Aug 10, 2011 - Could the 'vulture restaurants' be a lifeboat for the recently rediscovered bone-skippers (Diptera: Piophilidae)?. Daniel Martın-Vega ⢠Arturo ...
J Insect Conserv (2011) 15:747–753 DOI 10.1007/s10841-011-9429-0
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Could the ‘vulture restaurants’ be a lifeboat for the recently rediscovered bone-skippers (Diptera: Piophilidae)? Daniel Martı´n-Vega • Arturo Baz
Received: 26 May 2011 / Accepted: 22 July 2011 / Published online: 10 August 2011 Ó Springer Science+Business Media B.V. 2011
Abstract 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
Introduction Described as the first dipteran eradicated by humans (Courtney et al. 2009), the European bone-skipper Thyreophora cynophila (Panzer 1798) (Diptera: Piophilidae: Thyreophorina) has been an emblematic species considered as globally extinct (Fontaine et al. 2007). Nevertheless, surviving populations of T. cynophila were recently D. Martı´n-Vega (&) A. Baz Departamento de Zoologı´a y Antropologı´a Fı´sica, Universidad de Alcala´, 28870 Alcala´ de Henares, Madrid, Spain e-mail: daniel.martinve@uah.es
discovered in the Iberian Peninsula (Carles-Tolra´ et al. 2010; Martı´n-Vega et al. 2010), a region where it has not been previously recorded (although see ‘‘Discussion’’). Until 2010, the known historic distribution of T. cynophila covered Germany and France, where the species has not been recorded since 1849, as well as Austria and Algeria, where it has been recorded only from old pinned specimens without dates, preserved in Naturhistorisches Museum of Vienna (Martı´n-Vega et al. 2010). In view of this, it comes as no surprise that there is a lack of information about the biology of T. cynophila, with the exception of its strange winter phenology and its attraction to large mammal carcasses in advanced stages of decay (e.g., RobineauDesvoidy 1842). Thyreophora cynophila has probably disappeared from its early known distribution area, and it has been suggested that the limited availability of large mammal carcasses due to changes in livestock management and improved carrion disposal, as well as to the impoverishment of the megafauna in Europe, could have driven the species to extinction (Fontaine et al. 2007; Courtney et al. 2009). Furthermore, two other ‘thyreophorines’ have been recorded from Europe in the past, and both species are also considered as probably extinct in Europe: Centrophlebomyia anthropophaga (Robineau-Desvoidy 1830) is a poorly known species only recorded from France, India and Italy, while Centrophlebomyia furcata (Fabricius 1794) has been found in several European countries, as well as in Algeria and Israel (see Martı´n-Vega et al. 2010 for a review). Curiously, C. furcata, like T. cynophila, was recently rediscovered in central Spain (Go´mez-Go´mez et al. 2009). Improved hygienic conditions in the disposal of large carcasses have also been suggested as the main cause of the apparent disappearance of this species in some countries (Go´mez-Go´mez et al. 2009).
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The low densities of wild ungulates and the removal of dead livestock have also been implicated in the disappearance of many avian scavengers from several regions of Europe during the last two centuries (Margalida et al. 2010). Spain still holds the largest populations of avian scavengers in Europe due to both legal protection and high livestock carcasses availability maintained until the second half of the twentieth century (Dona´zar et al. 2010). However, the crisis of bovine spongiform encephalopathy (BSE) meant the implementation of strict laws in the European Union at the beginning of the twenty-first century with the aim of guaranteeing the disposal of animal by-products, thus depriving scavenger bird populations of the resources they depend on to survive (Dona´zar et al. 2010; Margalida et al. 2010). Subsequent regulations have allowed the maintenance of some supplementary feeding stations, commonly named ‘vulture restaurants’, in order to protect and conserve scavenger bird populations. Regrettably, the low number and patchy distribution of these feeding stations, as well as their high economic cost, makes these feeding stations less than ideal for supporting avian scavengers (Margalida et al. 2010). Moreover, supplementary feeding stations are located at permanent places, but the periodicity of the supply of carrion varies depending on the type of management (see ‘‘Sampling sites and methods’’). Additional information about the use and management procedures of the ‘vulture restaurants’ in Spain can be found in Fundacio´n CBD-Ha´bitat (2010). The recent discovery of T. cynophila and C. furcata populations in Spain, where vulture populations had been Fig. 1 Sampled ‘vulture restaurants’ at central Spain. Information for each numbered locality is given in Table 1
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well conserved until now, together with the parallels between the disappearance of these fly species and that of scavenger birds from many European regions, lead us to think that ‘vulture restaurants’ could also serve as a supply of food for thyreophorine populations and as sites where the species could be easily found. In this sense, ‘vulture restaurants’ could be important not only for scavenging birds conservation but also to support and maintain an important part of the insect community associated with the decomposition of animal carrion.
