Introduction
The grey partridge belongs to the class Aves, order Galliformes, genus Perdix and family Phasianidae. The grey partridge Perdix perdix is an autochthon species in Serbia, and inhabits most of the European territory, from Sweden to Mediterranean, and from Spain deep into the Asian continent (Bro et al., Reference BRO, SARRAZIN, CLOBERT and REITZ2000; Aebischer and Ewald, Reference AEBISCHER and EWALD2004; Kuijper et al., Reference KUIJPER, OOSTERVELD and WYMENGA2009). It prefers plains with smaller fields planted with grains, such as wheat, barley, millet, maize, alfalfa and beet. Adult partridges feed on insects and other invertebrate, waste seeds and greens, while chicks need about 95 to 98% of the diet as animal proteins (Borg and Toft, Reference BORG and TOFT2000). Partridges never damage field crops. Miscellaneous seeding structure provides plentiful feed and also a good covert from predators (Browne et al., Reference BROWNE, AEBISCHER, MOREBY and TEAGUE2006). In the past, sugar beet has been planted nearby ranches, because poultry, particularly guineafowl, turkeys and partridges efficiently remove the sugar beet weevil Bothynoderes punctiventris Germ. and the flea beet Chaetocnema tibialis Illig. In this paper the relationship between the use of pesticides and grey partridge poisoning mainly due to the irregular use of rodent baits is reviewed. The aim of this review is to emphasise the existing problem of partridge extinction and how it would impact the agriculture ecology.
Population trends of the grey partridge
The grey partridge used to be widespread in agricultural areas throughout Europe however today it is considered a rare bird (Kuijper et al., Reference KUIJPER, OOSTERVELD and WYMENGA2009). Due to the improper and overuse of insecticide preparations, the grey partridge has become almost extinct from Serbian plains, as well as from numerous countries across Europe (Figala et al., Reference FIGALA, PRCHALOVA and TESTER2001; Taylor et al., Reference TAYLOR, MAXWELL and BOIK2006). Small quantities of ingested poisonous substances by insect feeding causes decreased growth and/or weakening to partridges and they therefore become an easy target for predators (Watson et al., Reference WATSON, AEBISCHER, POTTS and EWALD2007; Kapetanov et al., 2012). In winter, rodent baits made of grains coated with zinc phosphide, thalium sulphate or carbonfuranes are used to prevent damage to field crops. Mass intoxications of starved partridges were frequent when such baits were improperly set on the ground (Kapetanov et al., 2012). In long term surveys on partridge populations in Europe, such as in Poland, Great Britain and Hungary (Panek, Reference PANEK2005; Báldi and Faragó, Reference BÁLDI and FARAGÓ2007) a continuous decrease in partridge numbers has been observed. Changes in the landscape and transformation of native land into arable land, the modernisation of agriculture including hard mechanisation and the intensive use of pesticides have all contributed to the rapid decline of partridge populations, to the point of extinction (Šálek et al., Reference ŠÁLEK, MARHOUL, PINTÍŘ, KOPECKÝ and SLABÝ2004; Wubbenhorst and Leuschner, Reference WUBBENHORST and LEUSCHNER2006). The average rate of population decline in the period from 1990 to 2000 was approximately 30% and ranged from 1 to 80% (Birdlife International, 2004). In contrast, in Russia and the Czech Republic, the number of partridges showed an increasing trend (Kuijper et al., Reference KUIJPER, OOSTERVELD and WYMENGA2009).
