Leibniz Institute for Animal Biodiversity

Bonn, Germany

Leibniz Institute for Animal Biodiversity

Bonn, Germany
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News Article | May 9, 2017
Site: www.sciencemag.org

Entomologists call it the windshield phenomenon. "If you talk to people, they have a gut feeling. They remember how insects used to smash on your windscreen," says Wolfgang Wägele, director of the Leibniz Institute for Animal Biodiversity in Bonn, Germany. Today, drivers spend less time scraping and scrubbing. "I'm a very data-driven person," says Scott Black, executive director of the Xerces Society for Invertebrate Conservation in Portland, Oregon. "But it is a visceral reaction when you realize you don't see that mess anymore." Some people argue that cars today are more aerodynamic and therefore less deadly to insects. But Black says his pride and joy as a teenager in Nebraska was his 1969 Ford Mustang Mach 1—with some pretty sleek lines. "I used to have to wash my car all the time. It was always covered with insects." Lately, Martin Sorg, an entomologist here, has seen the opposite: "I drive a Land Rover, with the aerodynamics of a refrigerator, and these days it stays clean." Though observations about splattered bugs aren't scientific, few reliable data exist on the fate of important insect species. Scientists have tracked alarming declines in domesticated honey bees, monarch butterflies, and lightning bugs. But few have paid attention to the moths, hover flies, beetles, and countless other insects that buzz and flitter through the warm months. "We have a pretty good track record of ignoring most noncharismatic species," which most insects are, says Joe Nocera, an ecologist at the University of New Brunswick in Canada. Of the scant records that do exist, many come from amateur naturalists, whether butterfly collectors or bird watchers. Now, a new set of long-term data is coming to light, this time from a dedicated group of mostly amateur entomologists who have tracked insect abundance at more than 100 nature reserves in western Europe since the 1980s. Over that time the group, the Krefeld Entomological Society, has seen the yearly insect catches fluctuate, as expected. But in 2013 they spotted something alarming. When they returned to one of their earliest trapping sites from 1989, the total mass of their catch had fallen by nearly 80%. Perhaps it was a particularly bad year, they thought, so they set up the traps again in 2014. The numbers were just as low. Through more direct comparisons, the group—which had preserved thousands of samples over 3 decades—found dramatic declines across more than a dozen other sites. Such losses reverberate up the food chain. "If you're an insect-eating bird living in that area, four-fifths of your food is gone in the last quarter-century, which is staggering," says Dave Goulson, an ecologist at the University of Sussex in the United Kingdom, who is working with the Krefeld group to analyze and publish some of the data. "One almost hopes that it's not representative—that it's some strange artifact." No one knows how broadly representative the data are of trends elsewhere. But the specificity of the observations offers a unique window into the state of some of the planet's less appreciated species. Germany's "Red List" of endangered insects doesn't look alarming at first glance, says Sorg, who curates the Krefeld society's extensive collection of insect specimens. Few species are listed as extinct because they are still found in one or two sites. But that obscures the fact that many have disappeared from large areas where they were once common. Across Germany, only three bumble bee species have vanished, but the Krefeld region has lost more than half the two dozen bumble bee species that society members documented early in the 20th century. Members of the Krefeld society have been observing, recording, and collecting insects from the region—and around the world—since 1905. Some of the roughly 50 members—including teachers, telecommunication technicians, and a book publisher—have become world experts on their favorite insects. Siegfried Cymorek, for instance, who was active in the society from the 1950s through the 1980s, never completed high school. He was drafted into the army as a teenager, and after the war he worked in the wood-protection division at a local chemical plant. But because of his extensive knowledge of wood-boring beetles, the Swiss Federal Institute of Technology in Zurich awarded him an honorary doctorate in 1979. Over the years, members have written more than 2000 publications on insect taxonomy, ecology, and behavior. The society's headquarters is a former school in the center of Krefeld, an industrial town on the banks of the Rhine that was once famous for producing silk. Disused classrooms store more than a million insect specimens individually pinned and named in display cases. Most were collected nearby, but some come from more exotic locales. Among them are those from the collection of a local priest, an active member in the 1940s and 1950s, who persuaded colleagues at mission stations around the world to send him specimens. (The society's collection and archive are under historical preservation protection.) Tens of millions more insects float in carefully labeled bottles of alcohol—the yield from the society's monitoring projects in nature reserves around the region. The reserves, set aside for their local ecological value, are not pristine wilderness but "seminatural" habitats, such as former hay meadows, full of wildflowers, birds, small mammals—and insects. Some even include parts of agricultural fields, which farmers are free to farm with conventional methods. Heinz Schwan, a retired chemist and longtime society member who has weighed thousands of trap samples, says the society began collecting long-term records of insect abundance partly by chance. In the late 1970s and early 1980s, local authorities asked the group for help evaluating how different strategies for managing the reserves affected insect populations and diversity. The members monitored each site only once every few years, but they set up identical insect traps in the same place each time to ensure clean comparisons. Because commercially available traps vary in ways that affect the catch, the group makes their own. Named for the Swedish entomologist René Malaise, who developed the basic design in the 1930s, each trap resembles a floating tent. Black mesh fabric forms the base, topped by a tent of white fabric and, at the summit, a collection container—a plastic jar with an opening into another jar of alcohol. Insects trapped in the fabric fly up to the jar, where the vapors gradually inebriate them and they fall into the alcohol. The traps collect mainly species that fly a meter or so above the ground. For people who worry that the traps themselves might deplete insect populations, Sorg notes that each trap catches just a few grams per day—equivalent to the daily diet of a shrew. Sorg says society members saved all the samples because even in the 1980s they recognized that each represented a snapshot of potentially intriguing insect populations. "We found it fascinating—despite the fact that in 1982 the term ‘biodiversity' barely existed," he says. Many samples have not yet been sorted and cataloged—a painstaking labor of love done with tweezers and a microscope. Nor have the group's full findings been published. But some of the data are emerging piecemeal in talks by society members and at