Nocturnal moths as pollinators -- and effects of light pollution

Most pollinator studies have focused on insects that are active during daytime, largely ignoring nocturnal insects.  Many nocturnal insects have suffered significant declines.  For example, the populations of two-thirds of the widespread large moth species in Great Britain have significantly declined over the last 40 years.  In addition to bats, beetles, and flies, moths are important nocturnal pollinators; particularly the nectar-feeding species from the moth families Sphingidae, Noctuidae, Geometridae, and Erebidae.  A great diversity of plants, in a wide range of ecosystems, benefit from pollination by moths.

Long-term trends reveal that moth populations have declined, and distributions have narrowed, in Great Britain, the Netherlands, and Finland.  Surely this has been a widespread occurrence elsewhere, though long-term trend data is not necessarily widely-available.  It is likely that habitat degradation and climate change are causing much of these declines, as is the case for diurnal (daytime) pollinators.  Additionally, artificial lighting during nighttime has also been proposed as a cause of nocturnal moth declines.

Moths are well-known to be attracted to artificial lights, often in large numbers.  Shorter wavelengths are generally more attreactive to moths, attractiveness peaking around wavelengths of 400 nm (violet light).  Males of some species have been significantly more-frequently observed at light traps than females, but it is unclear whether this is due to males having a higher attraction to lights, or males being more active and therefore more likely to move into an artificial light's area of influence.  Other than this flight-to-light behavior, moths may be affected by increased ambient light at night, or altered perception of photoperiod in the vicinity of artificial lights.  Additionally, hot components of lamps, or radiant energy from bright lights, can kill insects or damage their wings, legs, and antennae.

Moth reproduction may also be negatively affected by artificial night lighting.  Artificial light can prevent egg-laying, as well as the release of sex pheromones (disrupting mating activity), in some nocturnal moth species.  Artificial lighting could also distract males from female pheromone signals.  In fact, artificial lights have been observed to redirect dispersing- or migrating moths to locations that are unsuitable for breeding, creating an ecological trap for the moths.

Aside from the fact that nocturnal moths are an important food item for numerous other organisms, the loss of these pollinators would certainly lead to the loss of plant diversity, since many plants are reliant on a single- or a few species of moths in order for the plant to sexually reproduce.

LINK to Macgregor et al.'s 2015 article in Ecological Entomology.

Carnivorous pitcher plants as a habitat

In order to obtain nutrients in their nutrient-poor environments, carnivorous pitcher plants trap animals that, once trapped, usually die within a short amount of time.  Animal bodies are dissolved by digestive enzymes produced by the plant, or by mutualistic organisms.  The objective of prey capture is to obtain inorganic nutrients, especially nitrogen and phosphorus.  The epidermis of the trap is composed of a porous cuticle where dissolved nutrients are absorbed.

Carnivorous pitcher plants evolved independently five times in different geographic regions, yet the traps are very similar in all species (Approximately 110 species known).  The uppermost part of the pitcher contains glands that produce nectar and volatiles, which attracts prey.  Prey falls into a hollow leaf, and is unable to climb out due to the ultrastructural composition of the waxy exocuticle (loose wax crystals make climbing impossible for most organisms); the slippery surface at the pitcher margin, and inward-pointing hairs, causes the prey to fall into the pitcher.  The lower part of the pitcher is filled with a fluid that often contains glands for enzyme production.  The biodiversity and ecology of any waterbody is strongly influenced by water chemistry; of all phytotelmata (waterbodies held by living terrestrial plants), carnivorous pitcher plants undoubtedly have the strongest influence over their enclosed waterbody.

In the pitcher plant genera Nepenthes and Cephalotus, closed immature traps already contain fluid which is transferred from the xylem, into the parenchyma, and through glands covering the inner surface of the modified leaf.  Large Nepenthes traps may contain over 1 L of fluid.  The pH of most pitcher fluid is acidic; changes in pH are caused by epidermal cells secreting hydrogen ions.  The fluid of Nepenthes rafflesiana is extremely viscoelatic; the viscoelasticity of the fluid is maintained even after much dilution (up to 95 % dilution), possibly an adaptation to rainfall.  Many pitcher plants have a hood over the trap to keep rainfall from entering the trap.  Surfactants likely occur in several carnivorous pitcher plants, in order to cause drowning of prey by reducing surface tension of the fluid.  Additionally, prey animals stop struggling within a few minutes, which is much faster than in pure water.

Digestive enzymes are found in the fluid of numerous carnivornous pitcher plants; this is an additional energy investment of the plant.  In pitcher plants that do not produce digestive enzymes, a community of organisms within the fluid is essential for breaking down food items.  Some pitcher plants collect non-living organic matter, such as dead leaves.  Aerial (upper) pitchers of a climbing pitcher plant, Nepenthes lowii, lack structures for trapping prey, but still produce nectar.  The nectar of N. lowii is consumed by tree shrews (Tupaia montana) that drop their feces into the pitchers, providing the plant with nutrients.  Still, most carnivorous pitcher plants mainly trap social insects, especially ants.

No species of pitcher plants kills all organisms entering the traps.  Some organisms, from bacteria to amphibians, are able to survive and reproduce within the trap.  For some pitcher inhabitants, pitcher traps are the only habitat in which the species lives.  Pitcher plants grow in different climates, around various plant communities; and different species have differently-shaped pitchers holding fluids with different chemical compositions.  As a consequence of this, they host different inhabitants.  Freshwater animals from most taxonomic phyla inhabit pitcher plants.  Flies are the most diverse animal order found in pitchers; their mobility, along with their well-developed eyes and sense of smell, allows them to find the pitchers in which they lay their eggs.  Misumenops thienemanni and other crab spiders (family Thomisidae) enter pitcher fluid while hanging from a strand of silk, overcoming the high viscoelasticity of the fluid by using extremely slow movements.  Other spiders creating a silk net, sealing the pitcher, catching animals that visit the plant.  The frog species Kalophrynus pleurostigma and Microhyla nepenthicola use Nepenthes ampullaria pitchers as nurseries; up to 100 tadpoles of K. pleurostigma can develop within one pitcher.  Up to four trophic levels, including micro-organisms, can be found in a single N. ampullaria pitcher.