Pesticide poisoning of grey partridges
The improper setting of baits, in many cases randomly on field surfaces, poses a great threat to game. A lethal outcome five hours after the consumption of only a dozen treated grains has been seen in pheasants (Novotny et al., Reference NOVOTNY, MISIK, KOZLOVA, ONDRACEK, KUCA, VAVRA and RACHAC2011). In the past few decades, cases of both sporadic and mass poisoning of domestic and wild animals have been reported. The use of carbamate pesticides and organochlorine insecticides has predominantly influenced the decrease of partridges (Wobeser et al., Reference WOBESER, BOLLINGER, LEIGHTON, BLAKLEY and MINEAU2004; Novotny et al., Reference NOVOTNY, MISIK, KOZLOVA, ONDRACEK, KUCA, VAVRA and RACHAC2011) and other game fowl (Berny, Reference BERNY2007; Wang et al., Reference WANG, KRUZIK, HELSBERG, HELSBERG and RAUSCH2007; Berny and Gaillet, Reference BERNY and GAILLET2008). In the retrospective study by Novotny et al. (Reference NOVOTNY, MISIK, KOZLOVA, ONDRACEK, KUCA, VAVRA and RACHAC2011), a total of 181 cases of poisoning in wild animals including partridges were analysed. The authors found that the most frequent cause of poisoning was consumption of insects, carcasses or rodent baits, all previously exposed to carbamate pesticides and organochlorine insecticides. It seems such cases represent mostly collateral damage to intensive agriculture (Kapetanov et al., 2012; Mihaljev et al., 2012). Some studies suggest that today partridges are better adjusted to arable fields compared to other game fowl, however they are rarely seen in this habitat. However, Henderson et al. (Reference HENDERSON, RAVENSCROFT, SMITH and HOLLOWAY2009) proposed more selective and a reduced use of pesticides in agriculture as a realistic means to reintroduce partridge into nature. Gabriel et al. (Reference GABRIEL, CARVER, DURHAM, KUNIN, PALMER, SAIT, STAGL and BENTON2009) suggested redirect activities towards organic food production. Kuijper et al. (Reference KUIJPER, OOSTERVELD and WYMENGA2009) stated that the increased pesticide use may have caused direct effects on partridges by poisoning birds, or indirect effects through killing their food. Furthermore, the mentioned authors noted that the reported number of cases that can be attributed to direct effects is relatively small, and indirect effects seem to play a much more important role.
Clinical signs and pathological lesions of pesticide poisoning in grey partridge
Kapetanov et al. (2012) reported that dead partridges were found on fields in close proximity to baits, with prostrated necks, outstretched legs and wide spread wings, indicating poisoning with intra vitam signs of neural excitation (Johnston et al.,1994). The death time was estimated to be less than five hours after bait consumption. Section findings were similar in all 39 carcasses. Due to excitation, mechanical disruption of skeletal muscles was present, particularly on breast muscles. Ingluvial and stomach contents consisted of green masses of alfalfa or wheat, with coloured barley and wheat grains. The colour of grains varied between grey and bright red. Hyperemic capillaries were found on the meninges of the cerebrum and cerebellum.
Qualitative and quantitative analysis of rodent baits (treated seed), the ingluvial and stomach contents of dead birds, for detecting the presence of pesticides is performed by using gas chromatography-mass spectrometry (GC-MS) methods (Poppenga et al., Reference POPPENGA, ZIEGLER, HABECKER, SINGLETARY, WALTER and MILLER2005; Reljić et al., Reference RELJIĆ, SREBOČAN, HUBER, KUSAK, ŠURAN, BRZICA, CUKROV and CRNIĆ2012).
Conclusions
The described cases of poisoning in partridges indicate that only trained personnel should select and allocate rodent baits and these personnel need to have a good insight and knowledge of local fauna. The locations and time schedule of actions to control rodent populations need to be available beforehand to local communities, game associations and societies for ecology and nature preservation. The complete exclusion of pesticides from intensive agriculture is not realistic, although it is possible to selectively reduce their use. The free and illegal trade of poisonous substances must be suppressed, particularly carbofuran, since it is banned from production. The introduction of organic agriculture is one of the most promising measures to increase the partridge population. Lower concentrations or the absence of residual pesticides in the environment would elicit repopulation of not only partridges as a biological regulator of insects on crop fields, but also other predators important for vermin control in the ecosystem.
Acknowledgments
This research was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (ТР31084).