a hearing at the German Bundestag, the national parliament, and they are unsettling. Beyond the striking drop in overall insect biomass, the data point to losses in overlooked groups for which almost no one has kept records. In the Krefeld data, hover flies—important pollinators often mistaken for bees—show a particularly steep decline. In 1989, the group's traps in one reserve collected 17,291 hover flies from 143 species. In 2014, at the same locations, they found only 2737 individuals from 104 species. Since their initial findings in 2013, the group has installed more traps each year. Working with researchers at several universities, society members are looking for correlations with weather, changes in vegetation, and other factors. No simple cause has yet emerged. Even in reserves where plant diversity and abundance have improved, Sorg says, "the insect numbers still plunged." Changes in land use surrounding the reserves are probably playing a role. "We've lost huge amounts of habitat, which has certainly contributed to all these declines," Goulson says. "If we turn all the seminatural habitats to wheat and cornfields, then there will be virtually no life in those fields." As fields expand and hedgerows disappear, the isolated islands of habitat left can support fewer species. Increased fertilizer on remaining grazing lands favors grasses over the diverse wildflowers that many insects prefer. And when development replaces countryside, streets and buildings generate light pollution that leads nocturnal insects astray and interrupts their mating. Neonicotinoid pesticides, already implicated in the widespread crash of bee populations, are another prime suspect. Introduced in the 1980s, they are now the world's most popular insecticides, initially viewed as relatively benign because they are often applied directly to seeds rather than sprayed. But because they are water soluble, they don't stay put in the fields where they are used. Goulson and his colleagues reported in 2015 that nectar and pollen from wildflowers next to treated fields can have higher concentrations of neonicotinoids than the crop plants. Although initial safety studies showed that allowable levels of the compounds didn't kill honey bees directly, they do affect the insects' abilities to navigate and communicate, according to later research. Researchers found similar effects in wild solitary bees and bumble bees. Less is known about how those chemicals affect other insects, but new studies of parasitoid wasps suggest those effects could be significant. Those solitary wasps play multiple roles in ecosystems—as pollinators, predators of other insects, and prey for larger animals. A team from the University of Regensburg in Germany reported in Scientific Reports in February that exposing the wasp Nasonia vitripennis to just 1 nanogram of one common neonicotinoid cut mating rates by more than half and decreased females' ability to find hosts. "It's as if the [exposed] insect is dead" from a population point of view because it can't produce offspring, says Lars Krogmann, an entomologist at the Stuttgart Natural History Museum in Germany. No one can prove that the pesticides are to blame for the decline, however. "There is no data on insecticide levels, especially in nature reserves," Sorg says. The group has tried to find out what kinds of pesticides are used in fields near the reserves, but that has proved difficult, he says. "We simply don't know what the drivers are" in the Krefeld data, Goulson says. "It's not an experiment. It's an observation of this massive decline. The data themselves are strong. Understanding it and knowing what to do about it is difficult." The factors causing trouble for the hover flies, moths, and bumble bees in Germany are probably at work elsewhere, if clean windshields are any indication. Since 1968, scientists at Rothamsted Research, an agricultural research center in Harpenden, U.K., have operated a system of suction traps—12-meter-long suction tubes pointing skyward. Set up in fields to monitor agricultural pests, the traps capture all manner of insects that happen to fly over them; they are "effectively upside-down Hoovers running 24/7, continually sampling the air for migrating insects," says James Bell, who heads the Rothamsted Insect Survey. Between 1970 and 2002, the biomass caught in the traps in southern England did not decline significantly. Catches in southern Scotland, however, declined by more than two-thirds during the same period. Bell notes that overall numbers in Scotland were much higher at the start of the study. "It might be that much of the [insect] abundance in southern England had already been lost" by 1970, he says, after the dramatic postwar changes in agriculture and land use. The stable catches in southern England are in part due to constant levels of pests such as aphids, which can thrive when their insect predators are removed. Such species can take advantage of a variety of environments, move large distances, and reproduce multiple times per year. Some can even benefit from pesticides because they reproduce quickly enough to develop resistance, whereas their predators decline. "So lots of insects will do great, but the insects that we love may not," Black says. Other, more visible creatures may be feeling the effects of the insect losses. Across North America and Europe, species of birds that eat flying insects, such as larks, swallows, and swifts, are in steep decline. Habitat loss certainly plays a role, Nocera says, "but the obvious factor that ties them all together is their diet." Some intriguing, although indirect, clues come from a rare ecological treasure: decades' worth of stratified bird droppings. Nocera and his colleagues have been probing disused chimneys across Canada in which chimney swifts have built their nests for generations. From the droppings, he and his colleagues can reconstruct the diets of the birds, which eat almost exclusively insects caught on the wing. The layers revealed a striking change in the birds' diets in the 1940s, around the time DDT was introduced. The proportion of beetle remains dropped off, suggesting the birds were eating smaller insects—and getting fewer calories per catch. The proportion of beetle parts increased slightly again after DDT was banned in the 1970s but never reached its earlier levels. The lack of direct data on insect populations is frustrating, Nocera says. "It's all correlative. We know that insect populations could have changed to create the population decline we have now. But we don't have the data, and we never will, because we can't go back in time." Sorg and Wägele agree. "We deeply regret that we did not set up more traps 20 or 30 years ago," Sorg says. He and other Krefeld society members are now working with Wägele's group to develop what they wish they had had earlier: a system of automated monitoring stations they hope will combine audio recordings, camera traps, pollen and spore filters, and automated insect traps into a "biodiversity weather station". Instead of tedious manual analysis, they hope to use automated sequencing and genetic barcoding to analyze the insect samples. Such data could help pinpoint what is causing the decline—and where efforts to reverse it might work best. Paying attention to what E. O. Wilson calls "the little things that run the world" is worthwhile, Sorg says. "We won't exterminate all insects. That's nonsense. Vertebrates would die out first. But we can cause massive damage to biodiversity—damage that harms us."

