Ecology

AffiliationsCAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, ChinaHong QianResearch and Collections Center, Illinois State Museum, Springfield, IL, USAHong QianDepartment of Biology, University of Missouri–St. Louis, St. Louis, MO, USARobert E. RicklefsUniv. Grenoble Alpes, Univ. Savoie Mont Blanc, CNRS, LECA, Laboratoire d’Ecologie Alpine, Grenoble, FranceWilfried ThuillerAuthorsHong QianRobert E. RicklefsWilfried ThuillerCorresponding authorCorrespondence to
Hong Qian. More

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In this study, we confirmed that P. longissimus is nonbioluminescent, despite its close relationship to the luminous species P. litoralis (Supplementary Fig. S2)8. The presence of both luminous and nonluminous species in a single genus is likely widespread, but only a few examples have been confirmed; for example, the genera Vibrio and Photobacterium (marine bacteria)9, Epigonus (deep-sea fishes)10, Mycena (bonnet mushrooms)11 and Eisenia (terrestrial earthworms)12 have been reported to contain both luminous and nonluminous species. P. litoralis and P. longissimus can easily be collected at the same beach8 and reared in a laboratory; thus, they are suitable for studying the ecology and evolution of bioluminescence.In vitro luciferin-luciferase cross-reaction tests of P. longissimus and P. litoralis confirmed that the luminescence ability of P. litoralis is due to the presence of multiple bioluminescent components in coelomic fluid, i.e., luciferin, luciferase and the light emitter. Cross-reaction tests have previously indicated that luminous earthworms in the genera Pontodrilus (Megascolecidae), Microscolex and Diplocardia (Acanthodrilidae) share the same basic bioluminescence mechanisms5,7,13,14, despite their distant relationships to each other15,16. It is expected that the ancestral state of Pontodrilus is nonbioluminescent because the nearest extant relatives of Pontodrilus belong to the genus Plutellus Perrier, 1873, and all members of this group are nonbioluminescent6,17. These findings suggested that P. litoralis secondarily acquired bioluminescent properties through parallel evolution, similar to the case of bioluminescence in lampyrid and elaterid beetles18. We detected a clear difference in the protein composition of the secreted fluid between P. litoralis and P. longissimus (Supplementary Fig. S1). Luciferase and other bioluminescent components of luminous earthworms were not identified, and further comparative analyses of the protein bands, which appear only in the secreted fluid of luminous species, will be useful to understand the mechanisms of bioluminescence and its parallel evolution.In Thailand, P. longissimus was found sympatrically with P. litoralis at the beaches along the coast, but the microhabitats of the two congeners are different; P. litoralis was collected on the beach surface (under trash or leaf litter on sandy beaches), whereas P. longissimus was found at a greater depth than P. litoralis, i.e., a depth of more than 10 cm, where trash and leaves are scarce8 (Fig. 4A–D). It has been hypothesized that the biological function of bioluminescence in Annelida, including P. litoralis, is to stun or divert attention as an anti-predator defense19,20,21,22,23,24,25, but experiments and observations of the prey are limited. Sivinski & Forrest25 reported that the luminescence of Microscolex phosphoreus deterred predation by the mole cricket Scapteriscus acletus under laboratory conditions, although the specimen was ultimately consumed. A British television program26 presented by David Attenborough showed that the French luminous earthworm Avelona ligra glowed when attacked by the carabid beetle, but the beetle consumed the luminescent worm without any hesitation. We suggest that the absence of bioluminescence in P. longissimus may be associated with its presence in habitats with low predation pressure, whereas P. litoralis acquired a bioluminescent property during evolution that enabled it live on the surface of the beach, which is rich in nutrition and food sources3,27 as well as potential predators.Figure 4(A) The microhabitat of Pontodrilus litoralis from Aichi Prefecture, Japan. (B) The microhabitat of P. longissimus in Ranong, Thailand; sympatric Pontodrilus specimens were collected from this location8. (C) P. longissimus was found at a depth of 10–30 cm in muddy sand; the earthworm is shown by an arrow. (D) Bright field image of the Pontodrilus species included in this study. (E) An earwig (Anisolabis maritima) (a potential Pontodrilus predator) grooming its forelegs after attacking P. litoralis. (F) A. maritima (arrowhead) was found in the same microhabitat as P. litoralis in Aichi Prefecture, Japan.Full size imageIndeed, while we observed some burrowing bivalves, no potential predators were observed in the deep sand inhabited by P. longissimus. In contrast, various carnivorous invertebrates, such as earwigs, rove beetles and carabid beetles, were observed on the surface of beaches in Thailand and Japan, where P. litoralis live (Seesamut pers. obs.). We therefore performed a feeding experiment using maritime earwigs sympatrically distributed in a P. litoralis habitat. The maritime earwig Anisolabis maritima (Dermaptera, Anisolabididae) is a cosmopolitan species that can be found in Japan. It has well-developed compound eyes (Fig. 4E) and is considered a carnivorous animal that forages for prey at night28, 29. A. maritima (body length ≤ 30 mm) was the predominant predator at the beach where P. litoralis was collected (Fig. 4F). Some rove beetles (Coleoptera, Staphylinidae) were found in the same habitat, but they seemed to be too small ( More

In Europe, bumblebees pollinate the flowers called foxgloves, but foxgloves that spread to the Americas are also pollinated by hummingbirds and have evolved as a result. Credit: Getty

Ecology
16 April 2021
Flowers adapt to welcome the birds — but not the bees

Once in the Americas, foxgloves swiftly evolved under pressure by pollinating hummingbirds.

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Evolution can forge new relationships between plants and pollinators in fewer than 85 generations.The showy purple flowers called common foxgloves (Digitalis purpurea) are native to Europe, where they are pollinated by bumblebees. When admiring humans took the foxglove to the Americas, it was enthusiastically embraced by a new guild of nectar-drinkers — the hummingbirds.Maria Clara Castellanos at the University of Sussex in Brighton, UK, and her colleagues tallied visitors to foxgloves in the United Kingdom, Colombia and Costa Rica during more than 2,000 3-minute study periods. They found that hummingbirds pollinate up to 27% of foxgloves in Colombia and Costa Rica, where the flowers’ corollas — the long purple tubes that gardeners love so much — are 13% and 26% longer, respectively, than those of UK foxgloves.So why would foxgloves with longer corollas do better? Plants with corollas too long for bumblebees to reach their nectar are guaranteed to be pollinated by hummingbirds, which are more effective than bees at depositing pollen on the next flower. The longer corolla also creates a more comfortable fit for a hovering hummingbird, perhaps improving pollination rates.Hummingbirds can travel further between flowers than can bees, which might reduce plant inbreeding.

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