Sampling sites and methods Eleven supplementary feeding stations of central Spain (Figs. 1, 2) were visited from January 2011 to March 2011 with the aim to find new T. cynophila and C. furcata populations. Information about the location, carrion source and protection status of the sampled sites can be found in Table 1. The periodicity of the supply of carcasses in the sampled feeding stations depends on their typology and kind of management. Thus, in the feeding stations associated with livestock farming (sampling site 7 in Table 1) and slaughterhouses, (sampling sites 2, 5 and 9 in Table 1) or managed by civil services (sampling sites 1, 3, 4 and 10 in Table 1), the carrion is supplied weekly. In those feeding stations associated with hunting grounds (sampling site 6 in Table 1), the periodicity of the supply of carrion is determined by the hunting season. The frequency of the supply of carrion in the feeding stations managed by conservation
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Fig. 2 a General view of the ‘vulture restaurant’ in Montejo de la Vega (Natural Park ‘Hoces del Rı´o Riaza’). b General view of the ‘vulure restaurant’ in Checa (Guadalajara). c Thyreophora cynophila on carrion in the ‘vulture restaurant’ of Galve de Sorbe (Guadalajara). d Thyreophora cynophila in the ‘vulture restaurant’ in Checa (Guadalajara). Photos by Marco Antonio Nieto
organizations (sampling sites 8 and 11 in Table 1) is determined by their financial resources so can be very variable. Land use percentages for each locality (Table 1) were obtained from the CORINE Land Cover 2000 Project (Spanish Ministerio de Fomento). In every feeding station, animal carcasses were examined (see Table 1 for sampling times), paying special attention to skulls, where more individuals of T. cynophila and C. furcata could be found. Adults of T. cynophila and C. furcata were easily caught with forceps, and a maximum number of 10 living individuals were collected at each site. Dead specimens (some mortality may be due to excessively cold conditions) were collected too. Collected specimens were preserved in 80% ethanol and deposited in the collection of the Department of Zoology and Physical Anthropology of the University of Alcala´.
Results A total of 40 T. cynophila individuals were collected at the following sites (Table 1): Pelegrina (2 living males); Galve
de Sorbe (7 living males, 2 living females, 10 dead males, 3 dead females); Checa (7 living males, 3 living females, 1 dead female); Montejo de la Vega de la Serrezuela (2 living males, 1 living female) and Valsaı´n (1 living male, 1 living female). A total of 10 C. furcata individuals were collected at the following sites (Table 1): Finca El Castan˜ar (5 living males, 2 living females) and Montejo de la Vega de la Serrezuela (1 living male, 2 living females). For both species, some additional living individuals were observed at each site but not collected. Most of the specimens were found in the crevices of mammal skulls. Along with T. cynophila and C. furcata specimens, adults from Calliphora vicina (Robineau-Desvoidy) (Diptera: Calliphoridae), Necrobia rufipes (De Geer), Necrobia violacea (L.) (Coleoptera: Cleridae), Nitidula flavomaculata Rossi (Coleoptera: Nitiduliidae), Thanatophilus rugosus (L.), Thanatophilus ruficornis (Kuster) (Coleoptera: Silphidae), Mesochelidura bolivari (Dubrony) (Dermaptera: Forficulidae) and unidentified Heleomyzidae and Sphaeroceridae species (Diptera) and Staphylinidae species (Coleoptera) were also collected on animal carcasses. All these taxa are commonly associated with carrion. No individuals of
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123
Guadalajara
Guadalajara
Toledo
Segovia
Segovia
Segovia
Galve de Sorbe
Checa
Molina de Arago´n
Finca El Castan˜ar
Ayllo´n
Montejo de la Vega de la Serrezuela San Pedro de Gaı´llos
Valsaı´n
El Espinar
3
4
5
6
7
8
10
11
Segovia
Segovia
11-032011
11-032011
07-032011
07-032011
07-032011
28-022011
21-022011
21-022011
21-012011
21-012011
21-012011
Date
Non-protected
Protected public forest
Non-protected
Natural Park
Non-protected
Hunting property
Non-protected
Natural Park
Natural Park
Non-protected
Natural Park
Protection status
U Urban, F farmland, G grassland, B bushland, W woodland
9
Guadalajara
Sigu¨enza
2
Guadalajara
Guadalajara
Pelegrina
1
Province
Locality
Ref.
