Article

Taxonomy, natural history and immature stages of the bone-skipper, Centrophlebomyia furcata (Fabricius) (Diptera: Piophilidae, Thyreophorina)

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Abstract

Centrophlebomyia furcata (Fabricius) is rediscovered (in Israel) after not being found for about 100 years. Thyreolepida cinerea Sack from Israel is found to be congeneric and conspecific (new synonym). Field and laboratory observations on this species are reported. The egg, third instar larva and puparium are described for the first time in the Thyreophorina. Relationships of the Thyreophorina within the Piophilidae are discussed in view of the new information.

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... The subtribe Thyreophorina contains six genera distributed over the different continents [20]. They are commonly called the 'bone-skippers' due to their attraction to skeletonised remains of big mammalian carcasses and the typical leaping behaviour of the piophilid larvae [64]. Thyreophorines are a peculiar and interesting group among Diptera due to several reasons, such as their intriguing geographical distribution, which could indicate that this subtribe originated in the supercontinent Gondwanaland [6]. ...
... One of them, Centrophlebomyia furcata (Fabricius) was also cited (as 'Musca furcata') occurring on human corpses by Orfila and Lesueur [11], and Mé gnin [12] placed it in the 'fifth squad' together with T. cynophila. C. furcata was considered extinct in Europe during several years [20], but it could be regularly found in Israel [64]. However, in the past years, new records of this species from carcasses have begun to proliferate in the Mediterranean Basin [18,20]; hence, C. furcata does not seem to be particularly rare in this subregion. ...
... However, in the past years, new records of this species from carcasses have begun to proliferate in the Mediterranean Basin [18,20]; hence, C. furcata does not seem to be particularly rare in this subregion. This species is active from November to January [64]; thus, it could be a potentially useful forensic tool for cadavers in advanced stages of decay in cool seasons, as T. cynophila. Furthermore, the other species included in the genus Centrophlebomyia, C. anthropophaga (Robineau-Desvoidy), sometimes cited as Centrophlebomyia orientalis Hendel, actually a synonym of C. anthropophaga [20] should be taken into account. ...
Article
Among the insects which are typically considered of forensic interest, the family Piophilidae (Diptera) is frequently cited because of its common occurrence on carcasses in different stages of decay. Piophilids are mainly known from the cosmopolitan species Piophila casei, which can be also a major pest for the food industry and an agent of myiasis. However, many other species of Piophilidae occur frequently on carrion, including human corpses; hence, it is essential to ensure a careful identification of specimens. Reviews of relevant published information about the Piophilidae species of potential forensic use, including recent interesting records, are presented.
... The scarcity of records, in some cases limited to the original description of the species, is also a common peculiarity of all thyreophorines (Martín-Vega 2011). Moreover, the immature stages of many species remain unknown, and the life cycle and larval morphology have only been described for the species Protothyreophora grunini Ozerov (Ozerov 1984) and Centrophlebomyia furcata (Fabricius) (Freidberg 1981). Like T. cynophila, C. furcata had been considered as extinct in Europe, but curiously it was recently rediscovered in Spain (Gómez-Gómez et al. 2009) and subsequently in other areas of the Mediterranean Basin (Martín-Vega et al. 2010). ...
... Current preliminary observations on both T. cynophila and C. furcata reproductive behaviour are in accordance with those of Freidberg (1981) on laboratory colonies of C. furcata. Although Freidberg (1981) emphasized that no firm conclusions could be drawn from such preliminary observations, he highlighted the larger size of thyreophorine males, an unusual situation among Diptera, as well as manipulation of the male proboscis after copulation, which remains unclear. ...
... Further detailed observations, with special attention to the coexistence and interactions between T. cynophila and C. furcata individuals, should be carried out. Freidberg (1981) observed in a laboratory colony of C. furcata that larvae aestivated in soil as third-instars or pre-pupae, suggesting that pupation would probably be induced by lower temperatures during late summer and autumn. Such observations are in accordance with the present observations on both T. cynophila and C. furcata. ...