Protozoa are diverse and abundant in Sarracenia pitchers.  Most of these protozoa tolerate low water quality, which is expected due to the presence of dead prey.  Bacterial diversity is unknown; most grow on decaying prey.  Diversity and abundance of fungal hyphae in pitchers are low.  Approximately 70 % of all Sarracenia pitchers are inhabited by the rotifer Habrotrocha rosa, while other rotifers are rare.  Colonization of rotifers occurs by individuals attaching themselves to female pitcher-plant mosquitoes (Wyeomyia smithii).  As in Nepenthes pitchers, arthropods are the most diverse group inhabiting Sarracenia pitchers; this includes crustaceans, mites, spiders, and insects.  The food-webs in Sarracenia traps are quite similar to the food-webs in Nepenthes traps.  As Sarracenia fluid lacks digestive enzymes, micro-organisms most likely play a large role in prey degradation.

Pitcher plants of the genus Heliamphora are restricted to relatively-inaccessible table mountains, and few observations are documented.  Although the bacteria communities in Heliamphora are similar to those found in Sarracenia purpurea, fungi are more abundant in Heliamphora.  Regarding insects, only two species of pitcher-plant mosquitoes are regularly found in Heliamphora.  As with Nepenthes and Sarracenia, spiders create silk webs at the opening of Heliamphora pitchers.

Little is known about the inhabitants of the pitcher-traps of carnivorous bromeliads.  Notably, the bladderwort Utricularia humboldti was reported to colonize these traps; U. homboldti is the only vascular plant known to inhabit pitcher-traps.

In order for a species to establish a population within a pitcher trap, the species must first occur in the same habitat as the pitcher plant.  Then the organisms have to find a pitcher.  Micro-organisms enter traps by rainfall washing cells and spores from the air into the traps, or they may be attached to other organisms entering the pitcher fluid.  Pregnant female pitcher-plant mosquitoes actively search for traps as habitat for their larvae, showing a preferrence for unoccupied traps.  Next, survival in the pitcher fluid must be possible for a population of inhabitants to persist there; most organisms are unable to survive in the fluid.  Finally, resources must also be available for the inhabitants.  In pitchers of Sarracenia and Nepenthes, protists and bacteria are more abundant when the fluid contains more organic nutrients.  In pitchers of Sarracenia purpurea, populations of crab spiders and pitcher-plant mosquitoes are limited by the availability of drowned prey.  In contrast, amphibian tadpoles obtain nutrients from their own yolk until metamorphosis.  Research indicates that a higher species diversity of pitcher-fluid inhabitants increases the stability of pitcher-fluid communities.  Long-term survival is also determined by the life-span of the pitcher, and by the drying- or freezing of the pitcher-fluid.

Some pitcher-trap inhabitants may damage the pitcher or extract nutrients, thereby acting as parasites and parasitoids.  Algae are often abundant in pitcher fluid, consuming dissolved inorganic nutrients.  Caterpillars inhabit pitchers of Nepenthes and Sarracenia, feeding on the inner wall, which leads to the loss of the plant's trapping ability and destruction of the pitcher.  The weevil Metamasius callizona feeds on the meristem tissue at the bottom of C berteroniana pitchers, killing the plant.  The presence of tadpoles in Nepenthes ampullaria pitchers is most likely a commensal relationship, but the mating parents damage the pitchers.  A pitcher's trapping success is reduced by visitors feeding on the plant's prey; these parasitic visitors include crab spiders, the ant Camponotus schmitzi, apes, geckoes, crabs, mantises, among other animals.  Interestingly though, in Sarracenia and Nepenthes pitchers, visitors catch caterpillars that eat the pitchers.

Other pitcher-trap inhabitants may help the plant digest prey.  In pitcher plant species without digestive enzyme production, pitcher inhabitants degrade- and oxidize prey-derived macromolecules, improving a plant's ability to consume these nutrients.  Nepenthes species with poor digestive enzyme production allow bacterial growth by avoiding extreme pH of the pitcher fluid.  Within pitcher fluid, nutrients absorbed by bacteria are partly recycled back to the plant by animals feeding on the bacteria; an average Sarracenia purpurea pitcher hosts 388 ± 924 (range 0 - 960) rotifers (Habrotrocha rosa) feeding mainly on bacteria.  Phosphorus is excreted as phosphate, and 70 % of nitrogen excreted is in the form of ammonium.  Fly larvae also feed on the plant's prey and excrete nitogen in the form of ammonium.  Large insect larvae perform the additional task of physically breaking up prey items, improving accessibility for digestive enzymes and smaller organisms.  However, when insects leave the pitchers, they take valuable nitrogen and phosphorus with them.

Certainly carnivorous pitcher plants have some influence over the communities inhabiting the pitcher fluid.  There is growing evidence for the presence of toxic substances, digestive enzymes, radicals, detergents, narcotics, gelling agents, and acids in the fluid of some pitcher plant species.  The fluid is supplied with oxygen through gaps in the cuticle of the pitcher's inner walls.  Carbon dioxide produced by the fluid's inhabitants is easily absorbed by the leaf (pitcher), while photosynthetic oxygen easily diffuses into the fluid to be used by the inhabitants.

LINK to Adlassnig et al.'s 2011 article in Annals of Botany.