1,356
1,477
945
987
992
729
1.189
1,555
1,460
1,088
1,102
Elevation (m)
Horses
Horses
Rabbits and sheep
Sheep, domestic pigs and mules
Domestic pigs and calves
Red deer, sheep, pigs and mouflon
Rabbits and sheep
Red deer and sheep
Sheep
Wild boar and donkeys
Sheep and goats
Carrion source
0
0.02
0.58
0.09
0.33
0
2.78
0
0.42
1.8
0.3
U
0
0
83.39
28.43
94.99
75.1
63.3
15.05
1.11
21.52
15.72
F
Land use
0
0.74
0
0
0
0
0
0
10.28
0
2.72
G
97.25
36.66
7.35
57.22
3.76
24.9
33.92
69.01
37.56
53.12
55.60
B
2.75
62.58
8.69
14.26
0.92
0
0
15.94
50.63
23.56
25.66
W
-
?
-
?
-
-
-
?
?
-
?
Thyreophora cynophila
-
-
-
?
-
?
-
-
-
-
-
Centrophlebomyia furcata
Table 1 Location, date of sampling, protection status, carrion source and percentages of land use for sampled ‘vulture restaurants’, showing the presence (?) or absence (-) for both thyreophorine species at each locality
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T. cynophila and C. furcata were collected at the localities of Molina de Arago´n, Ayllo´n, San Pedro de Gaı´llos and El Espinar (Table 1).
Discussion 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 Carles-Tolra´ et al. (2010) and Martı´n-Vega et al. (2010), it is worth recalling that Rı´os (1902) included this species in his observations about insects on dead corpses which were very likely to have been examined in Zaragoza province (north of Spain), where Rı´os worked as anatomist. Regrettably, he did not offer concrete geographical nor seasonal data, so such observations must be taken with caution. In any case, it is obvious that T. cynophila is relatively widespread in central Spain, with some wild populations which had went unnoticed during the last centuries. In fact, the records of all the species of subtribe Thyreophorina are really scarce, although Paramonov (1954) noted that Australian thyreophorines are not particularly rare in nature, but only rarely collected. An analogous case occurs with C. furcata, which appeared to be very rare in Europe but relatively common on livestock carcasses in Israel from November to January (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). 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 summer, which suggest that high mortality rates could occur during this life stage. Thyreophora cynophila and C. furcata appear to be present in several localities, but the low number of adult specimens observed and collected in the present work, indicates these are low density species. Additionally, they occur with other abundant carrion-feeding insects. Thus, the low number of T. cynophila specimens collected by Martı´n-Vega et al. (2010) in carrion-baited traps contrasted enormously with the number of captures of other sarcosaprophagous flies.
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The same pattern was observed by Go´mez-Go´mez et al. (2009), who only collected a single specimen of C. furcata on a pig carcass in a carrion succession study in central Spain. The low density of both species could be due to their apparent specialization in the consumption of only large mammal carcasses in contrast to other carrion flies which also can exploit carcasses of different sizes, thus making thyreophorines ecologically rare species (Fontaine et al. 2007). This situation would be analogous again to that of vultures, which are specialized in the consumption of large carcasses opposite other scavenger birds which are more polyphagous (Dona´zar et al. 2010). The low availability of large mammal carcasses in the field is of concern with serious consequences for many scavenger species in the long-term (Dona´zar et al. 2010). The BSE crisis in Europe has been the coup de graˆce to a problem which began with the progressive abandonment of traditional farming practices like transhumance, which traditionally left fallen stock for carrion feeders. Historically, avian scavengers had always been abundant throughout the Mediterranean Basin (Margalida et al. 2010) benefitting from transhumance, which has been a common practice for centuries in this geographical subregion (Ruiz and Ruiz 1986). A similar relationship between thyreophorines and such traditional farming practices may have occurred as well. In fact, published literature and successive evidence indicates that European thyreophorines could be relatively widespread in the Mediterranean subregion (see Martı´n-Vega et al. 2010 for a review). Large herbivores and transhumance benefit ecosystem conservation in many different ways (Ruiz and Ruiz 1986; Van Wieren 1995), one of which is the supply of livestock carcasses, with a close relationship between vultures and this farming practice (Olea and Mateo-Toma´s 2009). Therefore, it is no surprise that the discovered populations of T. cynophila in Madrid (Martı´n-Vega et al. 2010) and La Rioja provinces (CarlesTolra´ et al. 2010) correspond to Natural Parks with an important tradition of transhumance (Anto´n Burgos 2007). Thyreophora cynophila appears to be a species associated with natural forest systems, as indicated by its occurrence in ‘vulture restaurants’ located in bushlands and woodlands (Table 1). By contrast, C. furcata could be more widespread in more open and modified anthropogenic areas as it shows its occurrence in the ‘vulture restaurant’ located at Finca El Castan˜ar (Table 1) and the single individual collected by Go´mez-Go´mez et al. (2009) at the fringe of an urban environment. In the present study, both thyreophorine species only coexisted in the ‘vulture restaurant’ located at Montejo de la Vega de la Serrezuela which belongs to a region with heterogeneous land use (Table 1). The ecological importance of scavengers and decomposers of carrion within ecosystems is fundamental and impossible to replace. They accelerate the return of
