects, propagating through species interactions. However, contrary to expectations, parasitoids were not affected by daylength. Our results demonstrate that range expansion of whole communities due to climate change can indeed change interaction strengths between species within ecological communities with consequences for community dynamics. This study provides the first evidence of daylength affecting community dynamics, which could not be predicted from studying single species separately.

Low Levels of Artificial Light at Night Strengthen Top-Down Control in Insect Food Web.

Artificial light has transformed the nighttime environment of large areas of the earth, with 88% of Europe and almost 50% of the United States experiencing light-polluted night skies [1]. The consequences for ecosystems range from exposure to high light intensities in the vicinity of direct light sources to the very widespread but lower lighting levels further away [2]. While it is known that species exhibit a range of physiological and behavioral responses to artificial nighttime lighting [e.g., 3-5], there is a need to gain a mechanistic understanding of whole ecological community impacts [6, 7], especially to different light intensities. Using a mesocosm field experiment with insect communities, we determined the impact of intensities of artificial light ranging from 0.1 to 100 lux on different trophic levels and interactions between species. Strikingly, we found the strongest impact at low levels of artificial lighting (0.1 to 5 lux), which led to a 1.8 times overall reduction in aphid densities. Mechanistically, artificial light at night increased the efficiency of parasitoid wasps in attacking aphids, with twice the parasitism rate under low light levels compared to unlit controls. However, at higher light levels, parasitoid wasps spent longer away from the aphid host plants, diminishing this increased efficiency. Therefore, aphids reached higher densities under increased light intensity as compared to low levels of lighting, where they were limited by higher parasitoid efficiency. Our study highlights the importance of different intensities of artificial light in driving the strength of species interactions and ecosystem functions.

Trophic redundancy reduces vulnerability to extinction cascades.

Current species extinction rates are at unprecedentedly high levels. While human activities can be the direct cause of some extinctions, it is becoming increasingly clear that species extinctions themselves can be the cause of further extinctions, since species affect each other through the network of ecological interactions among them. There is concern that the simplification of ecosystems, due to the loss of species and ecological interactions, increases their vulnerability to such secondary extinctions. It is predicted that more complex food webs will be less vulnerable to secondary extinctions due to greater trophic redundancy that can buffer against the effects of species loss. Here, we demonstrate in a field experiment with replicated plant-insect communities, that the probability of secondary extinctions is indeed smaller in food webs that include trophic redundancy. Harvesting one species of parasitoid wasp led to secondary extinctions of other, indirectly linked, species at the same trophic level. This effect was markedly stronger in simple communities than for the same species within a more complex food web. We show that this is due to functional redundancy in the more complex food webs and confirm this mechanism with a food web simulation model by highlighting the importance of the presence and strength of trophic links providing redundancy to those links that were lost. Our results demonstrate that biodiversity loss, leading to a reduction in redundant interactions, can increase the vulnerability of ecosystems to secondary extinctions, which, when they occur, can then lead to further simplification and run-away extinction cascades.

Nonhost diversity and density reduce the strength of parasitoid-host interactions.

The presence of nonprey or nonhosts is known to reduce the strength of consumer- resource interactions by increasing the consumer's effort needed to find its resource. These interference effects can have a stabilizing effect on consumer-resource dynamics, but have also been invoked to explain parasitoid extinctions. To understand how nonhosts affect parasitoids, we manipulated the density and diversity of nonhost aphids using experimental host-parasitoid communities and tested how this affects parasitation efficiency of two aphid parasitoid species. To further study the behavioral response of parasitoids to nonhosts, we tested for changes in parasitoid time allocation in relation to their host-finding strategies. The proportion of successful attacks (attack rate) in both parasitoid species was reduced by the presence of nonhosts. The parasitoid Aphidius megourae was strongly affected by increasing nonhost diversity with the attack rate dropping from 0.39 without nonhosts to 0.05 with high diversity of nonhosts, while Lysiphlebus fabarum responded less strongly, but in a more pronounced way to an increase in nonhost density. Our experiments further showed that increasing nonhost diversity caused host searching and attacking activity levels to fall in A. megourae, but not in L. fabarum, and that A. megourae changed its behavior after a period of time in the presence of nonhosts by increasing its time spent resting. This study shows that nonhost density and diversity in the environment are crucial determinants for the strength of consumer-resource interactions. Their impact upon a consumer's efficiency strongly depends on its host/prey finding strategy as demonstrated by the different responses for the two parasitoid species. We discuss that these trait-mediated indirect interactions between host and nonhost species are important for community stability, acting either stabilizing or destabilizing depending on the level of nonhost density or diversity present.

Defensive insect symbiont leads to cascading extinctions and community collapse.

Animals often engage in mutualistic associations with microorganisms that protect them from predation, parasitism or pathogen infection. Studies of these interactions in insects have mostly focussed on the direct effects of symbiont infection on natural enemies without studying community-wide effects. Here, we explore the effect of a defensive symbiont on population dynamics and species extinctions in an experimental community composed of three aphid species and their associated specialist parasitoids. We found that introducing a bacterial symbiont with a protective (but not a non-protective) phenotype into one aphid species led to it being able to escape from its natural enemy and increase in density. This changed the relative density of the three aphid species which resulted in the extinction of the two other parasitoid species. Our results show that defensive symbionts can cause extinction cascades in experimental communities and so may play a significant role in the stability of consumer-herbivore communities in the field.

Experimental Evidence for the Population-Dynamic Mechanisms Underlying Extinction Cascades of Carnivores.

Species extinction rates due to human activities are high, and initial extinctions can trigger cascades of secondary extinctions, leading to further erosion of biodiversity. A potential major mechanism for secondary extinction cascades is provided by the long-standing theory that the diversity of consumer species is maintained due to the positive indirect effects that these species have on each other by reducing competition among their respective resource species. This means that the loss of one carnivore species could lead to competitive exclusion at the prey trophic level, leading to extinctions of further carnivore species. Evidence for these effects is difficult to obtain due to many confounding factors in natural systems, but extinction cascades that could be due to this mechanism have been demonstrated in simplified laboratory microcosms. We established complex insect food webs in replicated field mesocosms and found that the overharvesting of one parasitoid wasp species caused increased extinction rates of other parasitoid species, compared to controls, but only when we manipulated the spatial distribution of herbivore species such that the potential for interspecific competition at this level was high. This provides clear evidence for horizontal extinction cascades at high trophic levels due to the proposed mechanism. Our results demonstrate that the loss of carnivores can have widespread effects on other species at the same trophic level due to indirect population-dynamic effects that are rarely considered in this context.

Artificial nighttime light changes aphid-parasitoid population dynamics.

Artificial light at night (ALAN) is recognized as a widespread and increasingly important anthropogenic environmental pressure on wild species and their interactions. Understanding of how these impacts translate into changes in population dynamics of communities with multiple trophic levels is, however, severely lacking. In an outdoor mesocosm experiment we tested the effect of ALAN on the population dynamics of a plant-aphid-parasitoid community with one plant species, three aphid species and their specialist parasitoids. The light treatment reduced the abundance of two aphid species by 20% over five generations, most likely as a consequence of bottom-up effects, with reductions in bean plant biomass being observed. For the aphid Megoura viciae this effect was reversed under autumn conditions with the light treatment promoting continuous reproduction through asexuals. All three parasitoid species were negatively affected by the light treatment, through reduced host numbers and we discuss induced possible behavioural changes. These results suggest that, in addition to direct impacts on species behaviour, the impacts of ALAN can cascade through food webs with potentially far reaching effects on the wider ecosystem.