Wesener T.,Leibniz Institute for Animal Biodiversity
Invertebrate Systematics | Year: 2014

Cyliosoma Pocock, 1895, the oldest available genus name for Australian giant pill-millipedes, is revised with a redescription of its type species, Sphaerotherium angulatum Butler, 1878. All 16 species of Epicyliosoma Silvestri, 1917 are transferred to Cyliosoma, together with two species, Sphaerotherium fraternum Butler, 1872 and S. marginepunctatum Karsch, 1881, which are redescribed here. A new phylogenetic analysis of the Sphaerotheriida was conducted using 100 morphological characters and including two Cyliosoma species and four recently described or redescribed species of the family Zephroniidae. Most character states are illustrated for Cyliosoma, including the first SEM images of a member of the genus. Cyliosoma is neither closely related to the South African Sphaerotherium, nor to the other Australian genus, Procyliosoma, and is here placed in a new family, Cyliosomatidae. The monotypic Australian genus Cynotelopus Jeekel, 1986 is also referred to the Cyliosomatidae. The current position of the Cyliosomatidae is in a trichotomy including the South African Sphaerotheriidae and the Malagasy-Indian Arthrosphaeridae. © CSIRO 2014.

Wesener T.,Leibniz Institute for Animal Biodiversity
Revue Suisse de Zoologie | Year: 2014

The first records of the colobognathan millipede order Siphonophorida from Madagascar and Mauritius are presented. Specimens representing both families of the order, Siphonophoridae and Siphonorhinidae, were discovered on Madagascar. The specimens were collected from 18 rainforest and montane rainforest localities using primarily the Winkler or Berlese extraction methods. The limited number of specimens (mostly less than 5) available from each site and the difficult taxonomic state of the order prevented the naming of any of the specimens. Specimens from one locality could be studied in more detail using SEM, and were tentatively determined as members of the Asian genus Siphonorhinus Pocock, 1894, presently known only from Asia. Four additional Siphonophorida samples representing at least two different species came from three localities on Mauritius, providing the first record of the order from the island. All Siphonophorida specimens should be carefully examined before taxonomic description attempts, as some might represent widespread tropical tramps.