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nutrients to the trophic web and disperse such nutrients over a wide area, thus contributing to the dilution of potentially infective disease foci from dead animals (Braack 1987). Furthermore, carrion supplies an additional nutrient resource for other organisms with a non-necrophagous diet, e.g., some insect pollinators (Baz et al. 2010). Some demonstration projects about the management of animal remains have been recently initiated at Belgium and the Netherlands in order to educate the public on the positive aspects of leaving carcasses within forests, with additional positive results for forensic entomology and research (Vanpoucke et al. 2010). It is important to recognize the high diversity of animals which exploit large carcasses, as well as the essential role that scavengers and decomposers play in ecosystems. In light of the current situation, it is necessary to continue intensive supplementary feeding programmes to support scavenger bird populations (Margalida et al. 2010). Importantly, the present work shows that those feeding stations are useful for maintaining other valuable species like the bone-skippers T. cynophila and C. furcata, which could depend exclusively on large mammal carcasses to survive. Both species have been only collected in ‘vulture restaurants’ located at areas with some kind of protection status (Table 1), which thus could facilitate their future conservation. ‘Vulture restaurants’ are therefore good places to look for thyreophorines in other countries. In this sense, ‘vulture restaurants’ are positive, but they also have disadvantages (Anderson and Anthony 2005; Margalida et al. 2010). They are not the perfect solution, or the only possible solution. An encouragement of wild ungulate populations which would generate naturally a significant amount of carrion could be a supporting strategy (Margalida et al. 2010). A recovering of transhumance which has been demonstrated to have given rise to highly diverse ecosystems (Olea and Mateo-Toma´s 2009) would be also desirable. In the meantime, the design of the net of supplementary feeding stations should be reinforced and redefined. The ‘vulture restaurants’ also benefit other insect species which exploit carcasses, thus maintaining the carrion-feeding community and its important role in ecosystems. Furthermore, such feeding stations can provide opportunities to study poorly known species like the European thyreophorines in depth. In fact, future studies should be focused in obtaining a more detailed mapping of T. cynophila and C. furcata populations and their distribution in Spain, in order to evaluate the real conservation status of two species which fortunately appear to have returned from the dead. Acknowledgments There have been many people who have contributed to this work. We acknowledge the invaluable assistance of Marco Antonio Nieto, curator of the Department of Zoology and Physical Anthropology of the University of Alcala´, whose skills in the management of carcasses have greatly facilitated our work. Others have facilitated access to the ‘vulture restaurants’. In the province of
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J Insect Conserv (2011) 15:747–753 Guadalajara, we are indebted to David Sa´nchez (Director) and Cristina Garcı´a of the General Directorate of Protected Areas and Biodiversity, Juan Sanz, Marı´a Garcı´a Olaya and Ana Marı´a Ballester of the Provincial Service of Protected Areas and Biodiversity of Guadalajara, and Vicente Garcı´a, forestry agent. In the province of Segovia, we thank the efforts of Francisco Sa´nchez Aguado, Director of the Natural Park ‘Hoces del Rı´o Riaza’. El Espinar facilities could be visited through the kindness of Jose´ Aguilera, a member of the collective ‘Campo Aza´lvaro’ which provides food for vultures. Marisol Redondo, responsible biologist for the conservation of flora and fauna in ‘Centro Montes y Aserradero de Valsaı´n’, allowed us access and kindly accompanied us to the ‘vulture restaurant’ of Valsaı´n. Juan Francisco Sa´nchez Rodrı´guez facilitated access to the private estate ‘El Castan˜ar’ in Toledo. We are also grateful to an anonymous reviewer for his comments and suggestions to improve the manuscript and to Tim Shreeve for his revision and corrections on English language. This work has been funded by the Spanish Ministerio de Ciencia y Tecnologı´a (Research Project BOS2003-00400). The authors are members of the IUICP (Instituto Universitario de Investigacio´n en Ciencias Policiales) of the University of Alcala´. DM-V works with a scholarship from the IUICP (Project IUICP/PI2010/ 001).