Article
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Considered at times as extinct, the European bone-skippers Thyreophora cynophila and Centrophlebomyia furcata (Diptera: Piophilidae) have been recently rediscovered in Spain, coexisting in some areas. Nevertheless, apart from their typical association with big mammal carcasses, little is known about them and the other species of subtribe Thyreophorina. In the present paper, the larval morphology of T. cynophila is described for the first time and compared with that of C. furcata. The morphology of cephalopharyngeal skeleton,
... The three European thyreophorines, Centrophlebomyia furcata (Fabricius, 1794), C. anthropophaga (Robineau-Desvoidy, 1830) and Thyreophora cynophila (Panzer, 1798), were even considered extinct for over a century. All three were rediscovered in the last 30 years, during which almost every record of a thyreophorine was published (Freidberg 1981;Michelsen 1983;Contini and Rivosecchi 1993;Gòmez-Gòmez et al. 2008;Martín-Vega and Baz 2011;Martín-Vega et al. 2010;Carles-Tolrá 2011;Carles-Tolrá et al. 2010, 2011Zaldivar Ezquerro et al. 2011), sometimes with a certain media emphasis (Appendix 1). Despite the aura of exceptionality surrounding these flies, and the excitement their rediscovery has recently raised among dipterists, there is still some confusion concerning their taxonomy and nomenclature. ...
... Preimaginal instars. Described by Freidberg (1981) and below. Distribution. ...
... Description of third instar and puparium. Both the larva and puparium of C. anthropophaga (Figs 30−38) correspond well to features given by McAlpine (1977), Ozerov (2000) and Ozerov and Norrbom (2010) for other piophilids and by Freidberg (1981) for C. furcata. Here we provide additional information not given in previous descriptions. ...
Article
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The European bone-skippers (Diptera: Piophilidae: Thyreophorina), long considered extinct, have recently been the object of much interest by dipterists after their unexpected rediscovery. Considerable faunistic work has been done on these flies in recent years. However, some nomenclatural and taxonomic issues still require attention. A neotype is designated for Thyreophora anthropophaga Robineau-Desvoidy, 1830 (now in the genus Centrophlebomyia Hendel, 1903) to fix the identity of this nominal species. Centrophlebomyia anthropophaga is recognized as a valid species. It is described and illustrated in detail, and information on its preimaginal instars is provided for the first time. Four Palaearctic species of Centrophlebomyia are recognized and reviewed and a key is provided for their identification. Centrophlebomyia orientalis Hendel, 1907 from northern India, is removed from synonymy with Centrophlebomyia anthropophaga and recognized as a valid species of Centrophlebomyia, stat. r. The nominal genus Protothyreophora Ozerov, 1984 is considered a junior synonym of Centrophlebomyia, syn. n.
... The subtribe Thyreophorina is hitherto known to include the following few species currently assigned to five genera: Thyreophora cynophila (Panzer, 1798) from Europe and Algeria, Centrophlebomyia anthropophaga (Robineau-Desvoidy, 1830) from France and Italy, Centrophlebomyia furcata (Fabricius, 1794) from Europe, Turkey, Israel and Algeria, Centrophlebomyia orientalis Hendel, 1907 from northern India (Darjeering and Kashmir), Centrophlebomyia grunini (Ozerov, 1984) from the Far Eastern Russia, Dasyphlebomyia stylata Becker, 1914 from the Ethiopian Region, Piophilosoma antipodum (Osten Sacken, 1811), Piophilosoma norrisi (Paramonov, 1954), and Piophilosoma palpatum Hendel, 1917 from Australia, and Bocainamyia necrophila Albuquerque, 1953 andBocainamyia hagmannarum Papavero, 1971 from the Neotropical Region (McAlpine 1977;Pitkin 1989;Ozerov 1984a;McAlpine 1989;Martín-Vega et al. 2010;Mei et al. 2013). The adults of most species of this subtribe appear during the cold season and their larvae breed mostly in decaying carcasses of large mammals particularly at the final stage of decay (Freidberg 1981;Ozerov 1984b;Martín-Vega & Baz 2011), as a result they are now very rare owing to shortage of such breeding sites in nature (Centrophlebomyia spp. : Freidberg 1981;Michelsen 1983;Cortini & Rivosecchi 1993;Mei et al. 2013); or once considered to be extinct but recently rediscovered in Europe (T. ...
... The adults of most species of this subtribe appear during the cold season and their larvae breed mostly in decaying carcasses of large mammals particularly at the final stage of decay (Freidberg 1981;Ozerov 1984b;Martín-Vega & Baz 2011), as a result they are now very rare owing to shortage of such breeding sites in nature (Centrophlebomyia spp. : Freidberg 1981;Michelsen 1983;Cortini & Rivosecchi 1993;Mei et al. 2013); or once considered to be extinct but recently rediscovered in Europe (T. In February of 2004, Dr. Hirofumi Okido (Kyushu Environmental Evaluation Association, Fukuoka) collected a few male specimens of a moderately large, densely pollinose, long pilose fly by sweep net in an evergreen broadleaved forest at Inokodani (ca. ...