Blanke A.,Leibniz Institute for Animal Biodiversity | Wesener T.,Leibniz Institute for Animal Biodiversity
Arthropod Structure and Development | Year: 2014

The external and internal anatomy of millipedes (Diplopoda) is poorly known compared to some of the other myriapod and arthropod groups. Due to both language barriers, which hindered the assessment of the character-rich older literature, and non-phylogenetic thinking, our knowledge of morphological characters useful for phylogenetic work diminished over the last decades. Here, a new character matrix with 64 characters, mainly derived from old literature data, is used to reconstruct a phylogeny of Diplopoda. As a tool to further our knowledge about the morphology of the different millipede orders, we show how micro-computer tomography (μCT) can be used to assess and illustrate specific parts of the Platydesmida. With the advent of μCT it is now possible to analyse many taxa and characters in a comparatively short time. A focus is put on potential phylogenetically useful characters. Our results support a Verhoeffian classification of the Diplopoda: Polyxenida + Chilognatha. Pentazonia are the sistergroup to the Helminthomorpha. Colobognatha form the sistergroup to Eugnatha, the latter split into monophyletic Juliformia and Polydesmida + Nematophora. © 2013 Elsevier Ltd.

Freyhof J.,Leibniz Institute for Animal Biodiversity
Ichthyological Exploration of Freshwaters | Year: 2014

Acanthobrama thisbeae, new species, is described from the lower Ceyhan and Orontes Rivers in Turkey. It is distinguished from other species of the genus by having 73-86/3-4 scales along the lateral line, a thin and short last unbranched dorsal-fin ray, flank scales with a crenulated posterior margin, and 14-16% branched anal-fin rays. Acanthobrarna orontis is a valid species distributed in the Orontes, Ceyhan and Seyhan rivers. Eleven species are recognised as valid in the genus Acanthobrania (A. centisquarna, A. hadiyahensis, A. lissneri, A. inarmid, A. microlepis, A. orontis, A. persidis, A. telavivensis, A. thisbae, A. tricolor, A. urmianus). Acanthalburnus is treated as a synonym of Acanthobrarna. © 2014 by Verlag Dr. Friedrich Pfeil, München, Germany.

The Italian pill millipede species Glomeris apuana Verhoeff, 1911, is redescribed from fresh material and its COI barcoding fragment is sequenced. The new specimens were compared to the original type series, of which a lectotype was selected. G. apuana was apparently still viewed as a subspecies of G. ligurica, as its name cannot be found in 'Fauna Europaea', or any faunal lists or catalogues in the last 85 years. We show that the species is both genetically and morphologically unique. G. apuana is easy to identify based on its entirely black coloration in combination with the absence of any main striae on the thoracic shield. Genetically, G. apuana shows large p-distances of >10% to four different populations of G. ligurica Latzel, 1884. G. apuana also differs from other sequenced Glomeris species, G. marginata Latreille, 1803, G. connexa Koch, 1847, and G. klugii Brandt, 1833 by p-distances of >10%. Specimens of G. klugii from a population occurring in sympatry with G. apuana were newly sequenced. All records of G. apuana, a large, easy to identify and conspicuous species, are from a narrow coastal zone of the Apuan Alps, an area in which the species might be microendemic.

Polyzonium malagassum de Saussure & Zehntner, 1902, the only indigenous record of the order Polyzoniida from Madagascar, is redescribed after a study of the type specimens. The only male specimen is selected as the lectotype and illustrated. P. malagassum is discovered to be a synonym of the widespread tropical tramp species Rhinotus purpureus (Pocock, 1894). A mapping of additional locality data of R. pupureus shows that the species is widespread in Malagasy rainforests and montane rainforests, and occurs locally in high densities. Seven potentially indigenous Polyzoniida morphospecies also occur on Madagascar, but these undescribed species are more localized and show a lower abundance than R. purpureus. Brief notes, locality data, and Museum acronyms are given for the undescribed Polyzoniida species, which will hopefully assist future studies on Malagasy representatives of this little-known but biogeographically interesting order. With the discovery of the ubiquitous presence of R. purpureus on Madagascar, the similarity of the defense secretions of South American and of endemic Malagasy poison dart frogs (family Mantellidae) might derive from the fact that both groups prey on and sequester alkaloids from the same species of millipede. Copyright © 2014 Magnolia Press.