References Anderson MD, Anthony A (2005) The advantages and disadvantages of vulture restaurants versus simply leaving livestock (and game) carcasses in the veldt. Vulture News 53:42–45 Anto´n Burgos FJ (2007) Trashumancia y turismo en Espan˜a. Cuad Turismo 20:27–54 Baz A, Cifria´n B, Martı´n-Vega D, Baena M (2010) Phytophagous insects captured in carrion-baited traps in central Spain. Bull Insectol 63:21–30 Braack LEO (1987) Community dynamics of carrion-attendant arthropods in tropical African woodland. Oecologia 72:402–409 Carles-Tolra´ M, Rodrı´guez PC, Verdu´ J (2010) Thyreophora cynophila (Panzer, 1794): collected in Spain 160 years after it was thought to be extinct (Diptera: Piophilidae: Thyreophorina). Bol SEA 46:1–7 Courtney GW, Pape T, Skevington JH, Sinclair BJ (2009) Biodiversity of diptera. In: Footit RG, Adler PH (eds) Insect biodiversity: science and society. Wiley-Blackwell, Chichester, pp 185–222 Dona´zar JA, Corte´s-Avizanda A, Carrete M (2010) Dietary shifts in two vultures after the demise of supplementary feeding stations: consequences of the EU sanitary legislation. Eur J Wildl Res 56:613–621 Fabricius JC (1794) Entomologia systematica emendata et aucta. vol 4, Copenhagen Fontaine B, Bouchet P, van Achtherberg K et al (2007) The European union’s 2010 target: putting rare species in focus. Biol Cons 139:167–185 Freidberg A (1981) Taxonomy, natural history and immature stages of the bone-skipper, Centrophlebomyia furcata (Fabricius) (Diptera: Piophilidae, Thyreophorina). Entomol Scand 12:320–326 Fundacio´n CBD-Ha´bitat (2010) Guı´a para la alimentacio´n de aves necro´fagas con subproductos animales no destinados a consumo humano. Obra social caja Madrid. http://www.cbd-habitat.com/ contenidos/informacion/Guia_alimentacion_para_aves_necro fagas.pdf. Accessed 10 July 2011 Go´mez-Go´mez A, Dı´az-Aranda LM, Michelsen V (2009) Rediscovery of Centrophlebomyia furcata (Fabricius, 1794) (Diptera: Piophilidae) in Europe. Studia Dipterol 15(2008):237–241
J Insect Conserv (2011) 15:747–753 Margalida A, Dona´zar JA, Carrete M, Sa´nchez-Zapata JA (2010) Sanitary versus environmental policies: fitting together two pieces of the puzzle of European vulture conservation. J Appl Ecol 47:931–935 Martı´n-Vega D, Baz A, Michelsen V (2010) Back from the dead: Thyreophora cynophila (Panzer, 1798) (Diptera: Piophilidae) ‘globally extinct’ fugitive in Spain. Syst Entomol 35:607–613 McAlpine JF (1977) A revised classification of the Piophilidae, including ‘Neottiophilidae’ and ‘Thyreophoridae’ (Diptera: Schizophora). Mem Entomol Soc Can 103:1–66 Olea PP, Mateo-Toma´s P (2009) The role of traditional farming practices in ecosystem conservation: The case of transhumance and vultures. Biol Conserv 142:1844–1853 Panzer GWF (1798) Faunae Insectorum Germaniae oder Deutschlands Insecten H. 54(1794). Nu¨rnberg Paramonov SJ (1954) Notes on Australian Diptera (XIII–XV). Ann Mag Nat Hist 7:275–297
753 Rı´os T (1902) Los insectos y la putrefaccio´n de los cada´veres (III– IV). La Cı´nica Moderna 1(4):171–180 Robineau-Desvoidy JB (1830) Essai sur les myodaires. Me´m Pre´sente´s par divers savans a` l’Acade´mia Royale des Sciences des l’Institut de France 2:1–813 Robineau-Desvoidy JB (1842) Note sur le Thyreophora cynophila. Ann Soc Entomol Fr 10:273 Ruiz M, Ruiz JP (1986) Ecological history of transhumance in Spain. Biol Conserv 37:73–86 Van Wieren SE (1995) The potential role of large herbivores in nature conservation and extensive land use in Europe. Biol J Linn Soc 56(Suppl):11–23 Vanpoucke S, Bourguignon L, Braet L, Dupont E, Raes D, Hubrecht F (2010) When death is life—Ecology, nature conservation, and forensic entomology. In: Proceedings of the 8th meeting of the European association for forensic entomology (Suppl.), Murcia, p 17
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