Article
A new genus, Diacanthomyia gen. nov. assigned to the subtribe Thyreophorina of the family Piophilidae is described based on a new species, Diacanthomyia okidoi sp. Nov. recently found in Honshu and Kyushu, Japan. The new genus is somewhat similar to the European Centrophlebomyia of the subtribe. However, the new genus is distinguished from the known genera of the subtribe by the following combination of characters: body extensively pollinose or pruinose, 2 pairs of strong reclinate fronto-orbital bristles, 1-2 strong subvibrissal bristles in addition to 2 strong vibrissae, prosternum setose, 1 presutural dorsocentral, 1 strong anterior postsutural intra-alar, scutellum with 2 pairs of scutellar bristles without additional setulae, extensively microtrichose wing membrane, a dark round spot at r-m crossvein and a dark stripe covering m-m crossvein, and vein CuA+CuP abruptly terminated distant from wing margin. The type species inhabits evergreen broadleaved and deciduous broadleaved forests and adults appear during the cold season from December to March. Adults are attracted to decaying carcasses of Japanese deer and wild boar and traps baited with decaying pork spareribs and chicken meat with bones. The larvae of this species feed on decaying meat and marrow of deer, take less than 2 months to grow to mature larvae, and enter into diapause in the soil until autumn.
... The 'long-extinct' T. cynophila has been collected in 5 of the 11 visited 'vulture restaurants' (Table 1), indicating a more widespread distribution in central Spain than previously known. Although apparently there were no Spanish records of the species prior to the works of Freidberg 1981). The limited number of entomologists surveying in winter, and particularly on carcasses, could be the explanation for the limited knowledge about the distribution of those species (McAlpine 1977). ...
... d knowledge about the distribution of those species (McAlpine 1977). Thyreophorines can be found during the cold season, but what do these species do during the rest of the year? Next to nothing is known about the life cycle of thyreophorines, although Freidberg (1981) succeeded in rearing some individuals of C. furcata under laboratory conditions. Freidberg (1981) observed that larvae of C. furcata overwintered and aestivated in soil as third instars or prepupae, suggesting that pupation in the field would probably be induced by lower temperatures during late summer or autumn, with adults emerging during autumn and winter. Freidberg (1981) also observed that many larvae desiccated and died during ...
Article
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The European bone-skippers Thyreophora cynophila and Centrophlebomyia furcata (Diptera: Piophilidae) had been considered as globally extinct or extinct in Europe, respectively, until their recent rediscovery in Spain. Improved hygienic conditions in livestock management and disposal of large carcasses (the preferred breeding sites for the bone-skippers) have been implicated as the main cause for their disappearance. The decline of many European avian scavenger populations in the last centuries has also been attributed to the same cause, which has promoted the creation of the commonly named ‘vulture restaurants’. Although these supplementary feeding stations are important to support scavenging bird populations, the present work demonstrates that they provide a guaranteed supply of food for rare necrophagous species like the European bone-skippers which have recently been rediscovered. Keywords Thyreophora cynophila – Centrophlebomyia furcata –Carrion–Ecosystem function–Vulture restaurants
... If another male approaches then the "guarding" male will raise his mid legs in the direction of the approacher to ward him off. If the male is very small and all of his legs are preoccupied with holding on to the female, then the female may respond to mounting by raising her mid legs dorsomedially (Freidberg 1981). Prochyliza xanthostoma Walker, 1859, also known as "waltzing flies", have sparring bouts between males, with the two spreading their fore legs and holding on to each other's fore tarsi (much like Abbreviations: acr s -acrostichal setae; dc s -dorsocentral setae; pprn lb -postpronotal lobe; sctl -scutellum. ...
... The sexual behaviour of the antler fly, Protopiophila litigata, has been described previously (see Bonduriansky and Brooks 1998a, 1998b, 1999a, 1999b ) and is summarized briefly in the Results for comparison with that of the other species. Very little is known of the sexual behaviour of any other piophilid species except the synanthropic " cheese skipper " , Piophila casei (Swammerdam 1758; Dufour 1844; Sacchi et al. 1978), and the " bone skipper " , Centrophlebomyia furcata (Freidberg 1981). A sexual-selection mechanism is defined here as any factor that exposes variation among individuals in the performance of tasks associated with competition for mates. ...