Wesener T.,Leibniz Institute for Animal Biodiversity
Zootaxa | Year: 2015

The type of the only species of the order Sphaerotheriida with a record in Nepal, Kophosphaera excavata (Butler, 1874), originally described from Sikkim, is redescribed. The subspecies K. excavata mammifera Attems, 1936 from Sureil, Darjeeling, India, is elevated to species rank, K. mammifera stat. nov.. A species of unclear country of origin ('Himalaya'), Sphaeropoeus montanus Karsch, 1881, is briefly redescribed and transferred to the genus Zephronia, Z. montana (Karsch, 1881) n. comb.. Z. tumida Butler, 1882, an apparently widespread north Indian Zephronia species, is redescribed. Sphaerotheriida specimens collected during several expeditions to Nepal undertaken by Prof. J. Martens in the 1970s and 1980s were examined. The material contained 10 specimens (7 males, 3 females) from seven localities, including three undescribed species, Zephronia nepalensis n. sp., Kophosphaera shivapuri n. sp., and Kophosphaera martensi n. sp., as well as a specimen of Kophosphaera politissima Attems, 1935, type species of the genus and described previously from India. A key to all (now seven) species of Kophosphaera is presented. A brief diagnosis of the Kophosphaera excavata group is provided. While Zephronia seems to be restricted to the eastern part of Nepal, two endemic and two more widespread Kophosphaera species occur also in its central and mid-western part, representing the western-most records of the family Zephroniidae in Asia. The current distribution of the family in Nepal clearly indicates the Zephroniidae as a family adapted to tropical environments. Copyright © 2015 Magnolia Press.

In order to evaluate the status of the only species of pill millipede (Glomerida) endemic to Germany, Glomeris malmivaga Verhoeff, 1912, a DNA barcoding study based on the COI mitochondrial gene was conducted. Sequences of G. malmivaga were compared to those of G. ornata Koch, 1847 from Slovenia, of which the former was previously described as a variety of the latter before being elevated to subspecies- and, recently, species-rank. Included in the analysis were specimens of G. helvetica Verhoeff, 1894, also originally described as a variety of G. ornata, which was supposed to be closely related to G. malmivaga based on its morphology, as well as geographical proximity of occurrence. Additionally, G. valesiaca Rothenbühler, 1899, which occurs in sympatry and looks quite similar to G. helvetica was also sequenced for the first time and included in the study. Sequences of four widespread Glomeris species, all occurring in close proximity to G. malmivaga, G. marginata Villers, 1789, G. connexa Koch, 1847, G. klugii Brandt, 1833 and G. intermedia Latzel, 1884 were downloaded from Genbank and incorporated in the analysis. While G. helvetica and G. valesiaca were found to be clearly separate from G. ornata (11.8-14.6% p-distance), G. malmivaga is almost identical to the latter (0.5% p-distance), despite the large geographical distance between both species. Because of their great morphological and genetical similarity, G. malmivaga n. syn. is synonymised under G. ornata. Copyright © 2015 Magnolia Press.

Burghardt I.,College St | Wagele H.,Leibniz Institute for Animal Biodiversity
Journal of Molluscan Studies | Year: 2014

For the first time, specimens of the nudibranch Melibe engeli hosting zooxanthellae (Symbiodinium spp.) were cultured for more than 9 months in aquaria in order to study this symbiotic system. Melibe engeli, in contrast to other previously studied 'solar-powered' nudibranchs, does not obtain its symbionts by feeding on prey that house Symbiodinium, but as by-catch from the water column. Specimens were exposed to different experimental conditions (nonfeeding vs feeding, light vs darkness) to estimate the efficiency of this putative mutualistic symbiosis. Photosynthetic efficiency of Symbiodinium measured by means of PAM fluorometry remained high, independent of experimental treatment. Specimens kept under nonfeeding conditions survived the whole experimental period, grew to modest size and laid fertile egg clutches continuously. Specimens fed additionally with crustaceans and turbellarians grew faster and larger and laid more egg clutches, implying higher fecundity. Symbiodinium density was higher in fed specimens, but is potentially regulated actively by M. engeli through various mechanisms. Fed specimens kept in continuous darkness died relatively soon, suggesting that light is crucial for survival. Histological analyses revealed specialized morphological structures of the digestive gland ('cisternae' and 'fine tubuli') that house Symbiodinium. These data suggest an advanced state of mutualistic symbiosis that enables M. engeli to survive times of food shortage. © 2014 The Author.

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