Article
Although many theoretical and empirical studies have addressed the dynamics of sexual selection, little is known about the evolution of multiple sexual-selection mechanisms within the same system. I performed a qualitative comparative study of sexual behaviours in seven sympatric species of piophilid flies to identify and compare the appar - ent mechanisms of sexual selection operating in each system. In each of the seven species I observed several distinct types of male-male and male-female interactions, potentially representing multiple mechanisms of sexual selection. Male-male interactions included scramble competition and, in some species, bouts of intense combat. Male-female interactions exhibited two distinct patterns: (1) some form of premounting courtship followed by a simple copulatory sequence or (2) no premounting courtship but palpation behaviours during the copulatory sequence. Either pattern was combined with male-female struggle in some species. In two species, male mating success also appeared to depend on the ability to overcome a "revealing obstacle", a female adaptation that exposed variation in male performance without direct assessment or struggle. In each species these mechanisms operated in a rough sequence and thus could be viewed as "layers" of sexual selection, with each layer potentially reducing the subset of individuals that have opportu - nities to compete in the next layer. A brief review of the literature suggests that layered sexual selection is the typical pattern in many animal groups and thus may have important evolutionary consequences.
... Hasta ese momento, el último registro documentado (SMITH, 1974(SMITH, , 1989 de C. furcata en el continente (Gales, Reino Unido) correspondía a la primera década del siglo XX. Los registros más recientes (FREIDBERG, 1981;STUBBS & CHANDLER, 2001;VIKHREV, 2008) sugieren que la especie mantendría poblaciones viables en Israel, Chipre y el oeste de Turquía. ...
... Invertebrate scavengers would also have been affected by the decline in megafauna diversity, although this is difficult to document. The flies known as bone skippers (Piophilidae: Thyreophorinae) are all necrophagous and associated with large vertebrate carrion, and the larvae have a preference for feeding on the marrow of the long bones (Freidberg, 1981). The three western Palaearctic species were long considered to be extinct until re-discovered in small and scattered populations (Pape, Bickel & Meier, 2009;Martín-Vega, Baz & Michelsen, 2010), where their survival appears to be associated with domestic goats, sheep and equids. ...
Article
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For hundreds of millions of years, large vertebrates (megafauna) have inhabited most of the ecosystems on our planet. During the late Quaternary, notably during the Late Pleistocene and the early Holocene, Earth experienced a rapid extinction of large, terrestrial vertebrates. While much attention has been paid to understanding the causes of this massive megafauna extinction, less attention has been given to understanding the impacts of loss of megafauna on other organisms with whom they interacted. In this review, we discuss how the loss of megafauna disrupted and reshaped ecological interactions, and explore the ecological consequences of the ongoing decline of large vertebrates. Numerous late Quaternary extinct species of predators, parasites, commensals and mutualistic partners were associated with megafauna and were probably lost due to their strict dependence upon them (co-extinctions). Moreover, many extant species have megafauna-adapted traits that provided evolutionary benefits under past megafauna-rich conditions, but are now of no or limited use (anachronisms). Morphological evolution and behavioural changes allowed some of these species partially to overcome the absence of megafauna. Although the extinction of megafauna led to a number of co-extinction events, several species that likely co-evolved with megafauna established new interactions with humans and their domestic animals. Species that were highly specialized in interactions with megafauna, such as large predators, specialized parasites, and large commensalists (e.g. scavengers, dung beetles), and could not adapt to new hosts or prey were more likely to die out. Partners that were less megafauna dependent persisted because of behavioural plasticity or by shifting their dependency to humans via domestication, facilitation or pathogen spill-over, or through interactions with domestic megafauna. We argue that the ongoing extinction of the extant megafauna in the Anthropocene will catalyse another wave of co-extinctions due to the enormous diversity of key ecological interactions and functional roles provided by the megafauna.
... casei . Nevertheless , the number of lobes in anterior spiracles could vary between different individuals of the same species , as well noted by Hennig ( 1943 ) and Freidberg ( 1981 ) . Moreover , it must be taken into account that the observed ranges for P . ...
Article
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Flies of family Piophilidae have been recorded as major pests in the food industry, as agents of human myiasis and typically associated with carcasses in advanced stages of decay, being thus important in forensic entomology. Despite that the cosmopolitan species Piophila casei is the most cited in entomological studies, many other piophilid species develop on both carrion and animal products from the food industry. One of those species is Prochyliza nigrimana, widely distributed throughout the Holarctic and Neotropical regions. In this study, the morphological features of the immature stages of P. nigrimana are described for the first time and compared with those of P. casei. The third-instar larvae and puparium of P. nigrimana are significantly shorter than those of P. casei; the contrary pattern is observed in egg length. The number and arrangement of the lobes of anterior spiracles, which had been used as a distinctive character of P. casei in some keys, are the same in both species. Morphological features of the cephaloskeleton (such as the general shape and the distance between the tips and the base of the mouth hooks/base of the mouth hooks ratio), the arrangement of anal segment in third-instar larvae and the appearance of the ventral creeping welts in the puparium are the main characters allowing for identification of both species.
... However, from 1906 onwards to 2004 no records were made of this fly in Europe, and several countries have declared it extinct. However, Freidberg (1981) reported that in Israel C. furcata could be found regularly on car- casses of goat, sheep and cow from November to January. Furthermore, he established that the male holotype from Palestine, upon which Sack (1939) based his description of a new genus and species, Thyreolepida cinerea, is actu- ally a female of C. furcata. ...
Article
We report on a sensational find in central Spain of six specimens of Thyreophora cynophila (Panzer, 1798), a colourful, strange-looking piophilid fly living on carcasses of big mammals in advanced stages of decay. Published data suggest that the species is known exclusively from central western Europe (Germany, Austria and France), and was observed last near Paris, France, in the late 1840s, i.e. more than 160 years ago. Accordingly, T. cynophila was placed in 2007 as the only dipteran on a list of recent European animals considered to be globally extinct. Collection-based data from all 16 known extant specimens found in seven European natural history museums revealed a specimen without date of T. cynophila from Algiers, Algeria. The status of the three thyreophorine piophilids known from Europe is summarized. For the smallest species we reinstate the name Centrophlebomyia anthropophaga (Robineau-Desvoidy, 1830) with Centrophlebomyia orientalisHendel, 1907 as a subjective junior synonym (syn.n.). We speculate as to why thyreophorines, and T. cynophila in particular, have evaded detection for so long.
Article
Observations suggesting that mature larvae of some carrion flies (Piophilidae) tend to leap off carcasses during rain motivated an investigation of the ontogeny and possible functions of larval leaping behaviour and larval responses to two stimuli associated with rain: moisture and sound. These behaviours were investigated in larvae of Prochyliza xanthostoma Walker (Diptera: Piophilidae) by means of laboratory and field observations and experiments. Mature larvae left their feeding substrates (rotting meat) in response to either moisture or rattling sound. The response to moisture was exhibited also by immature larvae. Once on the carcass surface, however, only mature larvae leaped off and pupated in the surrounding soil. The response to sound and the ability to leap only appeared late in larval development and were lost in the prepupal stage. Because rain may facilitate larval locomotion on carcass surfaces, and leaping appears to represent a more rapid and efficient means of leaving a carcass than creeping, these responses may reduce the metabolic costs and predation risks experienced by mature larvae moving to pupation sites in the soil. Thus, the ability to leap and the responses to moisture and sound may represent “ontogenetic adaptations” associated with a brief stage of larval development.
Thesis
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Medico-legal entomology is a part of forensic science that uses necrophagous insects found at the scene as scientific evidence. The insect identification is mandatory in medico-legal entomology because it is critical to validate and estimate Minimum Postmortem Interval (mPMI), and so far, researchers have well established morphological and molecular classification of necrophagous Calliphoridae and Sarcophagidae (Diptera) fly species. Phoridae and Piophilidae flies, which are believed to be less important than the aforementioned groups, are very often found in corpses at the actual crime scenes but classification studies of these groups have not been established nor any professional taxonomist studied them in Korea. As a result, necrophagous Phoridae species studies are left unrecorded and the Piophilidae remains uncatalogued in south-Korea. Researchers around the world also suffer the same deficiency of classification; the NCBI Genbank, the National Institutes of Health’s genetic information database, does not have enough reference nucleotide sequence for these classifications. Taxonomic confirmation of these collected species is very critical, and this study is intended to identify the insect fauna of these classification using the morphological characteristics and molecular strategy.
Article
“[We are aware] of the general lack of information and knowledge regarding biological diversity and of the urgent need to develop scientific, technical, and institutional capacities to provide the basic understanding upon which to plan and implement appropriate measures.” (from the The United Nations “Earth Summit” Conference on Environment and Development, Rio de Janeiro. 1992).
Article
Some recent models suggest a new role for evolutionary arms races between males and females in sexual selection. Female resistance to males is proposed to be driven by the direct advantage to the female of avoiding male-imposed reductions in the number of offspring she can produce, rather than by the indirect advantage of selecting among possible sires for her offspring, as in some traditional models of sexual selection by female choice. This article uses the massive but hitherto under-utilized taxonomic literature on genitalic evolution to test, in a two-step process, whether such new models of arms races between males and females have been responsible for rapid divergent evolution of male genitalia. The test revolves around the prediction that‘new arms races’are less likely to occur in species in which females are largely or completely protected from unwanted sexual attentions from males (e.g. species which mate in leks or in male swarms, in which males attract females from a distance, or in which females initiate contact by attracting males from a distance).
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